International Journal of Systematic and Evolutionary Microbiology (2016), 66, 9–37 DOI 10.1099/ijsem.0.000702

Review Review of the taxonomy of the genus Arthrobacter, emendation of the genus Arthrobacter sensu lato, proposal to reclassify selected species of the genus Arthrobacter in the novel genera Glutamicibacter gen. nov., Paeniglutamicibacter gen. nov., Pseudoglutamicibacter gen. nov., Paenarthrobacter gen. nov. and Pseudarthrobacter gen. nov., and emended description of Arthrobacter roseus

Hans-Ju¨rgen Busse

Correspondence Institute of Microbiology, Department of Pathobiology, University of Veterinary Medicine Vienna, Hans-Ju¨rgen Busse Veterina¨rplatz, 1A-1210 Vienna, Austria hans-juergen.busse@ vetmeduni.ac.at In this paper, the taxonomy of the genus Arthrobacter is discussed, from its first description in 1947 to the present state. Emphasis is given to intrageneric phylogeny and chemotaxonomic characteristics, concentrating on quinone systems, peptidoglycan compositions and polar lipid profiles. Internal groups within the genus Arthrobacter indicated from homogeneous chemotaxonomic traits and corresponding to phylogenetic grouping and/or high 16S rRNA gene sequence similarities are highlighted. Furthermore, polar lipid profiles and quinone systems of selected species are shown, filling some gaps concerning these chemotaxonomic traits. Based on phylogenetic groupings, 16S rRNA gene sequence similarities and homogeneity in peptidoglycan types, quinone systems and polar lipid profiles, a description of the genus Arthrobacter sensu lato and an emended description of Arthrobacter roseus are provided. Furthermore, reclassifications of selected species of the genus Arthrobacter into novel genera are proposed, namely Glutamicibacter gen. nov. (nine species), Paeniglutamicibacter gen. nov. (six species), Pseudoglutamicibacter gen. nov. (two species), Paenarthrobacter gen. nov. (six species) and Pseudarthrobacter gen. nov. (ten species).

The genus Arthrobacter was proposed by Conn & Dimmick Arthrobacter Fischer, emend. (1947) to encompass three species, including the type species Morphology. Varied, with a tendency to go through a of the genus, ‘Arthrobacter globiforme’. The type species was more or less definite life cycle, the most characteristic later renamed as Arthrobacter globiformis (Skerman et al., features of which are Gram-negative rods in young 1980); the second species, Arthrobacter tumescens,wasreclas- cultures and Gram-positive coccoid forms (arthros- sified in another genus (Collins et al., 1989; Manaia et al., pores?) in old cultures, with intermediate stages that 2004), and the third species, ‘Arthrobacter helvolum’, was may be clubs, branched forms, or short unbranched never mentioned again in a taxonomic paper. It has to be filaments. Large (1 to 2 m) spherical bodies are some- emphasized here that it was not reclassified as ‘Pseudoclavi- times observed which have been termed ‘cystites’. bacter helvolum’, as stated by Busse et al. (2012). Originally, the genus was described as follows: Cultural characteristics. Growth on surface of solid media soft and smooth, not dry and wrinkled or hard and leathery, as ordinarily in Mycobacterium Abbreviations: DGDG, digalactosyldiacyglycerol; DMDG, dimannosyl- and the Actinomycetoceae. Colonies on poured diacylglycerol; DMG, dimannosylglyceride; DPG, diphosphatidylglycerol; plates ordinarily small (punctiform). Growth in MDMMG, monoacyldimannosylmonoacylglycerol; MGDG, monogalacto- broth usually slow and never profuse. syldiacylglycerol; PE, phosphatidylethanolamine; PG, phosphatidyl- glycerol; PI, phosphatidylinositol; TeMDG, tetramannosyldiacylglycerol; Physiology. Can ordinarily use either ammonium salts TMDG, trimannosyldiacylglycerol. or nitrates as sole sources of nitrogen. Can utilize

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glucose and sometimes other sugars as sources of cells are Gram-positive but may be weakly so. Not carbon and energy, but ordinarily without producing acid-fast. sufficient quantities of acid to have appreciable effect The cell walls do not contain both meso-diaminopime- on the pH of highly buffered media (e.g. containing lic acid and arabinose. peptone). Gelatin usually slowly liquefied. Ordinarily cause blackening of Mueller’s tellurite agar. Chemoorganotrophs: Metabolism respiratory, never fermentative. Molecular oxygen is the term- Habitat. Primarily soil. inal electron acceptor. Type species. A. globiforme (Conn) Conn and Dimmick. Little or no acid is produced from glucose in peptone Concerning the description of the genus Arthrobacter,the medium. Do not attack cellulose. Catalase-positive. Approved Lists of Bacterial Names (Skerman et al.,1980) All species grow in a medium containing soil extract refer to Keddie (1974), which concentrates on cultural, mor- and yeast extract. Nutrient agar (peptone+meat phological and physiological characteristics. This description extract) is suitable for laboratory strains which do has been the basis for the classification of numerous novel not require terregens factor or vitamin B but may species of the genus Arthrobacter: 12 be inhibitory to newly isolated strains (Topping, 1937). Cells which in complex medium undergo a marked Strict aerobes. change in form during the growth cycle. Older cul- tures (generally 2–7 days) are composed entirely or Temperature optimum 20–30 8C; most strains grow largely of coccoid cells. In some strains the coccoid at 10 8C but usually not at 37 8C. Do not survive cells are uniform in size and spherical, and resemble heating at 63 8C for 30 min in skim milk. Grow micrococci; in others they are spherical to ovoid or best at a neutral to slightly alkaline pH. slightly elongate. In some cultures larger coccoid The G+C content of the DNA of the species exam- cells some 2–4 times the size of the remainder may ined ranges from ca. 60–72 moles %(T ). occur; these may predominate under some cultural m conditions. On transfer to fresh complex medium Type species: Arthrobacter globiformis (Conn) Conn growth occurs by enlargement (swelling) of the coc- and Dimmick 1947, 301. coid cells followed by elongation from one or By 1995, the following 16 additional species, that have not occasionally two parts of the cell to give rods which been reclassified in other genera to date, were assigned to usually have a diameter less than that of the enlarged the genus Arthrobacter, considering the genus descriptions coccoid cell (referred to a figure). In the larger coccoid given by either Conn & Dimmick (1947) or Keddie (1974): cells outgrowth may occur at two, three or rarely four Arthrobacter aurescens Phillips1953, Arthrobacter citreus parts of the cell (referred to a figure). In both cases sub- Sacks 1954, Arthrobacter crystallopoietes Ensign and Ritten- sequent growth and division give rise to irregular rods berg, 1963, Arthrobacter histidinolovorans Adams 1954, which vary considerably in size and shape and include Arthrobacter ilicis Collins et al. 1982a, Arthrobacter mysorens straight, bent and curved, wedge-shaped and club- Nand and Rao 1972, Arthrobacter nicotianae Giovannozzi- shaped forms (referred to a figure). A proportion of Sermanni 1959, Arthrobacter nicotinovorans Kodama et al. the rods are arranged at an angle to each other giving 1992, Arthrobacter oxydans Sguros 1954, Arthrobacter pascens V formations but more complex angular arrangements Lochhead and Burton 1953, Arthrobacter polychromogenes often occur. Post-fission outgrowths, usually from the Schippers-Lammertse et al. 1963, Arthrobacter protophormiae proximal ends of one or both cells of a pair of rods (Lysenko 1959) Stackebrandt et al. 1984, Arthrobacter ramosus (referred to a figure), and bud-like outgrowths from Jensen 1960, Arthrobacter sulfureus Stackebrandt et al. 1984, segments of septate rods (referred to a figure), especially Arthrobacter uratoxydans Stackebrandt et al. 1984 and Arthro- in richer media, may give the appearance of rudimen- bacter ureafaciens (Krebs and Eggleston 1939) Clark 1955. tary branching but true mycelia are not formed. As the exponential phase proceeds the rods become shorter With the reclassification of Micrococcus agilis in the genus and are eventually replaced by the coccoid cells charac- Arthrobacter as Arthrobacter agilis, the description of teristic of stationary phase cultures (referred to a the genus Arthrobacter was emended as follows (Koch et al., figure). The coccoid cells are formed either by a gradual 1995): shortening of the rods at each successive division or, ‘a marked rod-coccus growth cycle occurs during especially in richer media, by multiple fragmentation growth in complex media; stationary-phase cultures of larger rods (referred to a figure). The rods are non- (generally after 2 to 7 days) are composed entirely motile or motile by one subpolar or a few lateral fla- or largely of coccoid cells that are 0.6 to 1.0 mmin gella. Do not form endospores. diameter; one species forms only spherical cells.’ Gram-positive. However, the rods may be readily Another 51 species of the genus Arthrobacter have since been decolorized and may show only Gram-positive described, including four novel species assigned to the genus granules in otherwise Gram-negative cells. Coccoid since 2012, namely Arthrobacter cryoconiti (Margesin et al.,

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2012), Arthrobacter cupressi (Zhang et al., 2012), Arthrobacter from gene banks, multiply aligned using CLUSTAL_X siccitolerans (SantaCruz-Calvo et al., 2013) and Arthrobacter (Thompson et al., 1997) and edited manually to remove gyeryongensis (Hoang et al., 2014). However, none of these gaps and ambiguous nucleotides using BioEdit (Hall, descriptions considered the phylogenetic and chemotaxo- 1999). Phylogenetic calculations were carried out applying nomic heterogeneities found among species of the genus the maximum-likelihood, maximum-parsimony and neigh- Arthrobacter that have been known for some decades (Fiedler, bour-joining algorithms implemented in the PHYLIP package 1971; Schleifer & Kandler, 1972; Stackebrandt et al., 1983, 1988; (Felsenstein, 2009). Confidence levels of branchings were Collins et al., 1982b; Collins & Kroppenstedt, 1983; Koch et al., determined by bootstrap analysis implemented in the 1994). More often than not, novel species were described PHYLIP package. The results from phylogenetic calculations as members of the genus only when an established species carried out in the present study, including all established of the genus Arthrobacter was identified as the nearest species of the genus Arthrobacter and the type species of relative, the peptidoglycan was shown to contain the other members of the family Micrococcaceae,applyingthe diagnostic diamino acid lysine and a rod–coccus life cycle maximum-likelihood algorithm, are shown in Fig. 1. In was observed. this tree, only the branching of a few major lines is sup- ported by high bootstrap values or by the same branching At the time of writing, the genus Arthrobacter contains 70 order in the maximum-parsimony and neighbour-joining species, including Arthrobacter viscosus, which is obviously algorithms. One of these sublines is designated the ‘Arthro- misnamed, because it shares the highest 16S rRNA gene bacter protophormiae group’, comprising the species Arthro- sequence similarity with members of the genus Rhizobium bacter creatinolyticus, Arthrobacter soli, A. protophormiae, such as Rhizobium gallicum (98.1 % 16S rRNA gene A. uratoxydans, A. nicotianae, Arthrobacter arilaitensis, A. sequence similarity to the type strain), Rhizobium mongo- mysorens, Arthrobacter bergerei and Arthrobacter ardleyensis. lense (98.0 %) and Rhizobium leguminosarum (97.6 %) Within this subline, close relatedness is suggested from a (Heyrman et al., 2005). This affiliation is in agreement relatively high bootstrap value between A. ardleyensis and with chemotaxonomic traits of this species, including its A. bergerei. The second subline, designated the ‘Arthrobacter quinone system (ubiquinone Q-10 predominant), fatty psychrolactophilus group’, embraces the species Arthrobacter acid profile (hydroxy fatty acids present, C18 : 1 and alpinus, A. cryoconiti, Arthrobacter psychrochitiniphilus, C19 : 0 cyclo predominant) and a polar lipid profile that Arthrobacter livingstonensis, Arthrobacter stackebrandtii and suggests the presence of phosphatidylethanolamine (PE), Arthrobacter psychrolactophilus, and several internal nodes monomethylethanolamine, phosphatidylglycerol (PG), are supported by high bootstrap values. The third subline diphosphatidylglycerol (DPG) and phosphatidylcholine is designated the ‘Arthrobacter agilis group’ and contains (Collins, 1986). Phylogenetic analyses employing the the species Arthrobacter flavus, A. agilis, Arthrobacter subter- neighbour-joining algorithm and embracing the vast raneus, Arthrobacter tecti, Arthrobacter tumbae and Arthro- majority of species of the genus Arthrobacter (Ding et al., bacter parietis. High bootstrap support suggests that the 2009; Ganzert et al., 2011; Yassin et al., 2011b; Margesin latter four species form the stable core of the group. et al., 2012) do not indicate a stable internal structure of A fourth subline comprises A. citreus, Arthrobacter luteolus, the genus. This is indicated by the fact that many branching Arthrobacter koreensis and Arthrobacter gandavensis. nodes are not supported by high bootstrap values (.70 %) A deeply branching subline designated the ‘Arthrobacter and numerous nodes were not found with the maximum- albus/cumminsii group’ comprises the species Arthrobacter likelihood or maximum-parsimony algorithm. Further- albus and Arthrobacter cumminsii. A rather stable branching more, certain species occupy varying positions in different position within the tree suggests a close relatedness between trees, including A. crystallopoietes, Arthrobacter nasiphocae, the pairs of species Arthrobacter niigatensis/Arthrobacter Arthrobacter roseus, Arthrobacter russicus, Arthrobacter san- defluvii, Arthrobacter gangotriensis/Arthrobacter antarcticus, guinis and Arthrobacter woluwensis. However, it is worth Arthrobacter castelli/Arthrobacter pigmenti and Arthrobacter mentioning that the latter species always occupies a oryzae/Arthrobacter humicola. It has to be mentioned here rather deeply branching subline in all trees, often loosely that the latter two species can be considered to be the nearest associated with the ‘Arthrobacter sulfureus group’ (Fig. 1). relatives of A. pascens and A. globiformis (the type species of When representatives of additional members of the the genus), with which they also share .98 % 16S rRNA family Micrococcaceae are included in tree reconstructions gene sequence similarity, and the common branching node in addition to species of the genus Arthrobacter (Busse is also found with a second treeing algorithm (Fig. 1). The et al., 2012), the phylogenetic relationships become more representatives of the ‘Arthrobacter pigmenti group’, the unclear. In this maximum-likelihood tree (Busse et al., ‘Arthrobacter citreus group’ and the ‘A. albus/cumminsii 2012), several representatives of other genera branch group’ and A. russicus, A. nasiphocae and A. crystallopoietes within the radiation of established species of the genus are most distantly related to the type species of the genus Arthrobacter, indicating that the genus is not monophyletic. and, apparently, more closely related to other members of the In order to examine the phylogenetic arrangements within family Micrococcaceae. Rather separate positions within the the genus Arthrobacter, including the most recently tree are occupied by A. woluwensis and A. sanguinis.Theexist- described species, 16S rRNA gene sequences were extracted ence of these major sublines is also shown in other phylogenetic

