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Paenirhodobacter Enshiensis Gen. Nov., Sp. Nov., a Non-Photosynthetic

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Paenirhodobacter Enshiensis Gen. Nov., Sp. Nov., a Non-Photosynthetic %paper no. ije050351 charlesworth ref: ije050351& New Taxa - Proteobacteria International Journal of Systematic and Evolutionary Microbiology (2014), 63, 000–000 DOI 10.1099/ijs.0.050351-0 Paenirhodobacter enshiensis gen. nov., sp. nov., a non-photosynthetic bacterium isolated from soil, and emended descriptions of the genera Rhodobacter and Haematobacter Dan Wang, Hongliang Liu, Shixue Zheng and Gejiao Wang Correspondence State Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Gejiao Wang Huazhong Agricultural University, Wuhan, Hubei 430070, PR China [email protected] A Gram-reaction-negative, facultatively anaerobic, non-motile, rod-shaped, non-photosynthetic bacterial strain, DW2-9T, was isolated from soil. The highest 16S rRNA gene sequence similarities were found to Rhodobacter capsulatus ATCC 11166T (97.1 %), Rhodobacter viridis JA737T (96.4 %), Rhodobacter maris JA276T (96.2 %), Rhodobacter veldkampii ATCC 35703T (96.0 %), Haematobacter massiliensis CCUG 47968T (96.0 %), Haematobacter missouriensis CCUG 52307T (95.9 %) and Rhodobacter aestuarii JA296T (95.7 %). The genomic DNA G+C content was 67.2 mol% and the major respiratory quinone was ubiquinone 10 (Q-10). The major cellular fatty acids (.5 %) were C18 : 1v7c,C16 : 0,C19 : 0 cyclo v8c and summed feature 3 (one or more of iso-C15 : 0 2-OH, C16 : 1v6c and C16 : 1v7c). However, unlike species of the genus Rhodobacter, strain DW2-9T neither formed internal photosynthetic membranes nor produced photosynthetic pigments. DNA–DNA hybridization between strain DW2-9T and R. capsulatus JCM 21090T showed a relatedness of 33 %. Strain DW2-9T contained phosphatidylethanola- mine, phosphatidylglycerol and an unknown aminophospholipid as major polar lipids, which differed from those of species of the genera Rhodobacter and Haematobacter. In addition to the differences in phylogenetic position and polar lipid types, strain DW2-9T could be distinguished from species of the genus Haematobacter by the cultivation conditions. On the basis of our polyphasic taxonomic analysis, strain DW2-9T is considered to represent a novel genus and species, for which the name Paenirhodobacter enshiensis gen. nov., sp. nov. is proposed. The type strain of Paenirhodobacter enshiensis is DW2-9T (5CCTCC AB 2011145T5KCTC 15169T). Emended descriptions of the genera Rhodobacter and Haematobacter are also proposed. At the time of writing, the family Rhodobacteraceae contains contain ubiquinone 10 (Q-10) as the major respiratory 105 genera (http://www.bacterio.net/classifgenerafamilies. quinone (Q-10 is common within the Rhodobacteraceae; html#Rhodobacteraceae). Members of the genus Rhodobacter Tanaka et al., 2004; Sorokin et al., 2005; Yu et al., 2011). The are photosynthetic; the genus was proposed by Imhoff et al. predominant cellular fatty acid is C18 : 1 (Imhoff, 2005). Polar (1984), and the genus was reorganized by Hiraishi & Ueda lipid profiles have been reported only for Rhodobacter (1994). At the time of writing, the genus Rhodobacter has 17 capsulatus ATCC 11166T and R. viridis JA737T,andthese ; species with validly published names, of which five have been reports showed phosphatidylglycerol, phosphatidylethanola- reclassified in other genera; the remaining species are all mine and phosphatidylcholine as the major polar lipids Gram-reaction-negative, rod-shaped, photosynthetic bacteria. (Shalem Raj et al., 2013). Haematobacter is another genus of Phototrophically grown cells contain vesicular or lamellar the family Rhodobacteraceae, and it contains only two species. internal photosynthetic membranes and bacteriochlorophyll a Haematobacter massiliensis was originally proposed as Rhodo- and carotenoids as photosynthetic pigments (Eckersley & bacter massiliensis by Greub & Raoult (2003); later, it was Dow, 1980; Hiraishi & Ueda, 1994). Members of the genus reclassified in Haematobacter,togetherwithHaematobacter missouriensis (Helsel et al.,2007).Distinctfromtheother The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene genera of the Rhodobacteraceae, the members of the genus sequence of strain DW2-9T is JN797511. Haematobacter were isolated from clinical samples and differ Six supplementary figures are available with the online version of this from members of the genus Rhodobacter in cultivation con- paper. ditions, the absence of internal photosynthetic membranes, 050351 G 2014 IUMS Printed in Great Britain 1 %paper no. ije050351 charlesworth ref: ije050351& D. Wang and others non-production of photosynthetic pigments, the presence of A phylogenetic tree reconstructed using the maximum- T C19 : 0 cyclo v8c and phylogenetic position (Greub & Raoult, likelihood algorithm revealed that strains DW2-9 and 2003; Helsel et al., 2007). The other genera belonging to the DW2-13 grouped together within the cluster containing R. family Rhodobacteraceae are phenotypically, metabolically and capsulatus ATCC 11166T, R. viridis