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Aromatoleum Gen. Nov., a Novel Genus Accommodating the Phylogenetic Lineage Including Azoarcus Evansii and Related Species, and Proposal of Aromatoleum Aromaticum Sp

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Aromatoleum Gen. Nov., a Novel Genus Accommodating the Phylogenetic Lineage Including Azoarcus Evansii and Related Species, and Proposal of Aromatoleum Aromaticum Sp TAXONOMIC DESCRIPTION Rabus et al., Int J Syst Evol Microbiol 2019;69:982–997 DOI 10.1099/ijsem.0.003244 Aromatoleum gen. nov., a novel genus accommodating the phylogenetic lineage including Azoarcus evansii and related species, and proposal of Aromatoleum aromaticum sp. nov., Aromatoleum petrolei sp. nov., Aromatoleum bremense sp. nov., Aromatoleum toluolicum sp. nov. and Aromatoleum diolicum sp. nov. Ralf Rabus,1,* Lars Wöhlbrand,1 Daniela Thies,2 Markus Meyer,3 Barbara Reinhold-Hurek4 and Peter Kampfer€ 5 Abstract Comparative 16S rRNA gene sequence analysis and major physiological differences indicate two distinct sublineages within the genus Azoarcus: the Azoarcus evansii lineage, comprising Azoarcus evansii (type strain KB740T=DSM 6898T=CIP 109473T =NBRC 107771T), Azoarcus buckelii (type strain U120T=DSM 14744T=LMG 26916T), Azoarcus anaerobius (type strain LuFRes1T =DSM 12081T=LMG 30943T), Azoarcus tolulyticus (type strain Tol-4T=ATCC 51758T=CIP 109470T), Azoarcus toluvorans (type strain Td21T=ATCC 700604T=DSM 15124T) and Azoarcus toluclasticus (type strain MF63T=ATCC 700605T), and the Azoarcus indigens lineage, comprising Azoarcus indigens (type strain VB32T=ATCC 51398T=LMG 9092T), Azoarcus communis (type strain SWub3T=ATCC 51397T=LMG 9095T) and Azoarcus olearius (type strain DQS-4T=BCRC 80407T=KCTC 23918T=LMG 26893T). Az. evansii lineage members have remarkable anaerobic degradation capacities encompassing a multitude of alkylbenzenes, aromatic compounds and monoterpenes, often involving novel biochemical reactions. In contrast, Az. indigens lineage members are diazotrophic endophytes lacking these catabolic capacities. It is proposed that species of the Az. evansii lineage should be classified in a novel genus, Aromatoleum gen. nov. Finally, based on the literature and new growth, DNA–DNA hybridization and proteomic data, the following five new species are proposed: Aromatoleum aromaticum sp. nov. (type strain EbN1T=DSM 19018T=LMG 30748T and strain pCyN1=DSM 19016=LMG 31004), Aromatoleum petrolei sp. nov. (type strain ToN1T=DSM 19019T=LMG 30746T), Aromatoleumbremense sp. nov. (type strain PbN1T=DSM 19017T=LMG 31005T), Aromatoleum toluolicum sp. nov. (type strain TT=DSM 19020T=LMG 30751T) and Aromatoleum diolicum sp. nov. (type strain 22LinT=DSM 15408T=LMG 30750T). INTRODUCTION oxygenases are used, which employ highly reactive oxygen species derived from molecular oxygen (O ) [1]. However, A key role of bacteria in terrestrial and aquatic environ- 2 in many habitats, such as aquatic sediments, deeper soil ments is the remineralization of natural and anthropogenic layers and groundwater aquifers, anoxic conditions prevail, organic compounds to CO . Correspondingly, bacteria har- 2 demanding O -independent degradation pathways. bour a broad spectrum of degradation pathways. The excep- 2 tional chemical stability of aromatic compounds in general, Isolation of pure cultures with respective anaerobic degrada- and alkylbenzenes in particular, represents a special chal- tion capacities was instrumental for elucidation of the novel lenge for their biodegradation. Under oxic conditions, reactions and pathways involved [2–5]. Denitrifying isolates Author affiliations: 1Institute for Chemistry and Biology of the Marine Environment (ICBM), Carl von Ossietzky University Oldenburg, Carl-von- Ossietzky Str. 9-11, D-26111 Oldenburg, Germany; 2Max Planck Institute for Marine Microbiology, Celsiusstraße 1, D-28359 Bremen, Germany; 3Bruker Daltonik GmbH, Fahrenheitstr. 4, D-28359 Bremen, Germany; 4Laboratory for General Microbiology, University Bremen, PO Box 330440, D-28334 Bremen, Germany; 5Department for Applied Microbiology, Justus Liebig University, Heinrich-Buff-Ring 26-32, D-35392 Giessen, Germany. *Correspondence: Ralf Rabus, [email protected] Keywords: Aromatoleum gen. nov.; Aromatoleum aromaticum sp. nov.; Aromatoleum petrolei sp. nov.; Aromatoleum bremense sp. nov.; Aromatoleum toluolicum sp. nov.; Aromatoleum diolicum sp. nov.; anaerobic degradation; denitrification; alkylbenzene; monoterpene; aromatic compounds; taxonomy. Abbreviations: Ar, Aromatoleum; Az, Azoarcus. The GenBank / EMBL / DDBJ / PIR accession numbers for the 16S RNA gene sequences of strains EbN1T, pCyN1, ToN1T, PbN1T,TT, and 22LinT are X83531, Y17284, X83534, X83532, AF129465, and Y13222. Three supplementary tables are available with the online version of this article, 003244 ã 2019 IUMS 982 Rabus et al., Int J Syst Evol Microbiol 2019;69:982–997 were preferentially used for biochemical studies, since they [2, 4, 5, 19–23]). To avoid confusion with abbreviated