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Arthrobacter nasiphocae M597/99/10T (AJ292364) T Microbacterium lacticum DSM 20427 (X77441) T Kocuria rosea DSM 20447 (X87756) T Nesterenkonia halobia DSM 20541 (X80747) T Citricoccus muralis 4-0 (AJ344143) T Micrococcus luteus NCTC 2665 (CP001628) T Sinomonas flava CW 108 (EU370704) Arthrobacter monumenti LMG 19502T (AJ315070 Arthrobacter castelli LMG 22283T (AJ639826) ‘Arthrobacter pigmenti group’ 98 Arthrobacter pigmenti LMG 22284T (AJ639827) T Auritidibacter ignavus IMMIB L-1656 (FN554542) 88 T Yaniella halotolerans YIM 70085 (AY228479) Arthrobacter cumminsii DMMZ 445T (X93354) 100 Arthrobacter albus CF43T (AJ243421) ‘Arthrobacter albus/cumminsii group’ Arthrobacter crystallopoietes DSM 20117T (X80738) T Rothia dentocariosa ATCC 17931 (M59055) T Zhihengliuella halotolerans YIM 70185 (DQ372937) Arthrobacter woluwensis DSM 10495T (X93353) Arthrobacter sulfureus DSM 20167T (X83409) Arthrobacter cryotolerans LI3T (GU784867) Arthrobacter gangotriensis Lz1yT (AJ606061) 84 Arthrobacter antarcticus SPC26T (AM931709) ‘Arthrobacter sulfureus group’ Arthrobacter kerguelensis KGN15T (AJ606062) Arthrobacter psychrophenolicus AG31T (AJ616763) Arthrobacter protophormiae DSM 20168T (X80745) Arthrobacter creatinolyticus GIFU 12498T (D88211) Arthrobacter soli SYB2T (EF660748) Arthrobacter mysorens DSM 20647T (X83410) T Arthrobacter nicotianae DSM 20123 (X80739) ‘Arthrobacter protophormiae group’ 62 Arthrobacter arilaitensis CIP 108037T (AJ609628) Arthrobacter uratoxydans DSM20647T (X83410) 99 Arthrobacter bergerei CIP 108036T (AJ609630) Arthrobacter ardleyensis An25T (AJ551163) Arthrobacter halodurans JSM 078085T (EU583729) Arthrobacter rhombi F98.3HR69T (Y15885) 95 Arthrobacter humicola KV653T (AB279890) Arthrobacter oryzae KV651T (AB279889) T ‘Arthrobacter sensu stricto’ Arthrobacter globiformis DSM 20124 (M23411) Arthrobacter pascens DSM20545T (X80740) Arthrobacter sanguinis CCUG 46407T (EU086805) T Arthrobacter phenanthrenivorans Sphe3 (AM176541) ‘Arthrobacter oxydans group’ Arthrobacter chlorophenolicus A6T (CP001341) Arthrobacter methylotrophus TGAT (AF235090) Arthrobacter ramosus CCM 1646T (AM039435) Arthrobacter gyeryongensis DCY72T (JX141781) ‘Arthrobacter Arthrobacter alkaliphilus LC6T (AB248527) oxydans group’ Arthrobacter equi IMMIB L-1606T (FN673551) Acaricomes phytoseiuli DSM 14247T (AJ812213) Arthrobacter ilicis DSM 20138T (X83407) Arthrobacter nitroguaiacolicus G2-1T (AJ512504) Arthrobacter aurescens DSM 20116T (X83405) Arthrobacter ureafaciens DSM 20126T (X80744) ‘Arthrobacter aurescens group‘ Arthrobacter histidinolovorans DSM 20115 (X83406) Arthrobacter nicotinovorans DSM 420T (X80743) T Arthrobacter cupressi D48 (HQ657321) ‘Arthrobacter sensu stricto’? Arthrobacter defluvii 4C1-aT (AM409361) 60 Arthrobacter niigatensis LC4T (AB248526) Arthrobacter polychromogenes DSM 20136T (X80741) ‘Arthrobacter oxydans group’ Arthrobacter scleromae YH-2001T (AF330692) Arthrobacter oxydans DSM 20119T (X83408) Arthrobacter sulfonivorans ALLT (AF235091) Arthrobacter roseus CMS90rT (AJ278870) Arthrobacter siccitolerans 4J27T (GU815139) ‘Arthrobacter oxydans group’ Arthrobacter livingstonensis LI2T (GQ406811) T 99 Arthrobacter cryoconiti Cr6-08 Cr6-08 (GQ784867) Arthrobacter alpinus S6-3T (GQ227413) 92 T ‘Arthrobacter psychrolactophilus group’ 71 Arthrobacter stackebrandtii CCM 2783 (AJ640198) Arthrobacter psychrolactophilus JCM 13874T (AB588633) Arthrobacter psychrochitiniphilus GP3T (AJ810896) T Renibacterium salmoninarum ATCC 33209 (CP000910) 82 Arthrobacter russicus GTC 863T (AB071950) Arthrobacter flavus JCM 11496T (AB299278) 94 Arthrobacter agilis DSM 20550T (X80748) Arthrobacter subterraneus CH7T (DQ097525) Arthrobacter tumbae LMG 19501T (AJ315069) ‘Arthrobacter agilis group’ 77 Arthrobacter parietis LMG 22281T (AJ639830) Arthrobacter tecti LMG 22282T (AJ639829) Arthrobacter citreus DSM 20133T (X80737) Arthrobacter luteolus CF25T (AJ243422) 88 Arthrobacter koreensis CA15-8T (AY116496) ‘Arthrobacter citreus group’ 72 Arthrobacter gandavensis R5812T (AJ316140)

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Fig. 1. Maximum-likelihood tree based on 16S rRNA gene sequences (1224 nt). The 16S rRNA gene sequence of Micro- bacterium lacticum DSM 20427T was used as an outgroup. Bootstrap values .60 based on 100 replicates are given at nodes. Bar, 0.1 substitutions per nucleotide position. The names of groups of the genus Arthrobacter, as defined by Busse et al. (2012), are provided in shaded rectangles. Filled squares indicate that the same branching node with bootstrap support .60 % was found after analyses using the maximum-parsimony and neighbour-joining algorithms. Open circles indicate that the same branching node with bootstrap support .60 % was found after analyses using either the maximum-parsimony or neighbour-joining algorithm. Type species of genera are shown in bold face.

analyses, even though the complete set of species of the genus (360 bases), they showed that the reference species were sep- Arthrobacter was not always included in these calculations arated into at least six groups. These authors could also show (Ganzert et al., 2011; Busse et al., 2012; Zhang et al., 2012). that the 16S rRNA gene and recA phylogenies were well in accordance with each other. Reanalysis of the recA-based In a study on the diversity of isolates of the genus Arthro- phylogeny including sequences of type strains of species of bacter from terrestrial deep-subsurface sediments, van the genus Arthrobacter from van Waasbergen et al. (2000) Waasbergen et al. (2000) also investigated the recA phylo- supplemented with additional sequences since available geny of their isolates in relation to 12 established species from gene banks supported the earlier study (Fig. 2), and of the genus. On the basis of a fragment of the recA gene is also in agreement with the 16S rRNA gene-based

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Microbacterium lacticum DSM 20427T (AM181522) Micrococcus terreus NBRC 104258T (FR83795) Arthrobacter ureafaciens ATCC 7562T (AAF25429) Arthrobacter aurescens ATCC 13344T (AF214793) Arthrobacter histidinolovorans ATCC 11442T (AF214788) 94 Arthrobacter nicotinovovorans ATCC 49919T (AAF25431) Arthrobacter phenanthrenivorans Sphe3T (AM931439) 73 Arthrobacter oxydans ATCC 14358T (AAF25436) 64 66 Arthrobacter polychromogenes ATCC 15216 (AF214785) Arthrobacter chlorophenolicus A6T (CP001341) Arthrobacter pascens ATCC 13346T (AF214786) Arthrobacter globiformis ATCC 8010T (AF214780) Arthrobacter agilis ATCC 966T (AF214779) Arthrobacter citreus ATCC 11624T (AF214781) Arthrobacter gangotriensis Lz1yT (EMQ97464) 69 Arthrobacter sulfureus ATCC 19098T (AF214787) Arthrobacter uratoxydans ATCC 21749T (AF214791) 99 Arthrobacter nicotianae ATCC 15236T (AF214792) Arthrobacter protophormiae ATCC 19271T (AF214790) Arthrobacter arilaitensis RE117t (FQ311875) Micrococcus flavus DSM 19079T (FR83795) 91 Micrococcus endophyticus DSM 17945T (FR837952) 63 Micrococcus luteus NCTC 2665T CP001628 96 Micrococcus yunnanensis DSM 21948T (FR837954) Micrococcus cohnii WS4601T (FR832427) Micrococcus lylae ATCC 27566T (AF214778)

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Fig. 2. Maximum-likelihood tree based on recA gene sequences (381 nt). The corresponding gene sequence of Microbacter- ium lacticum DSM 20427T was used as outgroup. Bootstrap percentages .60 % based on 200 replicates are given at nodes. Bar, 0.1 substitutions per nucleotide position.

phylogeny (Fig. 1). With the exception of Arthrobacter All species of Arthrobacter analysed contain the diagnostic chlorophenolicus, all species were grouped in accordance diamino acid lysine, and the peptidoglycan type of arthro- with their 16S rRNA gene-based phylogeny. A. uratoxydans, bacters is either A3a (only monocarboxylic amino acids A. arilaitensis, A. protophormiae and A. nicotianae form one present in the interpeptide chain) or A4a (dicarboxylic clade corresponding to the ‘A. protophormiae group’. amino acids present in the interpeptide chain), as defined Another clade is formed by A. aurescens, A. ureafaciens, by Schleifer & Kandler (1972). However, additional differ- A. histidinolovorans and A. nicotinovorans, all assigned to ences occur in the presence of amino acids in the cross- the ‘Arthrobacter aurescens group’. A third clade is formed linking interpeptide chain of both peptidoglycan types a a by Arthrobacter phenanthrenivorans, A. oxydans and A3 and A4 (Table 1). To some extent, these amino A. polychromogenes, which are members of the ‘Arthrobacter acid compositions reflect relatedness as indicated by 16S oxydans group’. Within this tree, species of the genus rRNA gene sequence analyses. Where analysed, the amino Micrococcus represent the deepest branching line of descent. acids of the interpeptide chain usually occur in the L-form. Among species that show the A3a peptidoglycan Chemotaxonomically, members of the genus Arthrobacter type, the interpeptide chain is composed of either Lys– are rather diverse with respect to peptidoglycan structure, Ala1–4, Lys–Ala–Thr–Ala, Lys–Ser–Thr–Ala, Lys–Thr–Ala1–3, and differences in the quinone system and polar lipid pro- Lys–Ala–Ser–Ala3 (only found in species of Arthrobacter files are also observed. reclassified in the genus Sinomonas and in Arthrobacter

Downloaded from www.microbiologyresearch.org by http://ijs.microbiologyresearch.org 13 IP: 54.70.40.11 On: Mon, 04 Feb 2019 19:10:17 H.-J. Busse 95.5 % clade- 97.0 % clade- 97.5 % clade- 96.2 % 97.0 % clade 97.0 % 97.5 % 98.0 % 97.0 % clade- 97.2 % clade- 99 % clade- $ forming . forming Intragroup 16S rRNA gene sequence similarity . forming . . forming . . . . forming . forming . forming ) ) ) ) ) ) ) ) (2012) 2 2 2 2 2 2 2 2 et al. ) indicates that one isoprenoic unit MK-9 MK-10 Quinone system MK-9(H MK-9(H MK-9(H MK-9(H MK-9(H MK-8(H 2 1–3 2–3 2–3 4 1–4 2–3 Lys–Ala–Glu MK-8 and/or interpeptide bridge or Lys–Ala or Lys–Ala Lys–Ala–Glu or Lys–Ser–Glu Lys–Thr–Ala group’ Lys–Ala group’ Lys–Ala–Thr–Ala MK-9(H group’ Lys–Glu MK-8, MK-9 or group’ Lys–Ala–Ser–Ala group’ Lys–Ser–Thr–Ala MK-9(H group’ Lys–Ser–Ala group’ cumminsii group’ Lys–Thr–Ala / A. protophormiae A. albus A. sulfureus A. aurescens A. pigmenti A. globiformis Sinomonas A. agilis A. citreus A. psychrolactophilus A. oxydans group’ ‘ Group designation Peptidoglycan ‘ ‘ ‘ group’ ‘ ‘ group’ 2 2–3 1–4 Peptidoglycan interpeptide bridge designation Group VI Lys–Ala–Glu ‘ Group VII Lys–Glu ‘ Group IIGroup IIIGroup IV Lys–Ala–Thr–Ala Lys–Ala ‘ Lys–Ser–Ala Group I Lys–Ser–Thr–AlaGroup ‘ V Lys–Thr–Ala D Absent Arthrobacter ) Present ‘ 2 MK-9(H MK-8 and MK-9, MK-9 or MK-9 and MK-10 (1986) Komagata & Suzuki (1987) Busse et al. ) 2 or Lys– (1986). (1983). 1–4 et al. et al. (1986). or Lys–Ser–Thr– (Lys–Ala–Glu or (Lys–Ala et al. 2–3 a a (1983) and Keddie Peptidoglycan type Quinone system PI* Group Ala–Thr–Ala or Lys–Ser– Ala Lys–Glu) A4 Ala or Lys–Thr–Ala A3 et al. / d Overview of groupings within the genus or or group’ d D D A. globiformis A. nicotianae Group designation ‘ citreus ‘Globiformis’ group Stackebrandt ‘ group’ ‘Nicotianae’ group According to Stackebrandt According to Keddie Only considered by Keddie is dihydrogenated. D d Table 1. In the descriptions of the quinone system, MK-8, MK-9 and MK-10 indicate a menaquinone with eight, nine and ten isoprenoic units in the side chain and (H *

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castelli), Lys–Ala2–Gly2–3–Ala(Gly) (only reported for nutritional and other differences) or Arthrobacter sensu A. nasiphocae; Collins et al., 2002a) or Lys–Gly–Ala3 (only stricto, including the species Sinomonas atrocyanea (formerly reported for A. roseus;Reddyet al., 2002). Peptidoglycan Arthrobacter atrocyaneus), A. aurescens, A. crystallopoietes, A4a variations detected in arthrobacters are Lys–Ala–Glu, A. globiformis, A. histidinolovorans, A. ilicis (formerly Lys–Glu, Lys–Ser–Glu (only reported for A. cumminsii; Corynebacterium ilicis), A. nicotianae, A. oxydans, A. pascens, Funke et al., 1996), Lys–Ala–D-Glu (only reported for A. polychromogenes, A. ramosus, A. sulfureus (formerly Arthrobacter rhombi;Osorioet al., 1999) or Lys–D-Asp ‘Brevibacterium sulfureum’), A. ureafaciens and A. citreus. (only reported for A. woluwensis;Funkeet al., 1996). The The second group, designated the ‘simplex/tumescens’ quinone system of the majority of species of Arthrobacter group, comprised the species Pimelobacter simplex (formerly contains predominantly the monosaturated menaquinone Arthrobacter simplex)andTerrabacter tumescens (formerly MK-9(H2), but a smaller number of established species Arthrobacter tumescens), with LL-diaminopimelic acid as contain the completely unsaturated menaquinones MK-8, the characteristic peptidoglycan diamino acid, a tetrahydro- MK-9 and/or MK-10. Rather unusual quinone systems genated menaquinone with eight isoprenoic acids in the side were reported for Arthrobacter scleromae and A. phenanthre- chain [MK-8(H4)] and a substantially higher DNA G+C nivorans. They are composed of a combination of monosatu- content than those of the ‘globiformis’ group. The major rated and completely unsaturated menaquinones that also characteristics of the third group, represented by Microbac- differinthelengthoftheisoprenoicsidechains.A. scleromae terium terregens (formerly Arthrobacter terregens)andMicro- was reported to contain MK-8(H2) and MK-10 (Huang bacterium flavescens (formerly Arthrobacter flavescens)and et al., 2005), whereas A. phenanthrenivorans contains MK-8 hence designated the ‘terregens/flavescens’group,werethe and MK-9(H2) (Kallimanis et al., 2009). Combinations of presence of ornithine in the peptidoglycan and a DNA completely unsaturated and monosaturated quinones are G+C content higher than that of the type strain of A. glo- well known among the class Actinobacteria, but they usually biformis. Considering these differences, Keddie & Jones share the same length of isoprenoic side chain. Hence, there (1981) stated that the latter two groups should be removed are some reservations about the reproducibility of the qui- from the genus Arthrobacter. none systems of these two species. Stackebrandt et al. (1983) proposed the subdivision of the A fatty acid profile that contains predominantly iso- and species of the genus Arthrobacter into two groups on the anteiso-branched fatty acids with the major compound basis of their heterogeneity with respect to peptidoglycan anteiso-C15 : 0 is common to all species of Arthrobacter. types (A3a or A4a) and quinone systems [menaquinone Usually, relatively large amounts of iso-C , anteiso- 15 : 0 MK-9(H2) or MK-8 and/or MK-9]. Species with monosatu- C and/or iso-C are also present. Some species 17 : 0 16 : 0 rated menaquinone MK-9(H2) and peptidoglycan type A3a may also contain significant amounts of the straight- were placed in the ‘globiformis’ group, including A. globifor- chain fatty acid C16 : 0. Unfortunately, based on the avail- mis, A. oxydans, S. atrocyanea (formerly A. atrocyaneus)and able data, the importance of fatty acid profiles for A. ureafaciens. Species with completely unsaturated menaqui- identification or differentiation of species of Arthrobacter none MK-8 and/or MK-9 and peptidoglycan type A4a were cannot be evaluated. Fatty acid profiles of species of Arthro- placed in the ‘nicotianae’ group, including A. nicotianae, A. bacter have been reported that were analysed from biomass mysorens, A. protophormiae, A. uratoxydans and A. sulfureus. that was grown at different temperatures, with different medium compositions and without indication of the physio- Also based on different quinone systems (monosaturated logical age at which the cells were harvested. Dependence of or completely unsaturated menaquinones) and variations the fatty acid composition in bacteria on cultural conditions in the interpeptide chain of the peptidoglycan (A3a or and physiological age has been known for a long time, as A4a), Keddie et al. (1986) divided the genus into the demonstrated for representatives of different lines of des- ‘A. globiformis/A. citreus group’ [S. atrocyanea (formerly cent, including cyanobacteria, aerobic endospore-formers, A. atrocyaneus), A. aurescens, A. citreus, A. crystallopoietes, enterobacteria and the genera Listeria and Shewanella A. globiformis, A. histidinolovorans, A. ilicis, A. oxydans, (Marr & Ingraham, 1962; Olson & Ingram, 1975; Gill & A. pascens, A. ramosus and A. ureafaciens ]andthe‘A. Suisted, 1978; Bezbaruah et al., 1988; Suzuki & Komagata, nicotianae group’ (A. nicotianae, A. protophormiae, A. ura- 1983; Abu Hatab & Gaugler, 1997; Nichols et al.,2000, toxydans and A. sulfureus)(Table1). 2002), and the importance of standardization of growth A subdivision of the genus Arthrobacter into seven groups conditions and physiological age is also emphasized for (Table 1) was proposed by Komagata & Suzuki (1987) fatty acid-based identification of bacteria (Sasser, 2009). based on the detailed amino acid composition of the Keddie & Jones (1981) discussed the heterogeneity among peptidoglycan interpeptide chain: group I with Lys–Ser– species of Arthrobacter and, based mainly on the diamino Thr–Ala (A. oxydans, A. polychromogenes); group II with acid in the peptidoglycan and differences in the DNA Lys–Ala–Thr–Ala (A. aurescens, A. histidinolovorans, G+C content, they subdivided arthrobacters into three A. ilicis, A. nicotinovorans, A. ureafaciens); group III with groups (Table 1). Species with lysine in the peptidoglycan Lys–Ala1–4 (A. crystallopoietes, A. globiformis, A. pascens, were placed in the first category, designated the ‘globiformis’ A. ramosus); group IV with Lys–Ser–Ala2–3 (S. atrocyanea, group and A. citreus (assigned to this first group despite formerly A. atrocyaneus); group V with Lys–Thr–Ala2 Downloaded from www.microbiologyresearch.org by http://ijs.microbiologyresearch.org 15 IP: 54.70.40.11 On: Mon, 04 Feb 2019 19:10:17 H.-J. Busse