JA737T, R. maris ecologically diverse (Imhoff, 2005). In this study, a soil JA276T, R. aestuarii JA296T and R. vinaykumarii JA123T, bacterial isolate, designated strain DW2-9T,wasfoundtobe but strains DW2-9T and DW2-13 formed a separate closely related to species of the genera Rhodobacter and branch. Strain DW2-9T was separated from H. massi- Haematobacter based on 16S rRNA gene sequence analysis; liensis CCUG 47968T, H. missouriensis CCUG 52307T, however, on the basis of phenotypic and phylogenetic analyses, Roseicitreum antarcticum ZS2-28T and T. pacifica TL2T it is proposed that strain DW2-9T represents a novel genus and (Fig. 1). The neighbour-joining and maximum-parsimony species. trees (Figs S1 and S2, available in IJSEM Online) both supported the phylogenetic position obtained with the The soil sample was collected from a sewage outlet of the maximum-likelihood tree. Bafeng pharmaceutical factory (29u 529 550 N 110u 039 210 E) located in Enshi, Hubei province, PR China. Soil For analyses of morphological, physiological and biochem- texture, organic matter, nitrogen, phosphorus, sulfur, iron ical characteristics, strain DW2-9T and the five most closely T and pH were analysed as described by Okkenhaug et al. related type strains, R. capsulatus JCM 21090 , R. maris T T (2011) and the nitrate concentration was analysed as JCM 14794 , R. aestuarii JCM 14887 (from the Japan described by Andrews et al. (2002). The soil texture was Collection of Microorganisms), H. missouriensis CCUG T T heavy loam type with a pH of 6.9. The organic matter, N, 52307 and H. massiliensis CCUG 47968 (from the P, S, Fe and NO concentrations were 59.7, 5.8, 1.8, 3.4, Culture Collection of the University of Go¨teborg), were 3 T 96.7 and 398.4 g?kg21, respectively. For bacterial isolation, analysed in parallel. Strain DW2-9 , R. capsulatus JCM T T T 1 g soil was added to 99 ml sterilized water and then 21090 , R. maris JCM 14794 , R. aestuarii JCM 14887 serially diluted and cultured on 1/5 TSBA plates (tryptic were cultured on modified Biebl & Pfennig’s medium 21 soy broth agar, pH 7.0; Difco BD). containing (l ) 0.5 g KH2PO4, 0.2 g MgSO4 .7H2O, 0.4 g NaCl, 0.6 g NH4Cl, 0.05 g CaCl2 .2H2O, 3.0 g sodium A nearly full-length 16S rRNA gene sequence was amplified pyruvate, 0.3 g yeast extract, 5 ml ferric citrate solution as described by Fan et al. (2008) and compared with (0.1 %, w/v) and 1 ml micronutrient solution [l21:1ml sequences available in the EzTaxon-e server (Kim et al., HCl (25 %, v/v), 0.07 g ZnCl2, 0.1 g MnCl2 .4H2O, 0.06 g 2012). Multiple alignments were performed using the H3BO3, 0.2 g CoCl2 .6H2O, 0.02 g CuCl2 .H2O, 0.02 g CLUSTAL_X program (Thompson et al., 1997). Phylogenetic ] NiCl2 .6H2O and 0.04 g NaMoO4 .2H2O (Biebl & analysis was carried out using MEGA 4.0 (Tamura et al., Pfennig, 1981), unless otherwise mentioned. H. mis- 2007) and the PHYML online web server (Guindon et al., souriensis CCUG 52307T and H. massiliensis CCUG 2010). Phylogenetic trees, viewed with MEGA 4.0, were 47968T were grown under clinical culture conditions using reconstructed using the neighbour-joining (Saitou & Nei, brain-heart infusion (BHI) (Helsel et al., 2007) or buffered 1987), maximum-parsimony (Kluge & Farris, 1969) and charcoal yeast extract (BCYE) agar (Greub & Raoult, 2003), maximum-likelihood (Felsenstein, 1981) methods with respectively. For all analyses, strain DW2-9T, R. capsulatus bootstrap analyses based on 1000 replications. Type strains JCM 21090T, R. maris JCM 14794T, R. aestuarii JCM of all species of the genera Rhodobacter and Haematobacter 14887T were incubated at 30 uC, while H. missouriensis and representative strains from 12 other genera of the CCUG 52307T and H. massiliensis CCUG 47968T were family Rhodobacteraceae were included in the phyloge- incubated at 35 uC, unless otherwise mentioned. netic trees. Strain DW2-13 (GenBank/EMBL/DDBJ no. KC820799), isolated from the same soil, was also included Cell morphology was observed using light microscopy in the phylogenetic analyses. (Olympus; 61000) and transmission electron microscopy (H-7650; Hitachi) (Grossart et al., 2000) with cells cultured The nearly full-length (1428 bp) 16S rRNA gene sequence of for 48 h. Motility tests were performed using the strain DW2-9T shared sequence identities in the range 97.1– appropriate medium supplemented with 0.3 % agar. 94.7 % with type strains of species of Rhodobacter and Gram staining was determined using the method described Haematobacter. The highest 16S rRNA gene sequence by Dussault (1955). Growth at 4, 10, 28, 30, 37, 42 and T similarities were found with R. capsulatus ATCC 11166 45 uC and 0–5 % (w/v) NaCl was assessed after 7 days of (97.1 %), R. viridis JA737T (96.4 %), R. maris JA276T incubation. Growth at pH 4–10 (at intervals of 1 pH unit) (96.2 %), R. veldkampii ATCC 35703T (96.0 %), H. massi- was determined using the following buffer systems: pH 4– T liensis CCUG 47968 (96.0 %), H. missouriensis CCUG 7, 0.1 M citric acid/0.2 M Na2HPO4; pH 8–9, 0.1 M Tris/ T T 52307 (95.9 %) and R. aestuarii JA296 (95.7 %). The only 0.2 M HCl; pH 10, 0.05 M NaHCO3/0.1 M NaOH.
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