gen- grow relatively fast and yield considerable cell mass. The era names, henceforth we use Ar. for Aromatoleum and Az. majority of these denitrifying strains can be grouped into for Azoarcus. two phylogenetic clusters within the Betaproteobacteria. One cluster corresponds to the genus Thauera [6] and includes besides the well studied Thauera aromatica K172T METHODS [7] other anaerobic degraders of aromatic compounds, Bacterial strains namely Thauera aminoaromatica S2T [8], Thauera chloro- benzoica 3CB-1T [9], Thauera mechernichensis TL1T [10] Bacterial strains from the proposed genus Aromatoleum and Thauera phenylacetica B4PT [8], as well as the monoter- used in this study are listed in Table S1. The denitrifying T T T T pene degraders Thauera linaloolentis 47LolT and Thauera strains EbN1 , ToN1 , PbN1 , mXyN1 and pCyN1 have terpenica 58EuT [11]. The other cluster consists of the genus been subcultured in our laboratory since their isolation [24, T T T T Azoarcus, which was originally described to contain mainly 25]. The strains T (=DSM 9506 ), 22Lin (=DSM 15408 ), T T T T T N2-fixing endophytes or root surface colonizers of Kallar KB740 (=DSM 6898 ), U120 (=DSM 14744 ), LuFRes1 grass, such as Azoarcus indigens VB32T, Azoarcus communis (=DSM 12081T) and Td21T (=DSM 15124T) were obtained SWub3T and Azoarcus sp. strain BH72 deserving the rank of from the Deutsche Sammlung von Mikroorganismen und a separate but initially unnamed species [12]. With a high Zellkulturen (DSMZ). The strains Tol-4T (=ATCC 51758T) genomic similarity [average nucleotide identity (ANI) of and MF63T (=ATCC 700605T) were obtained from the 98.98 %] [13], strain BH72 can be assigned to the recently American Type Culture Collection (ATCC). Az. indigens described species Azoarcus olearius [14]. The first taxonom- VB32T (=ATCC 51398T), Az. communis SWub3T (=ATCC ically described anaerobic degrader of aromatic compounds 51397T) and Az. olearius BH72 were provided by the labora- from this second cluster is Azoarcus evansii KB740T [7] and tory of B. Reinhold-Hurek. the biochemical differences to Az. indigens VB32T and Az. T communis SWub3 were already obvious. In subsequent Cultivation conditions and substrate utilization studies, the anaerobically aromatic compound-degrading tests Azoarcus buckelii U120T [8], Azoarcus anaerobius LuFRes1T [15], Azoarcus tolulyticus Tol-4T [16], Azoarcus toluvorans Growth under nitrate-reducing conditions was tested in Td-21T [17] and Azoarcus toluclasticus MF63T [17] were defined, ascorbate-reduced (4 mM) medium with nitrate described and taxonomically allocated into the genus Azoar- (7 mM) as electron acceptor [24]. Nitrate-free medium cus. Henceforth, we will refer to this group with versatile (in (containing 5.6 mM NH4Cl) was used when growth was particular anaerobic) degradation capabilities as ‘degrada- tested under oxic conditions [24]. Anaerobic cultivation was tion specialists’. Since they are equally close related to the carried out at 28 C in anoxically sealed glass tubes, and plant-endophytic Azoarcus species and the Thauera species, hydrocarbons and other poorly water soluble organic com- the need for describing them as a new genus has been noted pounds were added as dilute solutions in inert 2,2,4,4,6,8,8- before [18]. Phenotypic separation of this cluster of degrada- heptamethylnonane (carrier phase) as previously described tion specialists from the plant-endophytic Azoarcus [24, 26]. Soluble organic substrates were added from sterile species was further corroborated in the present study by the stock solutions [27]. Three parallel cultures were used for absence of nifH genes and nitrogenase activity in most of each individual substrate test. All growth tests for an indi- the degradation specialists and the inability of Az. indigens vidual strain were inoculated from the same culture grown VB32T, Az. communis SWub3T and Az. olearius BH72 to with benzoate (4 mM) under nitrate-reducing conditions, degrade aromatic compounds under anoxic conditions. except for Az. indigens VB32T, Az. communis SWub3T and Az. olearius BH72 (5 mM malate under oxic conditions). Therefore, we propose to consolidate these findings by allo- Growth was monitored by measuring the optical density at cating this cluster of denitrifying degradation specialists to a 660 nm over a period of at least 4 weeks. Some tests for car- novel genus, Aromatoleum gen. nov. In addition to the six already described species of this new genus, we propose bon sources used for aerobic growth were carried out using here five new species from various aquatic and terrestrial Biotype 100 strips (API bioMerieux) as described previously habitats (Table S1, available in the online version of this [18] with readings after 7 days. Mass cultivation (400 ml or – article). Most of the Aromatoleum species can be metaboli- 2 l volume) for FAME-analyses, DNA DNA hybridization cally differentiated by the anaerobic utilization of specific or mass spectrometric
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