(A. citreus); group VI with Lys–Ala–Glu (A. nicotianae, chromatographic motility than the diglycosyldiacylglycerol A. creatinolyticus, A. uratoxydans, A. protophormiae); and (GA)ofA. ilicis.ThetwostrainsofA. citreus were shown to con- group VII with Lys–Glu (A. sulfureus). tain DPG, PG, PI, a major glycolipid of medium hydrophobi- city corresponding to the chromatographic motility of a Though the first studies on polar lipids in arthrobacters were published more than 40 years ago, and interesting differ- diglycosyldiacylglycerol (GA)ofA. ilicis and minor amounts ences in the polar lipid compositions of arthrobacters were of a second glycolipid of high hydrophobicity exhibiting the reported approximately 30 years ago, this approach has chromatographic motilities of monoglycosyldiacylglycerol only rarely been considered in the description of novel (GB). species of Arthrobacter and their differentiation. In an early Amadi & Alderson (1982) reported that the type strains of A. study, Shaw & Stead (1971) examined the polar lipid profiles globiformis, A. crystallopoietes, A. oxydans, A. polychromogenes of the type strains of A. crystallopoietes and A. pascens and A. and A. ramosus all contain DPG, PG and PI in their polar globiformis strain 616 and reported no significant qualitative lipid profiles, and they reported the variable presence of an differences. Major lipids in the three species were reported unidentified phospholipid and the glycolipids G1 (supposed to be the phospholipids DPG, PG and phosphatidylinositol to represent MGDG), G3 (supposed to represent DMDG), (PI) and the glycolipids monogalactosyldiacylglycerol G4 (supposed to represent DGDG) and G5 (supposed to rep- (MGDG), digalactosyldiacyglycerol (DGDG) and dimanno- resent TMDG). Reservations exist concerning the assumption syldiacylglycerol (DMDG) and probably also small amounts that glycolipid G4 represents DGDG because, relative to the of trimannosyldiacylglycerol (TMDG) and tetramannosyl- mannolipid DMDG, the chromatographic motility of the diacylglycerol (TeMDG). The three major glycolipids corresponding spot is in disagreement with that indicated showed properties identical to those of three glycolipids of by Shaw & Stead (1971) and Collins et al. (1982b). In A. globiformis strain 616 identified earlier by Walker & A. globiformis and A. oxydans, four glycolipids were detected, Bastl (1967) as 3-O-b-D-galactosylpyranosyl-sn-1,2-diglyceride G ,G,G and G ;inA. crystallopoietes and A. ramosus,the (MGDG), 3-[O-b-D-galactosylpyranosyl-(1R6)-O-b-D-gala- 1 3 4 5 glycolipids G and G were detected; and, in A. polychromo- ctosylpyranosyl]-sn-1,2-diglyceride (DGDG) and 3-[O-a-D- 1 3 mannopyranosyl-(1R3)-O-a-D-mannopyranosyl]-sn-1,2- genes, the glycolipids G1,G3 and G5 were detected. The diglyceride (DMDG). Kostiw et al. (1972) also detected the polar lipid profile of A. ramosus is well in agreement with glycolipids MGDG and DGDG in A. crystallopoietes,butno itscloserelatednesstoA. ilicis and A. aurescens (Fig. 1). indicationofthepresenceofDMDG,TMDGorTeMDG The polar lipid profiles of A. globiformis and A. polychromo- was reported. genes are most similar to those reported for these two species by Collins et al. (1982b). Though A. oxydans and A. polychro- A. ilicis was the first species of the genus Arthrobacter to be mogenes are close phylogenetic relatives (Fig. 1), G4 was not described with the inclusion of the polar lipid profile reported for the latter species. Like in the report of Kostiw (Collins et al., 1981). This species was described to contain et al. (1972), A. crystallopoietes was shown to contain only DPG, PG, PI and two glycolipids designated GA and GB and two glycolipids but, insteadofDGDG,thepresenceof supposed to represent the diglycosyldiacylglycerols DGDG DMDG was reported. Collins & Kroppenstedt (1983) con- or DMDG and the monoglycosyldiacylglycerol MGDG, firmed only the presence of the glycolipid of medium hydro- respectively. Very similar polar lipid profiles were reported phobicity in A. citreus. These authors also showed that the for the type strain of A. aurescens, a close relative of A. ilicis, type strains of A. nicotianae, A. protophormiae (formerly and the more distantly related species A. polychromogenes Brevibacterium protophormiae)andA. sulfureus (formerly (Collins et al., 1982b). The latter authors also detected ‘Brevibacterium sulfureum’) lack PI and contain a single glyco- two major glycolipids in A. crystallopoietes that show chro- lipid of medium hydrophobicity. However, the glycolipid of matographic motilities similar to the monoglycosyldiacyl- glycerol and diglycosyldiacylglycerol of A. ilicis. In the A. nicotianae and A. protophormiae shows a chromatographic same study, Collins et al. (1982b) reported on the polar motility different from that of the glycolipid of A. sulfureus. lipid profiles of the type strain of A. globiformis and two Considering the information given by Keddie et al. (1986) strains of A. citreus, including the type strain. The type and the report of Shaw & Stead (1971), the identity of the strain of A. globiformis showed a polar lipid profile that is different glycolipids shown by Collins et al. (1982b) and qualitatively in agreement with that reported by Shaw & Collins & Kroppenstedt (1983) can be determined. The glyco- Stead (1971) for A. globiformis strain 616. It contains lipid with the highest hydrophobicity corresponds to MGDG. DPG, PG, PI and four glycolipids that exhibit different degrees The glycolipid with the lowest hydrophobicity corresponds to of hydrophobicity, as indicated from their chromatographic TMDG, because, in the first chromatographic dimension motilities. One glycolipid spot shows high chromatographic [corresponding to the solvent system applied by Shaw & motility, corresponding to the monoglycosyldiacylglycerol Stead (1971)], it shows the same motility as PG (Shaw & (GB)ofA. ilicis and indicating the highly hydrophobic nature Stead, 1971). Since the glycolipid of medium hydrophobicity of the lipid. Another spot shows low chromatographic motility, of A. sulfureus was suggested to correspond to DGDG, indicating low hydrophobicity, and two spots show medium whereas all other species of Arthrobacter studied contain chromatographic motility, indicating medium hydrophobi- DMDG (Keddie et al. 1986), the medium-hydrophobic glyco- city. One of these latter spots exhibits slightly higher lipidwiththeslightlyhigherRf in both chromatographic Downloaded from www.microbiologyresearch.org by 16 International Journal of Systematic and Evolutionary Microbiology 66 IP: 54.70.40.11 On: Mon, 04 Feb 2019 19:10:17 Taxonomy of the genus Arthrobacter dimensions represents DGDG, whereas the other one corre- exclusively DPG, PG and PI (Li et al., 2004b). The absence sponds to DMDG. of any glycolipid in A. russicus, A. tecti and A. tumbae is More recently, the chemical structures of the two major most surprising, because the presence of a diglycosyldiacyl- glycolipids of A. globiformis were analysed by Pas´ciak glycerol is apparently a characteristic of members of the et al. (2010). These authors confirmed the identity of one family Micrococcaceae. Hence, reanalyses of the polar major glycolipid in A. globiformis to be monogalactosyldia- lipid profiles of these three species would be desirable in cylglycerol but, in contrast to earlier reports, the other order to confirm these unexpected traits. A. livingstonensis major glycolipid was identified as a monoacyldimannosyl- and Arthrobacter cryotolerans were reported to contain PG monoacylglycerol (MDMMG). The same two major glyco- only (Ganzert et al., 2011), but a polar lipid profile with lipids were also found in A. scleromae. Interestingly, only a single lipid appears unlikely, because bacterial cyto- MDMMG was also reported to be a major lipid in other plasmic membranes are generally composed of several members of the family Micrococcaceae, including the type different lipid components. However, in the corresponding strains of S. atrocyanea (Niepel et al., 1997) and Rothia paper, the polar lipid profiles of the latter two species were dentocariosa, and it was demonstrated that Rothia mucilagi- incomplete. In addition to PG, HPLC-MS-MS analyses of nosa, Rothia amarae and M. luteus contain a major the polar lipid profiles demonstrated that A. livingstonensis glycolipid (Pas´ciak et al., 2002, 2010) that shows the also contains PI, DPG and two types of unidentified same chromatographic motility as MDMMG detected in glycolipid, and that A. cryotolerans contains DPG and A. globiformis, A. scleromae and R. dentocariosa. For an unidentified glycolipid (Kai Mangelsdorf, personal A. globiformis and M. luteus, this result is surprising, because communication). Walker & Bastl (1967), Shaw & Stead (1971) and Pakkiri The detection of PE, as reported for A. phenanthrenivorans, et al. (2004) reported that the major mannolipid of A. antarcticus, A. cupressi, A. flavus and A. roseus (Kalli- A. globiformis strain 616 and the type strain of M. luteus is manis et al., 2009; Pindi et al., 2010; Reddy et al., 2000, DMDG. It appears unlikely that these species switch between 2002; Zhang et al., 2012), like the absence of any glycolipid, DMDG and MDMMG depending on environmental con- is surprising for representatives of the family Micrococca- ditions and/or physiological age, because it can be supposed ceae because, like the presence of at least one glycolipid, that different enzymes would be required to transfer a fatty the absence of PE appears to be a common trait in polar acid to the mannose and the glycerol. Hence, it has to be lipid profiles of members of the family. Hence, reanalyses supposed that the result from one structural analysis of of the polar lipids of these five species would also be desir- this mannolipid is due to an error. able. However, exceptions concerning the presence of PE may occur in selected strains of Arthrobacter, as indicated Arthrobacter psychrophenolicus, a close phylogenetic relative from the observation that, in the genome of Arthrobacter of A. sulfureus, was reported to contain PG, DPG, PI and sp. MA-N2, a sequence was annotated to encode a putative an unidentified glycolipid (Margesin et al., 2004). The pre- phosphatidylserine decarboxylase (Ru¨diger Pukall, per- sence of PI in A. psychrophenolicus is surprising; this lipid sonal communication), which catalyses the formation of would be expected to be absent, as in its close relative PE from phosphatidylserine. However, when compared to A. sulfureus. Since no image of the total lipid profile of this sequences of almost the same length in a FASTA search species was provided, it is not possible to evaluate whether (Pearson & Lipman, 1988), the amino acid sequence the unidentified glycolipid corresponds to DGDG, found showed the highest similarity to the phosphatidylserine in A. sulfureus. decarboxylase of the epsilonproteobacterium Sulfurimonas The most recently described species, A. gyeryongensis (Hoang gotlandica (50.6 %). Among hits sharing 40–50 % et al., 2014), was described to contain DPG, two unidentified sequence identity, numerous betaproteobacterial strains, a glycolipids and two unidentified phospholipids. The two gly- few alpha-, gamma- and deltaproteobacterial strains and colipids show chromatographic motilities similar to a mono- several fungal strains were found, but only two actinobac- glycosyldiacylglycerol and diglycosyldiacylglycerol and the terial strains, assigned to the genus Frankia. Two additional two phospholipids might represent PG and PI. This polar actinobacterial strains assigned to the genus Streptomyces lipid profile is similar to that of A. ramosus, with which A. show only 36.2 and 37.7 % identity. This observation gyeryongensis shares the highest 16S rRNA gene sequence suggests that this type of phosphatidylserine decarboxylase similarity (98.2 % between the type strains). is not common among the actinobacteria. Hence, annota- The polar lipid profiles of Arthrobacter castelli, Arthrobacter tion as a phosphatidylserine decarboxylase in Arthrobacter monumenti, A. pigmenti and A. parietis (Heyrman et al., sp. MA-N2 can be considered to be questionable. 2005) share the presence of the lipids PG, DPG and PI In a pioneering study dealing with the dissection of the and one or two unidentified glycolipids with many species genus Micrococcus (Stackebrandt et al., 1995), the authors of Arthrobacter. Unidentified phospholipids were also also provided polar lipid data of groups I and II of Arthro- reported in some of these species. In contrast, A. tecti bacter, corresponding to the ‘A. globiformis/A. citreus and A. tumbae possess, in addition to PG, DPG and PI, group’ and the ‘A. nicotianae group’, respectively. With one unidentified phospholipid but no glycolipids reference to Jones & Collins (1986), the two groups were (Heyrman et al., 2005). A. russicus was reported to contain listed to contain DMDG and PI. Since no information

