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 Downloaded from www.microbiologyresearch.org by 000702 G 2015 IUMS Printed in Great Britain 9 IP: 54.70.40.11 On: Mon, 04 Feb 2019 19:10:17 H.-J. Busse 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., Downloaded from www.microbiologyresearch.org by 10 International Journal of Systematic and Evolutionary Microbiology 66 IP: 54.70.40.11 On: Mon, 04 Feb 2019 19:10:17