Downloaded from www.microbiologyresearch.org by http://ijs.microbiologyresearch.org 17 IP: 54.70.40.11 On: Mon, 04 Feb 2019 19:10:17 H.-J. Busse concerning lipids is provided in the cited chapter of Ber- rRNA gene sequence similarity (97.6 % between the type gey’s Manual of Systematic Bacteriology except that the strains) and similar chemotaxonomic traits. However, in two groups of Arthrobacter differ with respect to their phylogenetic trees, A. crystallopoietes is usually the sole lipid composition, citation of this paper concerning the species on a separate branch (Fig. 1; Ding et al.,2009; presence of DMDG and PI in both groups is apparently Ganzert et al., 2011; Yassin et al., 2011b; Margesin et al., due to an error. This information is also not provided in 2012; Busse et al., 2012). The peptidoglycan structure also the following chapter in Bergey’s Manual of Systematic Bac- does not assign this species clearly to the ‘A. globiformis teriology dealing with the genus Arthrobacter (Keddie et al., group’. Hence, A. crystallopoietes might be considered as 1986). These latter authors indicated that the majority of the sole species of an as-yet undefined group. species of Arthrobacter analysed for polar lipids, including Though placed phylogenetically separate from the ‘A. glo- two species of the ‘A. nicotianae group’, namely A. nicotia- biformis group’ but without bootstrap support for the nae and A. protophormiae, contain DMDG, whereas a single branching node (Zhang et al., 2012; Fig. 1), the recently representative of the ‘A. nicotianae group’, A. sulfureus, described species A. cupressi might be considered another instead contains DGDG. Keddie et al. (1986) also empha- member of this group. The type strain shares the highest sized the absence of PI in the representatives of the ‘A. nico- 16S rRNA gene sequence similarity with two members of tianae group’. Hence, the information that both groups of the group, A. oryzae (97.7 %) and A. humicola (97.3 %), the genus Arthrobacter are characterized by the presence of and 96.9 and 96.8 % similarity with the type strains of DMDG and PI in the polar lipid profile is misleading, A. pascens and A. globiformis, respectively. Like in species because the members of the ‘A. nicotianae group’ lack PI of the ‘A. globiformis group’, its peptidoglycan structure and contain either DMDG or DGDG. It is important to shows the interpeptide bridge Lys–Ala2, but the presence point out this error because, to date, Stackebrandt et al. of a glycine bound to the a-carboxyl group of D-gluta- (1995) only has been cited in eight papers in the IJSEM mic acid distinguishes it from other members of the for the presence of DMDG and PI in both groups of Arthro- group. bacter (Stackebrandt & Schumann, 2000; Altenburger et al., The ‘A. aurescens group’ is defined based on high 16S rRNA 2002; Li et al., 2004a, 2005c; Zhang et al., 2007; Schumann . et al.,2009;Zhouet al., 2009; Yassin et al.,2011a). gene sequence similarity among its members ( 97.5 %), the presence of the major respiratory menaquinone MK- Phylogenetic calculations have clearly demonstrated that 9(H2) and peptidoglycan of type A3a (Lys–Ala–Thr–Ala) the genus is not monophyletic but is mixed with other corresponding to peptidoglycan structure A11.17. The representatives of the family Micrococcaceae, including the group comprises six species, A. aurescens, A. histidinolovorans, genera Acaricomes, Auritidibacter, Citricoccus, Micrococcus, A. ilicis, A. nicotinovorans, Arthrobacter nitroguajacolicus and Nesterenkonia, Renibacterium, Sinomonas, Yaniella and A. ureafaciens. Zhihengliuella (Munoz et al., 2011; Busse et al., 2012). Hence, careful evaluation of the taxonomy of the genus The ‘A. oxydans group’ contains the species A. chloropheno- Arthrobacter is desirable. In this context, it is interesting licus, A. defluvii, A. niigatensis, A. oxydans, A. phenanthreni- that certain groupings within the radiation of the genus vorans, A. polychromogenes, A. scleromae and Arthrobacter Arthrobacter, as indicated from comparative 16S rRNA sulfonivorans, which share high 16S rRNA gene sequence . gene sequence analyses, are also reflected by identical or similarities ( 97 %), MK-9(H2) as a major quinone at least highly similar chemotaxonomic traits. [except A. scleromae, which was reported to contain predo- minantly MK-8(H2)] and a peptidoglycan type with Lys– The first move was made by Busse et al. (2012), by dissect- Ser–Thr–Ala in the interpeptide corresponding to peptido- ing the genus Arthrobacter into 11 groups, mainly on the glycan structure A11.23 chain (A. phenanthrenivorans was basis of robust phylogenetic clusters or high 16S rRNA not analysed for its peptidoglycan type). gene sequence similarities and group-specific chemotaxo- nomic traits. A phylogenetic tree showing these groups Arthrobacter equi, which was described recently by Yassin and including most recently described novel species of et al. (2011b), can be assigned to the ‘A. oxydans group’ Arthrobacter is shown in Fig. 1. for several reasons. It shares the highest 16S rRNA gene sequence similarity (97.9–99.2 %) with members of this The ‘A. globiformis group’ contains candidates for the group, as well as the quinone system and the peptidoglycan genus Arthrobacter sensu stricto. It is composed of the structure A11.23. Another recently described species, type species of the genus, A. globiformis, and A. pascens, A. siccitolerans (SantaCruz-Calvo et al., 2013), can also be which are closely related in all phylogenetic trees. A. humi- considered to belong to the ‘A. oxydans group’. It shows cola and A. oryzae were assigned to this group on the basis the same characteristic peptidoglycan structure and quinone of high 16S rRNA gene sequence similarity to A. globiformis . system and shares high 16S rRNA gene sequence similarity ( 98 %), similar peptidoglycan composition (Lys–Ala2–3) with species of the ‘A. oxydans group’ (.98 %). corresponding to peptidoglycan structures A11.5/A11.6 (Schumann, 2011; http://www.dsmz.de/?id5449) and the Species of the ‘A. protophormiae group’ (including quinone system menaquinone MK-9(H2). A. crystallopoietes A. rhombi) were reported to share 95.5–99.7 % 16S rRNA was tentatively assigned to the group on the basis of high 16S gene sequence similarity. The core of this group is composed

Downloaded from www.microbiologyresearch.org by 18 International Journal of Systematic and Evolutionary Microbiology 66 IP: 54.70.40.11 On: Mon, 04 Feb 2019 19:10:17 Taxonomy of the genus Arthrobacter of the species A. ardleyensis, A. arilaitensis, A. bergerei, of MK-10, MK-8 and MK-7 and peptidoglycan type A. mysorens, A. nicotianae, A. protophormiae, A. soli and Lys–Glu. Since these traits are in accordance with the A. uratoxydans, which share 96.7–99.7 % 16S rRNA gene characteristics of the ‘A. sulfureus group’, the assignment sequence similarity. Except A. soli, which was not analysed of A. cryotolerans to this group appears to be justified. for this trait, all species show peptidoglycan type A4a (Lys– Members of the ‘A. agilis group’ form a stable clade, as indi- Ala–Glu) corresponding to peptidoglycan structure A11.35. cated by a high bootstrap value (89 %). The group contains According to Stackebrandt et al. (1983), the glutamic acid the species A. agilis, A. flavus, A. parietis, A. subterraneus, in the interpeptide bridge of A. nicotianae, A. protophormiae A. tecti and A. tumbae, which share 97.3–99.6 % 16S rRNA and A. uratoxydans occurs in the L-configuration. The qui- gene sequence similarity, a peptidoglycan Lys–Thr–Ala none system contains exclusively completely unsaturated 2–3 corresponding to peptidoglycan structures A11.27/A11.28 menaquinones, always with MK-8 as a major component and a quinone system with the predominant menaquinone (no data are available for A. arilaitensis, A. bergerei and MK-9(H ). A. soli). A. rhombi and A. creatinolyticus had been assigned 2 to this group because they share 16S rRNA gene sequence The four species of the ‘A. citreus group’, A. citreus, A. gan- similarity of .96.5 % with at least one representative of davensis, A. koreensis and A. luteolus, show high 16S rRNA the group and show the presence of the group-specific pep- gene sequence similarity (97.6–98.9 %), a peptidoglycan tidoglycan composition and/or quinone system. However, Lys–Thr–Ala2 corresponding to peptidoglycan structure the presence of a quinone system menaquinone MK-9(H2) A11.27 and the major menaquinone MK-9(H2). was later reported for the type strain of A. rhombi (Chen The ‘A. psychrolactophilus group’ was defined based on 16S et al., 2009). Furthermore, the glutamic acid in the interpep- rRNA gene sequence similarities of .97.0 % among its tide chain occurs in the D-configuration (Osorio et al.,1999) members, a peptidoglycan with either Lys–Thr–Ala1–3 or and not in the L-configuration, like other members of the Lys–Ala corresponding to peptidoglycan structures group. These two chemotaxonomic traits clearly distinguish 2 A11.25/A11.27/A11.28 and A11.5, respectively, and MK- A. rhombi from members of the ‘A. protophormiae group’. 9(H ) as the major respiratory quinone. Also, the ability Hence, A. rhombi should not be considered to be a 2 of all members of this group to grow at low temperatures member of the ‘A. protophormiae group’. Since the combi- (0–4 8C) was also pointed out as a common characteristic. nation of menaquinone MK-9(H ) and a peptidoglycan 2 This group comprises the species A. psychrolactophilus, type A4a (variation Lys–Ala–D-Glu) is unique among A. stackebrandtii, A. psychrochitiniphilus and A. alpinus. arthrobacters, A. rhombi can be considered to be a represen- tative of another group of the genus Arthrobacter that was Recently, two species of Arthrobacter, A. livingstonensis and not defined by Busse et al. (2012). Arthrobacter halodurans, A. cryoconiti, have been described and placed phylogeneti- which was described by Chen et al. (2009) to share its qui- cally among the species representing the ‘A. psychrolacto- none system with A. rhombi and to belong to the same philus group’ (Ganzert et al., 2011; Margesin et al., 2012). line of descent but with peptidoglycan type A4a (variation The two species share 97.0–97.9 and 97.7–98.3 % 16S Lys–Ala–L-Glu), should hence not be considered a second rRNA gene sequence similarity, respectively, with the mem- species of this unnamed group of the genus Arthrobacter. bers of this group and exhibit the same quinone system and grow at low temperatures ((6 and 1 8C, respectively). Data The ‘A. sulfureus group’ contains the species A. antarcticus, from analysis of the peptidoglycan of A. livingstonensis A. gangotriensis, Arthrobacter kerguelensis, Arthrobacter psy- suggest that it is Lys–Thr–Ala (A11.25). This peptidoglycan chrophenolicus and A. sulfureus. In many trees, these species type is similar to those found in A. psychrolactophilus, form a clade though, in Fig. 1, this branch is not supported A. psychrochitiniphilus and A. alpinus. The peptidoglycan by a significant bootstrap value (37 %). However, the same of A. cryoconiti is Lys–Ala (A11.7), resembling that of degree of branching is also shown in the neighbour-joining 4 A. stackebrandtii, with Lys–Ala (A11.5). and maximum-parsimony tree (results not shown). 16S 2 rRNA gene sequence similarity among the species is Because of their almost identical quinone systems and pep- .97.0 %. All species share a peptidoglycan A4a (Lys– tidoglycan variations, the ‘A. agilis group’, the ‘A. citreus Glu) corresponding to peptidoglycan structure A11.54. group’ and several species of the ‘A. psychrolactophilus According to Stackebrandt et al. (1983) and Margesin group’ are distinguishable from each other only on the et al. (2004), the glutamic acid in the interpeptide bridge basis of 16S rRNA gene sequence similarity (94.2–96.8 % of A. sulfureus and A. psychrophenolicus occurs in the similarity between representatives of the three groups) L-configuration. Quinone systems of representatives of and phylogenetic clustering. Each of these three groups this group exclusively contain completely unsaturated forms a stable clade (Fig. 1). Hence, they can be considered menaquinones (MK-8, MK-9 and/or MK-10). to represent taxonomic entities separate from the core of the genus, Arthrobacter sensu stricto. Recently, the species Arthrobacter cryotolerans was described, which was placed phylogenetically at the root The ‘A. pigmenti group’ comprises the two core species of the branch comprising the members of the ‘A. sulfureus A. castelli and A. pigmenti, the type strains of which share group’ (Ganzert et al., 2011). This species contains a qui- 97.9 % 16S rRNA gene sequence similarity. Though shar- none system with MK-9 predominant and lesser amounts ing only 96.5 % 16S rRNA gene sequence similarity with

Downloaded from www.microbiologyresearch.org by http://ijs.microbiologyresearch.org 19 IP: 54.70.40.11 On: Mon, 04 Feb 2019 19:10:17 H.-J. Busse these two species and slightly higher similarity values with were detected. A. pascens WS 1766T showed a rather similar species of other groups, A. monumenti is placed at the root profile, differing mainly from A. globiformis DSM 20124T of this group in many phylogenetic trees. Common to the with respect to the amounts of certain lipids including three species is a quinone system with the major menaqui- DPG, PG and PI, glycolipids GL1, GL3, GL4 and GL5 none MK-9(H2), the presence of the cell-wall sugars galac- and the polar lipids L2 and L3. The major differing charac- tose and rhamnose and a peptidoglycan with four alanines teristic in the lipid profile of A. pascens was the presence of in the interpeptide bridge. However, A. castelli shows a the second highly hydrophobic glycolipid GL6 and absence peptidoglycan type Lys–Ala–Ser–Ala3 (not listed by Schu- of a second diglycosyldiacylglycerol (GL2; Fig. 3b) that was mann, 2011; http://www.dsmz.de/?id5449), whereas A. previously reported to be present in this species (Shaw & pigmenti and A. monumenti have peptidoglycan type Lys– Stead, 1971). The qualitative polar lipid composition of T Ala4 corresponding to peptidoglycan structure A11.7. A. globiformis DSM 20124 was in good agreement with the data reported by Shaw & Stead (1971). In contrast, The ‘A. albus/cumminsii group’ contains only the two equal amounts of the two diglycosyldiacylglycerols (GL2 species A. albus and A. cumminsii. The type strains of the and GL3) were not found, which might be related to the two species share 99.1 % 16S rRNA gene sequence simi- fact that, in the present study, the type strain of A. globifor- larity and form a rather deeply branching subline within mis was subjected to analysis and not A. globiformis strain the genus Arthrobacter in phylogenetic trees. The two 616, which had been examined by the latter authors. The species possess peptidoglycan type A4a (Lys–Ala–Glu or quinone system of A. globiformis DSM 20124T was com- Lys–Ser–Glu) corresponding to peptidoglycan structures posed of 85 % MK-9(H ), 6 % MK-8(H ), 6 % MK- A11.35 and A11.58, respectively. Analysis of the quinone 2 2 10(H ), 3 % MK-9 and traces (,1 %) of MK-7(H ) and system revealed the presence of the major menaquinone 2 2 the quinone system of A. pascens WS 1766T was composed MK-8(H ) in the two species. This quinone system dis- 2 of 69 % MK-9(H ), 28 % MK-10(H ), 2 % MK-8(H ) and tinguishes this group unambiguously from the vast 2 2 2 2 % MK-7(H ). majority of species of the genus Arthrobacter.Only 2 A. scleromae was reported to exhibit a similar quinone The polar lipid profile of A. polychromogenes WS 1989T system, but this species is assigned to the ‘A. oxydans consisted of the major lipids DPG, PI, GL1 and GL3 and group’, with which it shares the peptidoglycan type (Huang minor amounts of PG, three unidentified lipids (L1, L2 et al., 2005) and high 16S rRNA gene sequence similarity. and L7) and GL5 (Fig. 3c). This profile is in excellent agree- ment with data reported for this species by Collins et al. The ‘Sinomonas group’, as defined recently (Busse et al., (1982b). The quinone system was composed of 80 % 2012), harbours species of the genera Sinomonas and MK-9(H ), 13 % MK-10(H ), 5 % MK-8(H ), 1 % MK- Arthrobacter. After reclassification of Arthrobacter albidus 2 2 2 7(H ) and traces (,1 %) of MK-8, MK-9 and MK-10, and Arthrobacter echigonensis as Sinomonas albida and 2 which is similar to previous results for this species (Collins Sinomonas echigonensis (Zhou et al., 2012), the ‘Sinomonas et al., 1979). group’ no longer contains species of Arthrobacter, and hence it is not be dealt with further in this discussion. In A. histidinolovorans WS 1798T, the polar lipid profile was composed of the major lipids DPG, GL1, GL2 and PI and All other established species of the genus Arthrobacter not minor amounts of L1, L2 and GL5 (Fig. 3d). This polar mentioned above were only tentatively assigned to certain lipid composition is most similar to those of A. aurescens groups or remained unassigned. (Collins et al., 1982b) and A. ilicis (Collins et al. 1981), During this study on the taxonomy and chemotaxonomy close phylogenetic relatives of A. histidinolovorans (Fig. 1) of the genus Arthrobacter, reanalyses of the quinones and that were placed in the ‘A. aurescens group’ (Busse et al., polar lipids of several species of Arthrobacter were carried 2012). The quinone system was composed of 83 % MK- out due to availability, including A. globiformis, A. pascens, 9(H2), 9 % MK-8(H2), 4 % MK-7(H2), 3 % MK-10(H2), A. histidinolovorans, A. roseus, A. agilis, A. nicotinovorans, A. 1 % MK-9 and traces (,1 %) of MK-7, MK-8 and MK- psychrophenolicus, A. polychromogenes, A. alpinus and 10; this quinone system confirms that MK-9(H2) is the A. cryoconiti. Additionally, the polar lipids and quinones major menaquinone (Kodama et al., 1992), but other of A. cumminsii and A. albus, which had been described menaquinones are also present in significant amounts. without including these traits, were also analysed. Extrac- A. agilis DSM 20550T showed a rather simple polar lipid tion and analyses of quinones and polar lipids were carried profile that consisted of the major lipids DPG, PG, PI out as described by Tindall (1990a, b). For HPLC analyses and GL3 and minor amounts of GL5, L1 and L2. Further- of quinones, the equipment described by Altenburger et al. more, a reddish pigment spot could be detected (Fig. 3e). (1996) or Stolz et al. (2007) was used. The fact that PE was not detected, which is in accordance A globiformis DSM 20124T showed a polar lipid profile that with the majority of species of the genus Arthrobacter, was composed of the major lipids DPG, PG and glycolipid but contrasts with its reported presence in the next phylo- GL3 and moderate amounts of PI and glycolipid GL1 genetic relative, A. flavus (Reddy et al., 2000), supports (Fig. 3a). Furthermore, minor to trace amounts of glyco- concerns about the reliable identification of PE in the lipids GL2, GL4 and GL5 and two polar lipids (L1, L2) latter species.

Downloaded from www.microbiologyresearch.org by 20 International Journal of Systematic and Evolutionary Microbiology 66 IP: 54.70.40.11 On: Mon, 04 Feb 2019 19:10:17 Taxonomy of the genus Arthrobacter

(a) (b) The detection of PE and the absence of a diglycosyldiacyl- glycerol and other glycolipids in species of the family GL6 Micrococcaceae including species of the genus Arthrobacter GL1 GL1 DPG L1 is most surprising. The type strain of A. roseus, reported DPG to contain PE and accessible in the course of this study, was subjected to reanalysis of its polar lipid profile. The GL2 PG PG GL3 GL3 results did not provide any indication of the presence of GL7 GL4 GL4 PE (Fig. 3f). Like other arthrobacters, it had a polar lipid L2 PI PI profile containing predominantly DPG and PG, moderate GL5 GL5 L2 L3 amounts of PI, GL3 and three polar lipids (L1, L2, L4) and minor amounts of GL5 and two unidentified highly (c) (d) polar glycolipids GL8 and GL9, which so far are unique

GL1 among polar lipid profiles of members of the genus GL1 L1 DPG Arthrobacter. These results suggest the need to emend the L1 DPG description of the species A. roseus. L7

GL3 The most complex polar lipid profiles were detected in GL3 PG T PG L6 A. cumminsii DSM 10493 (Fig. 3g) and A. albus DSM L6 L8 T L2 13068 (results not shown). They were composed of the L2 PI major lipids DPG, PG and GL3, unidentified phospholipids GL5 GL5 PI PL1, PL3 and PL5 and moderate to minor amounts of PI, two unidentified phospholipids (PL2 and PL4), two glyco- (e) (f) lipids (GL1, GL5) and four polar lipids (L1, L3, L5, L6). A. albus DSM 13068T contained minor amounts of an L1 DPG L1 additional phospholipid. The quinone system of A. cum- L4 T DPG minsii DSM 10493 was composed of 85 % MK-8(H2), 6 % MK-8, 5 % MK-7(H2), 3 % MK-9(H2) and 1 % T GL3 PG MK-7 and the quinone system of A. albus DSM 13068

PG GL3 was composed of 83 % MK-8(H2), 2 % MK-8, 3 % MK- rPig L2 7(H2) and 11 % MK-9(H2). L2 PI GL5 PI GL5 T GL8 The polar lipid profile of A. nicotianae WS1765 (Fig. 3h) GL9 consisted of the major lipids DPG, PG and GL3, moderate (g) (h) amounts of GL1 and polar lipids L1 and L2 and minor amounts of GL5. In agreement with the observation of PL1 L1 GL1 Collins & Kroppenstedt (1983), PI was not detected, whereas PL2 GL1 L1 DPG DPG the presence of GL1, GL5, L1 and L2 was not reported by T L5 PL3 these authors. The quinone system of A. nicotianae WS1765 PG GL3 L6 contained 65 % MK-8, 31 % MK-9, 3 % MK-7 and 1 % PG PL5 GL3 MK-10, confirming earlier results published for this species PL4 GL5 L2 (Yamada et al., 1976; Collins & Kroppenstedt, 1983). PI L3 T GL5 In A. psychrophenolicus AG31 , the next phylogenetic relative of A. sulfureus, and the close relative A. cryotolerans LI3T,less (i) (j) complex polar lipid profiles were detected (Fig. 3i, j), show- ing only three major lipids, namely DPG, PG and GL2. Additionally, in A. cryotolerans LI3T, minor amounts of L1 L1 DPG

DPG

GL2 PG GL2 PG roseus DSM 14508T (f), A. cumminsii DSM 10493T (g), L2 A. nicotianae WS 1765T (h), A. psychrophenolicus AG31T (i) and A. cryotolerans LI3T (j) after two-dimensional TLC and detection with molybdatophosphoric acid. DPG, Diphosphatidylglycerol; PG, phosphatidylglycerol; PI, phosphatidylinositol; GL1, monoga- lactosyldiacylglycerol (MGDG); GL2, digalactosyldiacylglycerol Fig. 3. Polar lipid profiles of A. globiformis DSM 20124T (a), (DGDG); GL3, dimannosylglyceride (DMG); GL5, trimannosyldia- A. pascens WS 1766T (b), A. polychromogenes WS 1989T (c), cylglycerol (TMDG); GL4, GL6–GL9, unidentified glycolipids; L1– A. histidinolovorans WS 1798T (d), A. agilis DSM 20550T (e), A. L5, unidentified lipids; PL1–PL4, unidentified phospholipids.

Downloaded from www.microbiologyresearch.org by http://ijs.microbiologyresearch.org 21 IP: 54.70.40.11 On: Mon, 04 Feb 2019 19:10:17 H.-J. Busse and L2 were detectable. As suggested from the very close contains DGDG, to species included in the ‘A. sulfureus phylogenetic relationship to A. sulfureus, which was reported group’ as defined by Busse et al. (2012). to lack PI (Collins & Kroppenstedt, 1983), this lipid could Using information concerning the chromatographic motility also not be detected in A. psychrophenolicus AG31T and T T of glycolipids reported in the literature (Shaw & Stead, 1971; A. cryotolerans LI3 .ForA. psychrophenolicus AG31 ,this Collins et al., 1982b; Collins & Kroppenstedt, 1983; Keddie observation is in contrast to the data reported by Margesin et al., 1986) and the results presented in this study, another et al. (2004). The quinone system of A. psychrophenolicus two glycolipids (GL1 and GL5; Fig. 3) can be preliminarily AG31T was composed of 81 % MK-10, 13 % MK-9, 5 % , identified. Glycolipid GL1 corresponds to MGDG, indicated MK-7, 1 % MK-8 and traces ( 1 %) of MK-11, which is by the highly hydrophobic chromatographic motility similar to that reported by Margesin et al. (2004). reported for this lipid (Shaw & Stead, 1971) and its presence Simple polar lipid profiles were detected in A. alpinus S6-3T in A. globiformis, A. pascens and A. crystallopoietes;GL5 T and A. cryoconiti Cr6-08 (results not shown). Both strains corresponds to TMDG, as it exhibits the same Rf as PG in exhibited a polar lipid profile consisting of DPG, PG, the first chromatographic dimension (Shaw & Stead, 1971). PI and GL3. Minor amounts of PL5 were detected in T The presence of DGDG in arthrobacters that also contain A. alpinus S6-3 . The similarity in the polar lipid profiles DMG deserves closer consideration. Shaw & Stead (1971) is in agreement with their close phylogenetic relationship reported almost equal amounts of these two diglycosyldia- (Margesin et al., 2012). cylglycerols in A. globiformis strain 616 and the type strains In order to identify the motility of DMDG in our chroma- of A. pascens and A. crystallopoietes (Shaw & Stead, 1971). tographic system, the type strain of Micrococcus luteus, In contrast, Collins et al. (1982b) showed a polar lipid pro- which was reported to contain DMDG (Lennarz & file for the type strain of A. globiformis that contained a Talamo, 1966; Pakkiri et al., 2004), was subjected to major lipid with the chromatographic motility of DGDG polar lipid analysis. The chromatographic motility of and significantly smaller amounts of a lipid with the chro- DMDG of M. luteus was compared by co-chromatography matographic motility of DMG whereas, in the present in a mixture of extracts of A. globiformis DSM 20124T and study, DMG was the predominant glycolipid in A. globifor- A. polychromogenes WS 1989T. After staining with a- mis and DGDG was detected only in minor amounts naphthol, only a single positive spot was detected (results (Fig. 3a). The presence of almost equal amounts of not shown), demonstrating that the diglycosylglycerides DGDG and DMG in A. pascens (Shaw & Stead, 1971) of M. luteus, A. globiformis and A. polychromogenes show could not be reproduced in the present study, in which the same chromatographic motility. Applying sophisticated A. pascens showed DMG as the major glycolipid (Fig. methods, A. globiformis was described to contain MDMMG 3b). For the type strain of A. crystallopoietes, Collins et al. (Pas´ciak et al., 2010) and M. luteus to contain DMDG (1982b) could not reproduce the relatively large amounts (Pakkiri et al., 2004), but the results from the present of DGDG reported by Shaw & Stead (1971). This variability study indicate either that MDMMG and DMDG show of the amounts of DGDG in polar lipid profiles of identical chromatographic motility in the system applied A. globiformis, A. pascens and A. crystallopoietes may suggest here or that, in one of the studies on the structure of the that the expression of this glycolipid depends on growth diglycosylglycerides of A. globiformis and M. luteus,thedata conditions and/or the physiological age of biomass that from MS analysis were misinterpreted. Since the detailed was subjected to extraction of polar lipids. Hence, the pre- chemical structure of the mannolipid cannot be clarified sence of DGDG in arthrobacters that also contain signifi- here, nor can the question be answered whether MDMMG cant amounts of DMG should not be given too much and DMDG show the same chromatographic motility, the importance in drawing taxonomic conclusions. mannolipid will be designated dimannosylglyceride (DMG). Reservations concerning the polar lipid profiles reported Except A. psychrophenolicus and A. cryotolerans, all repre- for certain species of the genus Arthrobacter are based on sentatives of Arthrobacter examined in this study showed the consideration that major polar lipids are rather con- the presence of a major glycolipid (GL3) with chromato- served traits and are usually shared by all members of a graphic motility corresponding to DMG in A. globiformis genus or even family. The details were already discussed and A. polychromogenes. Hence, it is justified to conclude above and are summarized below. The polar lipid profiles that they all contain DMG. A. psychrophenolicus showed reported for the majority of arthrobacters and other mem- the presence of a glycolipid with the chromatographic bers of the family Micrococcaceae including representatives motility of a diglycosyldiacylglycerol corresponding to of the genera Auritidibacter, Citricoccus, Enteractinococcus, glycolipid Gb reported to be present in its close phyloge- Kocuria, Micrococcus, Nesterenkonia, Rothia, Sinomonas, netic relative A. sulfureus (Collins & Kroppenstedt, 1983). Yaniella and Zhihengliuella (Embley et al., 1984; Kova´cs Glycolipid Gb was supposed to represent DGDG (Keddie et al., 1999; Altenburger et al., 2002; Wieser et al., 2002; et al., 1986). Hence, glycolipid GL2 of A. psychrophenolicus Li et al., 2004a, 2005b; Zhang et al., 2007; Yassin et al., and A. cryotolerans can also be identified as DGDG. This 2011a; Zhou et al., 2012; Cao et al., 2012) suggest that finding suggests extending the statement of Keddie et al. they generally contain a core polar lipid profile that is com- (1986) that, among arthrobacters, only A. sulfureus posed of DPG, PG and at least one glycolipid (either a

Downloaded from www.microbiologyresearch.org by 22 International Journal of Systematic and Evolutionary Microbiology 66 IP: 54.70.40.11 On: Mon, 04 Feb 2019 19:10:17 Taxonomy of the genus Arthrobacter dimannosyl lipid or a digalactosyl lipid) and that PE is above are not considered in the following taxonomic absent. The majority of species of Arthrobacter also contain conclusions. PI, but members of the ‘A. nicotianae group’ (Keddie et al. 1986), recently split into the ‘A. protophormiae group’ and Chemotaxonomic data that can be considered to be suffi- the ‘A. sulfureus group’ (Busse et al., 2012), do not. Species ciently conserved to characterize genera are summarized in reported to deviate from these two core polar lipid profiles Table 2. These data suggest that five groups of the genus include A. antarcticus (Pindi et al., 2010), A. cupressi Arthrobacter, as recently defined (Busse et al., 2012), are (Zhang et al., 2012), A. flavus (Reddy et al., 2000), A. characterized by traits that distinguish them from the core phenanthrenivorans (Kallimanis et al., 2009), A. psychrophe- of the genus Arthrobacter (Arthrobacter sensu stricto), nolicus (Margesin et al., 2004), A. roseus (Reddy et al., which is composed of the type species of the genus, A. glo- 2002), A. russicus (Li et al., 2004b), A. tecti and A. biformis, and the additional species A. pascens, A. oryzae tumbae (Heyrman et al., 2005). and A. humicola, and from other groups of the genus Arthro- bacter, including the ‘A. aurescens group’, the ‘A. oxydans A. phenanthrenivorans, A. antarcticus, A. flavus and group’, the ‘A. protophormiae group’, the ‘A. sulfureus A. roseus were reported to contain PE and to lack any group’ and the ‘A. albus/cumminsii group’. Except the ‘A. glycolipid. The close relatives of A. phenanthrenivorans oxydans group’, these groups form clades in the phylogenetic (A. oxydans and A. polychromogenes), A. antarcticus (A. tree, but only the branching nodes of the ‘A. aurescens sulfureus)andA. flavus (A. agilis, A. parietis, A. tecti group’ and the ‘A. albus/cumminsii group’ were supported and A. tumbae)wereshowntolackPE,andmostof by another tree-calculating algorithm. High bootstrap sup- them have been shown to contain at least one glycolipid port was only found for the branching node of the (Amadi & Alderson, 1982; Collins & Kroppenstedt, 1983; ‘A. albus/cumminsii group’; the branching node of the Heyrman et al.,2005;Fig.3c,f,g,i,j).Hence,thereis ‘A. protophormiae group’ was supported by a relatively high some probability that the named species contain at bootstrap value (Fig. 1). Members of the ‘A. oxydans least one glycolipid and lack PE. The absence of PE group’ are split into several branches, with the core consist- and any other aminophospholipid and the presence of ing of A. oxydans, A. scleromae and A. polychromogenes and four glycolipids in the profile of A. roseus was shown the neighbouring species A. defluvii, A. sulfonivorans and in the present study (Fig. 3f), which is in line with the A. niigatensis. The species pair A. chlorophenolicus/A. phenan- core polar lipid profile supposed to characterize mem- threnivorans and the single species A. equi and A. siccitolerans bers of the family Micrococcaceae.ForA. cupressi each occupy separate positions in the vicinity of the core (Zhang et al., 2012), a polar lipid profile was shown con- species of the group. However, each of the species A. chloro- taining PE and a glycolipid exhibiting chromatographic phenolicus, A. phenanthrenivorans, A. equi and A. siccitolerans motility that can be supposed to represent TMDG. The shares high 16S rRNA gene sequence similarity (98.4–98.9, PE shows a chromatographic motility that would be 97.9–99.2, 97.6–99.2 and 98.4–99.3 %, respectively) with expected for a diglycosyldiacylglycerol and, hence, it is the core species and their closest neighbours. These data supposed here that the corresponding spot had been demonstrate that the high 16S rRNA gene sequence simi- misidentified. However, the presence of PE and the larities between the species of the group are not well reflected absence of a diglycosyldiacylglycerol has not been in the phylogenetic tree (Fig. 1) and, hence, the splitting of shown in any of the nearest related species to A. cupressi the members of the ‘A. oxydans group’ is of little or no (.96.5 % 16S rRNA gene sequence similarity) analysed for significance for taxonomic reorganization of the genus. polar lipids, including A. globiformis, A. pascens, A. histidi- In conclusion, it is proposed to reclassify members of these five nolovorans, A. equi and A. aurescens (Shaw & Stead, 1971; groups within the genus Arthrobacter in the novel genera Pae- Collins et al., 1982b; Yassin et al., 2011b; Fig. 3a, b, d). A. narthrobacter gen. nov. (the ‘A. aurescens group’), Pseudarthro- tecti, A. tumbae and A. russicus differ from the core polar bacter gen. nov. (the ‘A. oxydans group’), Glutamicibacter gen. lipid profile in the absence of any glycolipid. However, the nov. (the ‘A. protophormiae group’), Paeniglutamicibacter gen. close relatives of A. tumbae and A. tecti (A. agilis and A. parietis) nov. (the ‘A. sulfureus group’) and Pseudoglutamicibacter gen. were shown to contain two glycolipids (Fig. 3e; Heyrman et al., nov. (the ‘A. albus/cumminsii group’). 2005). Also, Renibacterium salmoninarum,thenearestphyloge- netic relative of A. russicus (Pukall et al., 2006; Munoz et al., The species A. aurescens, A. histidinolovorans, A. ilicis, 2011; Busse et al., 2012; Fig. 1), was reported to contain glyco- A. nicotinovorans, A. nitroguajacolicus and A. ureafaciens lipids (Collins, 1982). Hence, the presence of a glycolipid in the are reclassified in the genus Paenarthrobacter gen. nov. polar lipid profile would be also expected in A. russicus. A. psy- The species A. chlorophenolicus, A. defluvii, A. equi, A. nii- chrophenolicus was reported to contain PI, distinguishing it gatensis, A. oxydans, A. phenanthrenivorans, A. polychromo- from its close relative A. sulfureus. Reanalysis of the polar genes, A. scleromae, A. siccitolerans and A. sulfonivorans are lipid profile did not show the presence of PI in A. psychropheno- reclassified in the genus Pseudarthrobacter gen. nov. The licus (Fig. 3i), confirming the reservations expressed above. species A. ardleyensis, A. arilaitensis, A. bergerei, A. creatino- Because of these reservations, supported in two cases by lyticus, A. mysorens, A. nicotianae, A. protophormiae, A. soli data gained in this study, the reported polar lipid profiles of and A. uratoxydans are reclassified in the genus Glutamici- the other species of the genus Arthrobacter mentioned bacter gen. nov. The species A. antarcticus, A. cryotolerans,

Downloaded from www.microbiologyresearch.org by http://ijs.microbiologyresearch.org 23 IP: 54.70.40.11 On: Mon, 04 Feb 2019 19:10:17 H.-J. Busse D ) 2 , 1995; , 2009). or Lys– (Lys– ) (Embley 3 4 d a , 2002; Liu A. pigmenti et al. ‘ group’ A3 GL Ala–Ser– Ala Ala unspecified or A11.7 et al. , 2009, 2012); et al. gen. nov. and 1–3 et al. d ) A11.25, V 1–4 ) MK-9(H Renibacterium 2 GL(s) (Stackebrandt (Lys–Ala–Glu) (Lys–Thr–Ala a a A. psychrolactophilus ‘ group’ A3 A4 A11.27, A11.28 or A11.4, A11. 5, A11.6, A11.7 or Lys–Ala A11.35 , 2005; Kallimanis , 1995; Wieser 449). Data for reference genera , 2013); , 1997; Zhou 5 Kocuria ) MK-9(H ) et al. 2 et al. 2 d n other species. et al. et al. (Lys– (Lys– GL a a Paeniglutamicibacter A. citreus ‘ group’ A11.27 A4 Gly–Glu) A11.56 A3 Thr–Ala , 2013). , 2005a); ) ) ) MK-9(H ) MK-8, MK-9 MK-9, MK-10 (Niepel 2 2 2–3 2-3 d et al. et al. 22 2 2 22 2 ++ (Lys– (Lys– Arthrobacter sensu lato GL ww.dsmz.de/?id , no data available; MMK, methylmenaquinone. (Stackebrandt a a A. agilis ‘ group’ A3 Ser–Ala A3 Thr–Ala MK-9(H MK-9(H A11.22 A11.27 or A11.28 NA gen. nov., , 2006; Govender ) – 2 Sinomonas ), ) 2–3 , 2002; Li 2 2 et al. V (Lys– (Lys–Ala) –Gly 2 Micrococcus a a et al. Arthrobacter , Variable; A11.4 A3 7, MK-6(H A3 Ala MK-9(H MK-8(H Ala (Gly) A11.62 , 2008); V – et al. -Glu D , 2008); D d Glutamicibacter , 2006; Yoon ) as the predominant quinone (Huang NA NA NA -carboxyl , 2013). 2 a (Lys–Ala– (Lys– et al. a a (Altenburger et al. A. woluwensis A. nasiphocae A3 Gly) A11.47 MK-9, MK-10 MK-7 or MK- replaced by glycine) A11.60 Asp; group of A4 et al. gen. nov., , 2004b; Chou -Asp D § GLs Citricoccus d A. albus/ group’) , 2006; Zhou 2222 + +++++ ++++ + +++ et al. ) GL 2 -Glu or Lys– L -Glu) A11.42 or Lys–Gly– ( (Lys–Ala–Glu or L to contain MK-8(H et al. a a , 2009; Hamada , 2006); Pseudoglutamicibacter gen. nov. (‘ cumminsii MK-8(H A11.54 or A11.56 A4 MK-7 or MK-8 or MK-7, MK-8 or MK-8, MK-7, MK-9 or MK-8, MK-9 Gly– or Lys– A4 Lys–Ser–Glu) A11.35 or A11.58 and other groups of the genus , 2002; Li ) is that used by Schleifer & Kandler (1972). Information in parentheses indicates the type of inter- et al. et al. a )or ) 2 2 group’) et al. Lys– Pseudarthrobacter A. scleromae ( , 2004c, 2005b, 2008; Delgado 2 2 2 2 ) or MK- + ++ a 2 (Pukall -Asp) ciak D ´ , 2006; Mayilraj ), MK-8(H (Lys–Glu) 2 et al. ) and suggest that they correspond to MGDG and DMG (Govender a 2 A. sulfureus -Lys– , 2007; Tang Paeniglutamicibacter gen. nov. (‘ A2 or A4 MK-10 MK-8, MK-8(H MK-8(H L A11.pep or A11.31 peptide subunit or 7(H A4 A11.54 et al. ), ) gen. nov., ) ), 2 2 2 2 et al. Acaricomes , 2002; Pas , 2002b; Li gen. ) A11.6 or d et al. , 2005; Li 3–4 ), MK-9(H V V V ), MK-8(H 22 + 2 2 (Zhang et al. Arthrobacter sensu stricto GL(s) ) or MK-8(H ) or MK-8(H ) , 2011a); 2 2 2 et al. A. protophormiae ´ (Lys–Ala–Glu) (Lys–Ala a a Nesterenkonia suensis et al. Glutamicibacter nov. (‘ group’) A11.7 MK-8, MK-9 MK-8, MK-9 or or MK-8(H MK-7(H or MK-7 H MK-9(H A11.35 A4 A3 , 2000; Fan Paenarthrobacter et al. (Yassin Zhihengliuella , 1995; Collins * ) ) MK-7(H 2 V 2 +++ ++ , 2004; Tvrzova et al. (Lys–Ser– (Lys–Gly– a a A. oxydans , 2010); (Collins et al. Pseudarthrobacter gen. nov. (‘ group’) MK-9(H A3 A4 Thr–Ala) A11.23 Glu) A11.40/56 449. et al. ) 3 Auritidibacter 5 ) 2 Rothia ), 2 ) MK-9(H 2 22 2 22 2 2222222 2 2 2 2 (Stackebrandt (Lys–Ala– (Lys–Ala , 2003; Kim a a A. aurescens Paenarthrobacter gen. nov. (‘ group’) A3 MMK-10(H Thr–Ala) A11.17 A11.6 A3 et al. gen. nov. from each other and from ) 2–3 was reported to contain predominantly MK-8 and MK-9(H d ) MK-9(H 2 V 22 2 2 2 ++ ++ + ++ + ++ + ++ + Nesterenkonia (Lys–Gly– (Lys–Ala , 2004a, 2005c; Chen a a A. globiformis Arthrobacter sensu stricto (‘ group’) A11.5 or A11.6 L–Glu) A11.56 , 1999; Reddy et al. Chemotaxonomic traits that distinguish (Li et al. cs , 1983; Kusser & Fiedler, 1983); , 2000, 2007); ´ PL1–5 DMG PI TMDG DGDG PL1–5 MGDG PI MGDG DGDG DMG TMDG MGDG TraitQuinone(s) MK-10 Auritidibacter Acaricomes MK-10(H Citricoccus Kocuria Micrococcus Nesterenkonia Renibacterium Rothia Sinomonas Yaniella Zhihengliuella Trait Quinone(s) MK-9(H Peptidoglycan A4 Polar lipids GL Peptidoglycan A3 Polar lipids Not listed at http://www.dsmz.de/?id Glycolipid(s) was detected but chromatographic motility was not shown, which would be required in order to assign them to those identified as present i A. phenanthrenivorans D d §Chromatographic motilities of two glycolipids detected in Pseudoglutamicibacter peptide bridge. The four-digit code (Latin letter A/number/dot/number) specially indicates the composition of the interpeptide bridge (http://w Table 2. For the peptidoglycan composition, the three-digit code (Latin letter A/number/Greek letter * were taken from the following studies: Kova et al. Yaniella et al.

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A. gangotriensis, A. kerguelensis, A. psychrophenolicus and Description of Paenarthrobacter A. sulfureus are reclassified in the genus Paeniglutamicibacter histidinolovorans comb. nov. gen. nov. Finally, the species A. cumminsii and A. albus are Paenarthrobacter histidinolovorans (his9ti.di.no.lo.vor9ans. reclassified in the genus Pseudoglutamicibacter gen. nov. N.L. n. histidinolum histidinol; L. part. adj. vorans devour- ing, consuming; N.L. part. adj. histidinolovorans histidinol destroying).

Description of Paenarthrobacter gen. nov. Basonym: Arthrobacter histidinolovorans Adams 1954. Paenarthrobacter (Paen.ar9thro.bac9ter. L. adv. paene nearly, The description is as provided by Adams (1954) for almost; N.L. masc. n. Arthrobacter a bacterial genus name; Arthrobacter histidinolovorans with the following additional N.L. masc. n. Paenarthrobacter almost Arthrobacter). properties. In addition, it shares the characteristics listed in the genus description. According to Kodama et al. (1992), The peptidoglycan type is A3a (variation Lys–Ala–Thr–Ala; the predominant fatty acids of the type strain (JCM 2520T) A11.17). The quinone system contains menaquinone MK- are anteiso-C15 : 0, followed by anteiso-C17 : 0. Minor amounts 9(H2) predominantly. The polar lipid profile is composed of iso-C14 : 0,iso-C15 : 0,iso-C16 : 0,iso-C17 : 0,C14 : 0 and C16 : 0 of the major compounds diphosphatidylglycerol, phospha- and traces of C18 : 0 may also be present. L-Arginine, L- tidylglycerol, phosphatidylinositol, dimannosylglyceride asparagine, L-histidine, L-arabinose, D-galactose, D-glucose, and monogalactosyldiacylglycerol and minor amounts of D-ribose, D-xylose, histidinol, inositol, 4-aminobutyrate and trimannosyldiacylglycerol (Collins et al., 1981, 1982b; this p-hydroxybenzoate are utilized as carbon sources, but not study). The major fatty acid is anteiso-C15 : 0. Large L-leucine, butanediol or malonate. Citric acid, formic acid, amounts of iso-C15 : 0, iso-C16 : 0, anteiso-C17 : 0 and iso- propionic acid and uric acid are assimilated, but not adipic + C14 : 0 may also be present. The G C content of the geno- acid, benzoic acid, malonic acid or pimelic acid. Utilization mic DNA is in the range 61.3–62.5 mol%. The type species of L-rhamnose and assimilation of glutaric acid are weak. is Paenarthrobacter aurescens. Urea is formed from creatinine and uric acid. Nitrate is not reduced to nitrite, and no growth occurs in the presence of 10 % (w/v) NaCl. Starch is not hydrolysed. Does not produce nicotine blue. T5 T5 Description of Paenarthrobacter aurescens The type strain is ATCC 11442 CCUG 23888 CIP T5 T5 T5 comb. nov. 106988 DSM 20115 IFO (now NBRC) 15510 JCM 2520T5LMG 3822T5VKM Ac-1978T.TheG+Ccontentof Paenarthrobacter aurescens (au.res9cens. L. v. auresco to theDNAofthetypestrainis62.6mol%(HPLC;Kodama become golden; L. part. adj. aurescens becoming golden). et al., 1992). Basonym: Arthrobacter aurescens Phillips 1953. The description is as provided by Phillips (1953) for Description of Paenarthrobacter ilicis comb. nov. Arthrobacter aurescens with the following additional prop- Paenarthrobacter ilicis (i.li9cis. N.L. n. Ilex -icis a scientific erties. Shares the characteristics listed in the genus descrip- botanical genus name; N.L. gen. n. ilicis of Ilex). tion. According to Kodama et al. (1992), the predominant T fatty acid of the type strain (IAM 12340 ) is anteiso-C15 : 0, Basonym: Arthrobacter ilicis Collins et al. 1982. followed by anteiso-C . Minor fatty acids are iso-C , 17 : 0 15 : 0 The description is as provided by Collins et al. (1981) for iso-C , iso-C and C . Starch is hydrolysed. 16 : 0 17 : 0 16 : 0 Arthrobacter ilicis with the following additional properties. L-Arginine, L-asparagine, L-histidine, L-arabinose, D-galac- Shares the characteristics listed in the genus description. tose, D-glucose, D-ribose, D-xylose, 4-aminobutyrate and Predominant fatty acid of the type strain is anteiso-C , p-hydroxybenzoate are utilized as carbon sources, but not 15 : 0 followed by anteiso-C17 : 0. Minor fatty acids are iso- L-leucine, L-rhamnose, inositol or malonate. Citric acid, C , iso-C ,C and C and traces of iso-C formic acid and uric acid are assimilated, but not benzoic 15 : 0 16 : 0 14 : 0 16 : 0 14 : 0 may also be present (Kodama et al., 1992). According to acid, glutaric acid, malonic acid, pimelic acid or propionic Kodama et al. (1992), the type strain is positive for utiliz- acid. Utilization of butanediol and histidinol and assimila- ation of the carbon sources L-arginine, L-asparagine, L-his- tion of adipic acid are weak. Urea is formed from uric acid. tidine, L-arabinose, D-galactose, D-glucose, D-ribose, D- Nitrate is not reduced to nitrite, and no growth occurs in xylose, inositol, 4-aminobutyrate and p-hydroxybenzoate, the presence of 10 % (w/v) NaCl. Does not produce nicotine but negative for L-leucine, butanediol and malonate. blue. Citric acid, propionic acid and uric acid are assimilated, The type strain is ATCC 13344T5CIP 102364T5DSM but not adipic acid, benzoic acid, glutaric acid, malonic T T T 20116 5HAMBI 1850 5IFO (now NBRC) 12136 5JCM acid or pimelic acid. Utilization of L-rhamnose and histidi- 1330T5LMG 3815T5NRRL B-2879T5VKM Ac-1105T. nol and assimilation of formic acid are weak. Urea is The G+C content of the genomic DNA of the type formed from uric acid but not from creatinine. Does not strain is 61.9 mol% (HPLC; Kodama et al., 1992). reduce nitrate to nitrite. Does not hydrolyse starch. Does

Downloaded from www.microbiologyresearch.org by http://ijs.microbiologyresearch.org 25 IP: 54.70.40.11 On: Mon, 04 Feb 2019 19:10:17 H.-J. Busse not grow in the presence of 10 % (w/v) NaCl. Does not but the polar lipid profile is unknown. Predominant fatty produce nicotine blue. According to Kotoucˇkova´ et al. acid of the type strain is anteiso-C15 : 0, followed by ante- (2004), the type strain uses D-xylose, uridine and sucrose iso-C17 : 0.Minorfattyacidsareiso-C14 : 0,iso-C15 : 0,iso- for respiration and uses propionic acid, melibiose, 3- C16 : 0,iso-C17 : 0,C16 : 0 and C18 : 0 (Kodama et al., 1992). methyl glucose, raffinose and salicin weakly. Gluconate is According to Kodama et al. (1992), the type strain does not utilized and arbutin and a-cyclodextrin are not utilized not reduce nitrate to nitrite, does not hydrolyse starch and for respiration. Positive for pyrrolidonyl arylamidase and does not grow in the presence of 10 % (w/v) NaCl. Utilizes negative for elastase and oxidase. Aesculin and starch are L-arginine, L-asparagine, L-arabinose, D-galactose, D-glucose, not hydrolysed. D-xylose, inositol, 4-aminobutyrate and p-hydroxybenzoate, but not L-histidine, L-leucine, L-rhamnose, butanediol or The type strain is ATCC 14264T5DSM 20138T5NCPPB malonate. Citric acid, formic acid, propionic acid and uric 1228T. acid are hydrolysed, but not adipic acid, benzoic acid, malonic acid or pimelic acid. Utilization of D-ribose and Description of Paenarthrobacter nicotinovorans histidinol and assimilation of glutaric acid are weak. Does comb. nov. not reduce nitrate to nitrite. Does not produce nicotine blue. T5 T5 Paenarthrobacter nicotinovorans (ni.co.ti9no.vo9rans.N.L.n. The type strain is ATCC 7562 CIP 67.3 DSM T5 T5 T5 nicotinum nicotine; L. part. adj. vorans devouring, destroying; 20126 IFO (now NBRC) 12140 JCM 1337 LMG T5 T + N.L. part. adj. nicotinovorans nicotine devouring). 3812 VKM Ac-1121 .TheG C content of the DNA of the type strain is 63.6 mol% (HPLC; Kodama et al., 1992). Basonym: Arthrobacter nicotinovorans Kodama et al. 1992.

The description is as provided by Kodama et al. (1992) for Description of Pseudarthrobacter gen. nov. Arthrobacter nicotinovorans with the following additional properties. Shares the characteristics listed in the genus Pseudarthrobacter (Pseu.dar9thro.bac9ter. Gr. adj. pseudeˆs description, but the polar lipid profile is unknown. false; N.L. masc. n. Arthrobacter a bacterial genus name; N.L. masc. n. Pseudarthrobacter the false Arthrobacter). The type strain is SAM 1563T (5ATCC 49919T5CIP 106990T5DSM 420T5IFO (now NBRC) 15511T5JCM The peptidoglycan type is A3a (variation Lys–Ser–Thr-Ala; 3874T5LMG 16253T5VKM Ac-1988T). A11.23). The quinone system contains major amounts of MK-9(H2) but one species, Pseudarthrobacter scleromae, was originally described to contain predominantly Description of Paenarthrobacter MK-8(H2). The polar lipid profile contains the major nitroguajacolicus comb. nov. compounds diphosphatidylglycerol, phosphatidylinositol, Paenarthrobacter nitroguajacolicus (ni.tro.gu.a.ja.co9li.cus. dimannosylglyceride, monogalactosyldiacylglycerol, mod- N.L. neut. n. nitroguajacolum nitroguaiacol; L. suff. -icus erate to major amounts of phosphatidylglycerol and minor -a -um used with the sense of belonging to; N.L. masc. amounts of trimannosyldiacylglycerol (Collins et al. 1982b; adj. nitroguajacolicus pertaining to nitroguaiacol). Amadi & Alderson, 1992; this study) may also be present. The major fatty acid is anteiso-C15 : 0. Large amounts of iso- Basonym: Arthrobacter nitroguajacolicus Kotoucˇkova´ et al. C15 : 0,iso-C16 : 0,anteiso-C17 : 0 and iso-C14 : 0 may also be pre- 2004. sent. The G+C content of the genomic DNA is in the range The description is as provided by Kotoucˇkova´ et al. (2004) 62.0–71 mol%. The type species is Pseudarthrobacter for Arthrobacter nitroguajacolicus with the following polychromogenes. additional properties. Shares the characteristics listed in the genus description, but the polar lipid profile is unknown. Description of Pseudarthrobacter The type strain is G2-1T (5CCM 4924T5DSM 15232T5 polychromogenes comb. nov. T JCM 14115 ), isolated from forest soil. Pseudarthrobacter polychromogenes (po.ly.chro.mo9ge.nes. Gr. adj. polys many; Gr. n. chroma colour; Gr. v. gennaio produce; N.L. part. adj. polychromogenes producing many colours). Description of Paenarthrobacter ureafaciens comb. nov. Basonym: Arthrobacter polychromogenes Schippers-Lammertse et al. 1963. Paenarthrobacter ureafaciens (u.re.a.fa9ci.ens. N.L. n. urea urea; L. v. facio to make, to produce; N.L. part. adj. ureafa- The description is as provided by Schippers-Lammertse ciens urea-producing). et al. (1963) for Arthrobacter polychromogenes with the fol- lowing additional properties. Shares the characteristics Basonym: Arthrobacter ureafaciens Clark 1955. listed in the genus description. The predominant fatty The description is as provided by Clark (1955) for Arthrobac- acid is anteiso-C15 : 0, followed by anteiso-C17 : 0 and ter ureafaciens with the following additional properties. C16 : 0. Minor fatty acids are iso-C14 : 0, iso-C15 : 0, iso- Shares the characteristics listed in the genus description, C14 : 0, iso-C16 : 0,C14 : 0 and C15 : 0 (Kodama et al., 1992). Downloaded from www.microbiologyresearch.org by 26 International Journal of Systematic and Evolutionary Microbiology 66 IP: 54.70.40.11 On: Mon, 04 Feb 2019 19:10:17 Taxonomy of the genus Arthrobacter

The type strain is positive for utilization of the carbon The peptidoglycan type, quinone system, polar lipid profile sources L-arginine, L-asparagine, L-histidine, L-arabinose, and fatty acid profile are in agreement with the genus D-galactose, D-glucose, L-rhamnose, D-ribose, D-xylose description, but a glycolipid corresponding to trimannosyl- and malonate, but does not utilize inositol. Utilization of diacylglycerol is not detected. L-leucine and butanediol is weak. Citric acid, formic acid, The type strain is IMMIB L-1606T (5CCUG 59597T5DSM propionic acid and uric acid are assimilated, but not 23395T). adipic acid, benzoic acid, glutaric acid, malonic acid or pimelic acid. Reduces nitrate to nitrite. Does not produce nicotine blue (Kodama et al. 1992). The type strain is ATCC 15216T5BCRC 12114T5CCUG Description of Pseudarthrobacter niigatensis 23891T5CIP 106989T5CGMCC 1.1927T5DSM 20136T5 comb. nov. T5 T5 T5 IFO (now NBRC) 15512 IAM 14590 JCM 2523 Pseudarthrobacter niigatensis (ni.i.ga.ten9sis. N.L. masc. adj. T5 T5 T5 T KCTC 3384 LMG 3821 NCIB 10267 VKM Ac-1955 . niigatensis pertaining to the Niigata region, Japan). The G+C content of the genomic DNA of the type strain is 62.9 mol% (HPLC; Kodama et al., 1992). Basonym: Arthrobacter niigatensis Ding et al. 2009. The description is as provided by Ding et al. (2009) for Description of Pseudarthrobacter Arthrobacter niigatensis with the following additional prop- chlorophenolicus comb. nov. erties. The peptidoglycan type, quinone system and fatty acid profile are in agreement with the genus description, Pseudarthrobacter chlorophenolicus (chlo.ro.phe.no9li.cus. but the polar lipid profile is unknown. N.L. neut. n. chlorophenolum chlorophenol; L. masc. suff. The type strain is LC4T (5CCTCC AB 206012T5JCM -icus used with the sense of pertaining to; N.L. masc. adj. T chlorophenolicus pertaining to chlorophenols). 30147 ). Basonym: Arthrobacter chlorophenolicus Westerberg et al. 2000. Description of Pseudarthrobacter oxydans The description is as provided by Westerberg et al. (2000) comb. nov. for Arthrobacter chlorophenolicus with the following additional properties. The peptidoglycan type, quinone Pseudarthrobacter oxydans (o.xy9dans. N.L. part. adj. oxydans system and fatty acid profile are in agreement with the oxidizing). genus description, but the polar lipid profile is unknown. Basonym: Arthrobacter oxydans Sguros 1954. The type strain is strain A6T (5ATCC 700700T5CIP The description is as provided by Sguros (1954) for Arthro- 107037T5DSM 12829T5JCM 12360T5KCTC 9906T5 bacter oxydans with the following additional properties. NCIMB 13794T). The quinone system, fatty acid profile, polar lipid profile and peptidoglycan type are in accordance with the genus Description of Pseudarthrobacter defluvii comb. description but, in addition, the polar lipid profile is also nov. reported to contain digalactosyldiacylglycerol (Amadi & Alderson, 1982). The predominant fatty acid is anteiso- Pseudarthrobacter defluvii (de.flu9vi.i. L. gen. n. defluvii of C15 : 0, followed by anteiso-C17 : 0,C16 : 0, iso-C16 : 0 and sewage). iso-C15 : 0. Minor fatty acids are iso-C14 : 0, iso-C17 : 0, Basonym: Arthrobacter defluvii Kim et al. 2008. C14 : 0 and C15 : 0 (Kodama et al., 1992). According to Kodama et al. (1992), the type strain is positive for utiliz- The description is as provided by Kim et al. (2008) for ation of the carbon sources L-arginine, L-asparagine, L-his- Arthrobacter defluvii with the following additional proper- tidine, L-arabinose, D-galactose, D-glucose, L-rhamnose, D- ties. The peptidoglycan type, quinone system and fatty acid ribose, D-xylose and malonate but does not utilize inositol. profile are in agreement with the genus description, but the Utilization of L-leucine and butanediol is weak. Citric acid, polar lipid profile is unknown. formic acid, propionic acid and uric acid are assimilated, The type strain is 4C1-aT (5KCTC 19209T5DSM 18782T). but not adipic acid, benzoic acid, glutaric acid, malonic acid or pimelic acid. Reduces nitrate to nitrite. Does not produce nicotine blue. Description of Pseudarthrobacter equi comb. nov. The type strain is ATCC 14358T5BCRC (formerly CCRC) Pseudarthrobacter equi (e9qui. L. gen. n. equi of the horse). 11573T5CCUG 17757T5CIP 107005T5DSM 20119T5 HAMBI 1857T5IFO (now NBRC) 12138T5IMET 10684T5 Basonym: Arthrobacter equi Yassin et al. 2011. JCM 2521T5LMG 3816T5NCIMB 9333T5NRIC 0154T5 The description is as provided by Yassin et al. (2011b) for VKM Ac-1114T.TheG+C content of the genomic DNA of Arthrobacter equi with the following additional properties. thetypestrainis63.1mol%(HPLC;Kodamaet al., 1992).

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Description of Pseudarthrobacter Description of Pseudarthrobacter sulfonivorans phenanthrenivorans comb. nov. comb. nov. Pseudarthrobacter phenanthrenivorans (phe.nan9thre.ni.vo9rans. Pseudarthrobacter sulfonivorans (sul.fo9ni.vo9rans. N.L. n. N.L. n. phenanthrenum phenanthrene; L. part. adj. vorans sulfonum sulfone group; L. v. vorare to devour; N.L. adj. devouring, digesting; N.L. part. adj. phenanthrenivorans sulfonivorans sulfone-devouring). digesting phenanthrene). Basonym: Arthrobacter sulfonivorans Borodina et al. 2002. Basonym: Arthrobacter phenanthrenivorans Kallimanis et al. The description is as provided by Borodina et al. (2002) for 2009. Arthrobacter sulfonivorans with the following additional The description is as provided by Kallimanis et al. (2009) for properties. The peptidoglycan type, quinone system and Arthrobacter phenanthrenivorans with the following additional fatty acid profile are in agreement with the genus descrip- properties. In contrast to the genus description, the quinone tion, but the polar lipid profile is unknown. system consists predominantly of MK-8 and relatively large The type strain is ALLT (5ATCC BAA-112T5DSM amounts of MK-9(H ); the polar lipid profile contains phos- 2 14002T5IAM 15312T5JCM 13520T). phatidylethanolamine and glycolipids are absent. The type strain is Sphe3T (5DSM 18606T5JCM 16027T5 T LMG 23796 ). Description of Glutamicibacter gen. nov. Glutamicibacter (Glu.ta.mi9ci.bac9ter. N.L. n. acidum gluta- micum glutamic acid; N.L. masc. n. bacter a rod; N.L. masc. n. Glutamicibacter glutamic acid rod, referring to the pre- Description of Pseudarthrobacter scleromae sence of glutamic acid in the peptidoglycan interpeptide comb. nov. bridge). Pseudarthrobacter scleromae (scle.ro9mae. N.L. gen. n. scleromae Based on available data for the type species and other species of scleroma, a hardened part). assigned to the genus, the peptidoglycan type is A4a (Lys– Ala–Glu; A11.35). The quinone system contains exclusively Basonym: Arthrobacter scleromae Huang et al. 2005. unsaturated menaquinones (MK-8 and/or MK-9). The The description is as provided by Huang et al. (2005) for polar lipid profile is composed of the major compounds Arthrobacter scleromae with the following additional prop- diphosphatidylglycerol, phosphatidylglycerol and dimanno- erties. In contrast to the genus description, the major syldiacylglycerol. Monogalactosyldiacylglycerol and minor menaquinone is MK-8(H2). The polar lipid profile contains amounts of trimannosyldiacylglycerol may also be present. the major glycolipids dimannosylglyceride and monogalac- Phosphatidylinositol is absent. The major fatty acid is ante- tosyldiacylglycerol, but the presence of other lipids has not iso-C15 : 0. Relatively large amounts of iso-C15 : 0,iso-C16 : 0, been studied (Pas´ciak et al., 2010). anteiso-C17 : 0 and C16 : 0 may also be present. The G+C content of the genomic DNA is in the range 55–67 mol%. The type strain is YH-2001T (5CGMCC 1.3601T5CIP The type species is Glutamicibacter protophormiae. 108992T5DSM 17756T5JCM 12642T).

Description of Glutamicibacter protophormiae comb. nov. Description of Pseudarthrobacter siccitolerans Glutamicibacter protophormiae (pro.to.phor9mi.ae. N.L. comb. nov. gen. n. protophormiae of Protophormia, a genus of dipteran insects, referring to the isolation of the type strain from Pseudarthrobacter siccitolerans (sic.ci.to9le.rans. L. adj. Protophormia terraenovae). siccus dry; L. part. adj. tolerans tolerating; N.L. part. adj. siccitolerans tolerating dryness). Basonyms: Brevibacterium protophormiae Lysenko 1959; Arthrobacter protophormiae Stackebrandt et al. 1984. Basonym: Arthrobacter siccitolerans SantaCruz-Calvo et al. 2013. The description is as provided by Stackebrandt et al. (1983) for Arthrobacter protophormiae with the following The description is as provided by SantaCruz-Calvo et al. additional properties. Shares the characteristics listed in (2013) for Arthrobacter siccitolerans with the following the genus description (Collins & Kroppenstedt, 1983). additional properties. Shares the peptidoglycan type, qui- According to Osorio et al. (1999), the type strain is negative none system and fatty acid profile listed in the genus for urease and b-galactosidase. Positive for nitrate description, but the polar lipid profile is unknown. reduction and pyrazinamidase. Assimilates cellobiose, gly- The type strain is 4J27T (5CECT 8257T5LMG 27359T). cerol, maltose and 5-ketogluconate. Amygdalin, arbutin, The G+C content of the genomic DNA of the type D-arabitol, galactose, D-mannose, turanose, D-xylose, L-ara- strain is 65.3 mol% (HPLC). binose, inositol, mannitol, melibiose, rhamnose, ribose,

Downloaded from www.microbiologyresearch.org by 28 International Journal of Systematic and Evolutionary Microbiology 66 IP: 54.70.40.11 On: Mon, 04 Feb 2019 19:10:17 Taxonomy of the genus Arthrobacter salicin, starch, sucrose, trehalose, xylitol, gentiobiose and Description of Glutamicibacter creatinolyticus N-acetylglucosamine are not assimilated. comb. nov. The type strain is ATCC 19271T5CIP 106987T5DSM Glutamicibacter creatinolyticus [cre.a.ti9no.ly9ti.cus. N.L. n. 20168T5IFO (now NBRC) 12128T5JCM 1973T5LMG creatininum creatinine; N.L. masc. adj. lyticus (from Gr. 16324T5VKM Ac-2104T. masc. adj. lutikos) able to loose, able to dissolve; N.L. masc. adj. creatinolyticus creatinine-hydrolysing].

Description of Glutamicibacter ardleyensis Basonym: Arthrobacter creatinolyticus Hou et al. 1998. comb. nov. The description is as provided by Hou et al. (1998) for Glutamicibacter ardleyensis (ard.le.yen9sis. N.L. masc. adj. Arthrobacter creatinolyticus with the following additional ardleyensis pertaining to Ardley, where the type strain was properties. The peptidoglycan composition and quinone isolated). system are in accordance with the genus description, but the polar lipid and fatty acid profiles are unknown. Basonym: Arthrobacter ardleyensis Chen et al. 2005. The type strain is CCM 4673T (5CIP 105749T5DSM T T T The description is as provided by Chen et al. (2005) for 15881T5GIFU 12498 5JCM 10102 5KCTC 9903 5LMG Arthrobacter ardleyensis with the following additional prop- 22054T). erties. The peptidoglycan composition, quinone system and fatty acid profile are in accordance with the genus description, but the polar lipid profile is unknown. Description of Glutamicibacter mysorens The type strain is An25T (5CGMCC 1.3685T5DSM comb. nov. 17432T5JCM 12921T). Glutamicibacter mysorens (my.so9rens. mysorens pertaining to Mysore, where the organisms were first isolated). Description of Glutamicibacter arilaitensis Basonym: Arthrobacter mysorens Nand and Rao 1972. comb. nov. The description is as provided by Nand & Rao (1972) for Glutamicibacter arilaitensis (a.ri.lai.ten9sis. N.L. masc. adj. Arthrobacter mysorens with the following additional arilaitensis of Arilait, arbitrary name formed to honour Ari- properties. According to Wink (2012), the fatty acid profile lait-Recherches, a research association that coordinates the is composed predominantly of anteiso-C15 : 0, with moder- collective research programmes of the professional French ate amounts of iso-C15 : 0,iso-C16 : 0 and anteiso-C17 : 0 and dairy federations). minor amounts of iso-C14 : 0,C16 : 0,iso-C17 : 0 and C18 : 0. The patent strain ATCC 31021 has been shown to contain Basonym: Arthrobacter arilaitensis Irlinger et al. 2005. the peptidoglycan type Lys–Ala–Glu (Stackebrandt et al., The description is as provided by Irlinger et al. (2005) for 1983). Information concerning the quinone system and Arthrobacter arilaitensis with the following additional prop- polar lipid profile is not available. According to Irlinger erties. The peptidoglycan composition is in accordance et al. (2005), the species is positive for b-galactosidase with the genus description, but the quinone system and but negative for urease and gelatinase, hydrolysis of aescu- polar lipid and fatty acid profiles are unknown. lin and reduction of nitrate to nitrite. It utilizes 5-amino- valerate, (()-quinate, a-D(+)-glucose, D-xylose, D-ribose, The type strain is Re117T (5CIP 108037T5DSM 16368T5 L-arabinose, D-galactose and glycerol, but not DL-glycerate, IAM 153185JCM 13566T). lactose, L-rhamnose or D-xylitol. The type strain is ATCC 33408T5CIP 102716T5JCM 11565T5LMG 16219T5NBRC 103060T5NCIB (now Description of Glutamicibacter bergerei T comb. nov. NCIMB) 10583 . Glutamicibacter bergerei (ber.ge9re.i.N.L.gen.n.bergerei of Berge`re, to honour Jean-Louis Berge`re, a French microbio- Description of Glutamicibacter nicotianae logist). comb. nov. Basonym: Arthrobacter bergerei Irlinger et al. 2005. Glutamicibacter nicotianae (ni.co.ti.a9nae. N.L. gen. n. nico- tianae of Nicotiana, the tobacco plant). The description is as provided by Irlinger et al. (2005) for Arthrobacter bergerei with the following additional proper- Basonym: Arthrobacter nicotianae Giovannozzi-Sermanni ties. The peptidoglycan composition is in accordance with 1959. the genus description, but the quinone system and polar The description is as provided by Giovannozzi-Sermanni lipid and fatty acid profiles are unknown. (1959) and emended by Stackebrandt et al. (1983) for The type strain is Ca106T (5CCUG 523425CIP 108036T5 Arthrobacter nicotianae with the following additional DSM 16367T). properties. Shares the characteristics listed in the genus

Downloaded from www.microbiologyresearch.org by http://ijs.microbiologyresearch.org 29 IP: 54.70.40.11 On: Mon, 04 Feb 2019 19:10:17 H.-J. Busse description. According to Margesin et al. (2004), the type Basonym: Arthrobacter uratoxydans Stackebrandt et al. 1984. strain reduces nitrate. Positive for catalase and negative The description is as provided by Stackebrandt et al. (1983) for oxidase and urease. H S is not produced from thiosul- 2 for Arthrobacter uratoxydans with the following additional fate and indole is not produced. Alkaline phosphatase, a- properties. The peptidoglycan composition and quinone glucosidase, leucine arylamidase, esterase lipase (C8), system are in accordance with the genus description; the esterase (C4), pyrazinamidase and pyrrolidonyl fatty acid profile is in agreement with the genus descrip- arylamidase are present and skimmed milk is hydrolysed tion, consisting of the major fatty acid anteiso-C , fol- at 25 uC but not at 10 uC. Does not grow at pH 5 or 11. 15 : 0 lowed by iso-C , anteiso-C and iso-C . Minor Arabinose, glucose, gluconate, maltose, malate and citrate 15 : 0 17 : 0 17 : 0 fatty acids are iso-C , iso-C ,C and C are assimilated, but mannitol, mannose, mannitol, N- 16 : 0 14 : 0 16 : 0 18 : 0 (Funke et al., 1996). According to Osorio et al. (1999), acetylglucosamine, adipate, caprate and phenylacetate the type strain is negative for b-galactosidase. Positive for arenot.Argininedihydrolase,a-galactosidase, N-acetyl- nitrate reduction, urease and pyrazinamidase. Assimilates b-glucosaminidase, lipase (C14), gelatin hydrolysis, trypsin, glycerol, ribose and N-acetylglucosamine. Amygdalin, a-chymotrypsin, a-fucosidase, b-lactamase and pectate arbutin, cellobiose, D-arabitol, galactose, maltose, D-man- lyase are negative. n-Hexadecane and diesel oil are not uti- nose, turanose, D-xylose, L-arabinose, mannitol, melibiose, lized for growth. Glucose, ribose, xylose, mannitol, maltose, rhamnose, salicin, starch, sucrose, trehalose, xylitol, lactose, sucrose and glycogen are not fermented. Susceptible 2 2 gentiobiose and 5-ketogluconate are not assimilated. to ampicillin (8 mg l 1), imipenem (16 mg l 1)andcotri- 2 moxazole (sulfamethoxazole+trimethoprim, 16 mg l 1) The type strain is ATCC 21749T5CIP 102367T5DSM 2 and weakly susceptible to amikacin (16 mg l 1). Resistant 20647T5IFO (now NBRC) 15515T5JCM 11944T5KCTC 2 2 to aztreonam (32 mg l 1), cefamandole (16 mg l 1), cefo- 3482T5NCDO 2282T5NCIMB 702282T5LMG 16220T5 2 2 taxime (16 mg l 1), ceftazidime (16 mg l 1), ciprofloxacin VKM Ac-1979T. 2 2 (16 mg l 1), mezlocillin (16 mg l 1), norfloxacin (8 mg 2 2 l 1) and tetracycline (4 mg l 1). Additional traits were reported for the type strain by Osorio et al. (1999) as follows. The type strain is negative for b-galactosidase. Amygdalin, Description of Paeniglutamicibacter gen. nov. arbutin, cellobiose, D-arabitol, D-xylose, galactose, glycerol, L-arabinose, maltose, ribose, salicin, starch and gentiobiose Paeniglutamicibacter (Pae.ni.glu.ta.mi9ci.bac9ter. L. adv. paene are assimilated, but not D-mannose, turanose, inositol, man- nearly, almost; N.L. masc. n. Glutamicibacter abacterial nitol, melibiose, rhamnose, sucrose, trehalose, xylitol, N- genus name; N.L. masc. n. Paeniglutamicibacter almost acetylglucosamine or 5-ketogluconate. Glutamicibacter). T T The type strain is AS 1.1895 [5ATCC 15236 5CCM The peptidoglycan type is A4a (Lys–Glu; A11.54). The qui- T T T 1648 5BCRC (formerly CCRC) 11219 5CCUG 23842 5 none system contains exclusively unsaturated menaqui- T T T T CDA 883 5CIP 82.107 5DSM 20123 5HAMBI 1859 5 nones, with MK-9 or MK-10 predominating. The polar T T T IAM 12342 5IFO (now NBRC) 14234 5IMET 10353 5 lipid profile is composed of the major compounds dipho- T T T T JCM 1333 5LMG 16305 5NCIMB 9458 5NRIC 0153 ]. sphatidylglycerol, phosphatidylglycerol and digalactosyldia- cylglycerol. Phosphatidylinositol is absent. The major fatty acid is anteiso-C . Large amounts of iso-C , iso- Description of Glutamicibacter soli comb. nov. 15 : 0 15 : 0 C16 : 0, anteiso-C17 : 0 and C16 : 0 may also be present. The Glutamicibacter soli (so9li. L. neut. gen. n. soli of soil). G+C content of the genomic DNA is in the range 58– 68 mol%. The type species is Paeniglutamicibacter sulfureus. Basonym: Arthrobacter soli Roh et al. 2008. The description is as provided by Roh et al. (2008) for Arthrobacter soli with the following additional properties. The fatty acid profile is in accordance with the genus description. The quinone system is composed of MK-8, Description of Paeniglutamicibacter sulfureus MK-9, MK-7 and MK-10 (55 : 36 : 2 : 1; Peter Schumann, comb. nov. personal communication), but neither the polar lipid pro- Paeniglutamicibacter sulfureus (sul.fu9re.us. L. masc. adj. file nor the peptidoglycan composition is known. sulfureus of or like sulfur, meaning sulfur-coloured). T T T The type strain is SYB2 (5KCTC 19291 5DSM 19449 ). Basonym: Arthrobacter sulfureus Stackebrandt et al. 1984. The description is as provided by Stackebrandt et al. (1983) Description of Glutamicibacter uratoxydans for Arthrobacter sulfureus. Shares the properties given in the comb. nov. genus description. Glutamicibacter uratoxydans (u.ra.to9xy.dans. N.L. n. The type strain is ATCC 19098T5CIP 106986T5DSM uratum salt of uric acid; N.L. part. adj. oxydans oxidizing; 20167T5IFO (now NBRC) 12678T5JCM 1338T5LMG N.L. part. adj. uratoxydans uric acid oxidizing). 16694T5NRRL B-14730T.

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Description of Paeniglutamicibacter antarcticus The type strain is LI3T (5DSM 22826T5JCM 17806T5 comb. nov. NCCB 100315T). Paeniglutamicibacter antarcticus (an.tarc9ti.cus. L. masc. adj. antarcticus southern, used to refer to the Antarctic, referring to the isolation of the type strain from Antarctic Description of Paeniglutamicibacter marine sediment). gangotriensis comb. nov. Basonym: Arthrobacter antarcticus Pindi et al. 2010. Paeniglutamicibacter gangotriensis (gan.go9tri.en9sis. N.L. The description is as provided by Pindi et al. (2010) for masc. adj. gangotriensis of or pertaining to the Indian Ant- Arthrobacter antarcticus with the following additional arctic station Dakshin Gangotri). properties. Shares the quinone system and fatty acid profile Basonym: Arthrobacter gangotriensis Gupta et al. 2004. listed in the genus description but, in contrast to the genus description, the polar lipid profile is reported to be com- The description is as provided by Gupta et al. (2004) for posed only of phosphatidylethanolamine and diphosphati- Arthrobacter gangotriensis with the following additional dylglycerol and not to contain any glycolipid. properties. The peptidoglycan structure, fatty acid profile and quinone system are in accordance with the genus T T T The type strain is SPC26 (5LMG 24542 5NCCB 100228 ). description. The polar lipid profile is unknown. The type strain is Lz1yT (5CIP 108630T5DSM 15796T5 Additional information. The information on the pepti- JCM 12166T). doglycan composition given by Pindi et al. (2010) has not been added to the species description because it may cause confusion. In the species description for Arthro- bacter antarcticus, the authors state ‘The peptidoglycan Description of Paeniglutamicibacter diamino acids are lysine and alanine and the acyl type is kerguelensis comb. nov. a glutamic acid (A4 variation)’. Firstly, alanine is not a Paeniglutamicibacter kerguelensis (ker.gu.el.en9sis. N.L. diamino acid. Secondly, from the presence of the amino masc. adj. kerguelensis of or pertaining to the Kerguelen acids lysine, alanine and glutamic acid, the peptidoglycan Islands, Antarctica). variation A4a cannot be concluded because the majority of bacteria with the diamino acid lysine also contain Basonym: Arthrobacter kerguelensis Gupta et al. 2004. glutamic acid at position two of the peptide side chain. In The description is as provided by Gupta et al. (2004) for order to reach conclusions on the peptidoglycan type, at Arthrobacter kerguelensis with the following additional least relative amounts of the different amino acids must properties. The peptidoglycan structure, fatty acid profile be provided. Thirdly, the acyl type is never glutamic acid, and quinone system are in accordance with the genus but is either acetyl or glycolyl (Uchida & Seino, 1997). description. The polar lipid profile is unknown. The type strain is KGN15T (5CIP 108629T5DSM 15797T5 T Description of Paeniglutamicibacter cryotolerans JCM 12165 ). comb. nov. Paeniglutamicibacter cryotolerans (cry.o.to9ler.ans. N.L. pref. cryo from Gr. adj. kry´os cold; L. part. adj. tolerans Description of Paeniglutamicibacter tolerating, enduring; N.L. part. adj. cryotolerans cold- psychrophenolicus comb. nov. tolerating). Paeniglutamicibacter psychrophenolicus [psy.chro.phe.no9 Basonym: Arthrobacter cryotolerans Ganzert et al. 2011. li.cus. Gr. adj. psychros cold; N.L. masc. adj. phenolicus relating to phenol; N.L. masc. adj. psychrophenolicus relat- The description is as provided by Ganzert et al. (2011) for ing to phenol (degradation) at low temperatures]. Arthrobacter cryotolerans with the following additional properties and modifications. The peptidoglycan compo- Basonym: Arthrobacter psychrophenolicus Margesin et al. 2004. sition and quinone system are in accordance with the The description is as provided by Margesin et al. (2004) for genus description. In contrast to the genus description, Arthrobacter psychrophenolicus, except that the polar lipid C is the second most abundant fatty acid, and relatively 18 : 0 profile is composed of diphosphatidylglycerol, phosphati- large amounts of C ,C and C v9c (5–11 %) are 16 : 0 18 : 2 18 : 1 dylglycerol and digalactosyldiacylglycerol and phospha- present. Contrary to the species description for tidylinositol is absent (Fig. 3i). Arthrobacter cryotolerans, the polar lipid profile contains diphosphatidylglycerol, phosphatidylglycerol, digalactosyl- The type strain is AG31T (5CIP 108593T5DSM 15454T5 diacylglycerol and two minor lipids (Fig. 3j). IAM 15315T5JCM 135685LMG 21914T).

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Description of Pseudoglutamicibacter gen. nov. Status of the remaining species of the genus Arthrobacter Pseudoglutamicibacter (Pseu9do.glu.ta.mi9ci.bac9ter. Gr. adj. pseudeˆs false; N.L. masc. n. Glutamicibacter a bacterial The data discussed in this study strongly suggest that the genus name; N.L. masc. n. Pseudoglutamicibacter false genus Arthrobacter sensu stricto should be restricted to the Glutamicibacter). four species A. globiformis, A. pascens, A. oryzae and A. humicola, which share high 16S rRNA gene sequence The peptidoglycan type is A4a (Lys–Ala–Glu, A11.35; or similarities, a quinone system with MK-9(H ) predominant Lys–Ser–Glu, A11.58). The quinone system contains 2 and a peptidoglycan with Lys–Ala (A3a; A11.5, A11.6). predominantly menaquinone MK-8(H ). The polar lipid 2–3 2 However, such a proposal would exclude numerous species profile is more complex than in other arthrobacters. It is from the genus Arthrobacter without the option to reclassify composed of the major compounds diphosphatidylgly- them in other genera, since stable diagnostic traits are not cerol, phosphatidylglycerol and dimannosyldiacylglycerol. yet available. Hence, the description of Arthrobacter sensu Phosphatidylinositol, monogalactosyldiacylglycerol, triman- stricto should await the availability of data allowing the nosyldiacylglycerol and significant amounts of five unidenti- assignment to other genera of species that differ from the fied phospholipids are also present. The major fatty acid is genus description of Arthrobacter sensu stricto. anteiso-C15 : 0. Relatively large amounts of iso-C16 : 0 and ante- iso-C17 : 0 are also present. The G+C content of the genomic For this reason, a description of the genus Arthrobacter DNA of the type strain of the type species is 60 mol%. The sensu lato is provided in order to cover species belonging type species is Pseudoglutamicibacter cumminsii. to groups of the genus Arthrobacter that, so far, cannot be reclassified in novel genera. The description of Arthro- bacter sensu lato is provided to replace the original descrip- tion of Conn & Dimmick (1947) and the description given by Keddie (1974) because these descriptions are based Description of Pseudoglutamicibacter cumminsii exclusively on cultural, morphological and physiological comb. nov. characteristics that have to be considered not to be suffi- Pseudoglutamicibacter cumminsii (cum.min9si.i. N.L. gen. ciently conserved to characterize a genus. masc. n. cumminsii of Cummins, to honour Cecil S. Cummins, a prominent American microbiologist and a Emended description of the genus Arthrobacter pioneer of chemotaxonomy). Conn and Dimmick 1947, emend. Koch et al. 1995 Basonym: Arthrobacter cumminsii Funke et al. 1998. sensu lato The description is as provided by Funke et al. (1996, 1998) Cells exhibit a rod–coccus cycle but exclusively coccoid for Arthrobacter cumminsii with the following additional cells may occur. The quinone system usually contains properties. Shares the polar lipid profile and quinone MK-9(H2) as the predominant compound, but almost system listed in the genus description. The peptidoglycan equal amounts of MK-9(H2) and MK-8(H2) or MK-8(H2) structure is A4a (L-Lys–L-Ser–L-Glu; A11.58). as the major compound may occur. The peptidoglycan type is A3a [variations Lys–Ala , Lys–Thr–Ala , The type strain is DMMZ 445T (5ATCC 700218T5CCM 1–4 1–3 Lys–Ala–Ser–Ala ,Lys–Gly–Ala and Lys–Ala –Gly – 4574T5CCUG 36788T5CIP 104907T5DSM 10493T5JCM 3 3 2 2–3 Ala(Gly)]; peptidoglycan type A4a may also be present, as 11675T5KCTC 9904T). reported for Arthrobacter woluwensis (Lys–D-Asp) or in combinations with quinone system MK-9(H2)inArthrobac- ter rhombi and Arthrobacter halodurans (Lys–Ala–D-Glu; Chen et al., 2009). The polar lipid profile contains predomi- Description of Pseudoglutamicibacter albus nantly diphosphatidylglycerol, phosphatidylglycerol, phos- comb. nov. phatidylinositol and dimannosylglyceride. The fatty acid profile is dominated by anteiso- and iso-methyl-branched 9 Pseudoglutamicibacter albus (al bus. L. masc. adj. albus acids. The major fatty acid is usually anteiso-C .Fatty white, because of the white colonies of the organism). 15 : 0 acids iso-C15 : 0,iso-C16 : 0 and anteiso-C17 : 0 often contri- Basonym: Arthrobacter albus Wauters et al. 2000. bute significantly to the profile. The type species is Arthro- bacter globiformis. The description is as provided by Wauters et al. (2000) for Arthrobacter albus with the following additional properties. Shares the polar lipids and quinone system listed in the Emended description of Arthrobacter roseus genus description. The peptidoglycan structure is A4a Reddy et al. 2002 (L-Lys–L-Ala–L-Glu; A11.35). The description is as provided by Reddy et al. (2002), The type strain is CF43T (5ATCC BAA-273T5CCM except that the polar lipid profile does not contain 4905T5CCUG 43812T5CIP 106791T5DSM 13068T5JCM phosphatidylethanolamine. In addition to phosphatidylgly- 11943T5KCTC 9908T). cerol and diphosphatidylglycerol, phosphatidylinositol,

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