Roseivivax Atlanticus Sp. Nov., Isolated from Surface Seawater of the Atlantic Ocean

Roseivivax atlanticus sp. nov., isolated from surface seawater of the Atlantic Ocean

Guizhen Li, Qiliang Lai, Xiupian Liu, Fengqin Sun & Zongze Shao

Antonie van Leeuwenhoek Journal of Microbiology

ISSN 0003-6072 Volume 105 Number 5

Antonie van Leeuwenhoek (2014) 105:863-869 DOI 10.1007/s10482-014-0140-5

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1 23 Author's personal copy

Antonie van Leeuwenhoek (2014) 105:863–869 DOI 10.1007/s10482-014-0140-5

ORIGINAL PAPER

Roseivivax atlanticus sp. nov., isolated from surface seawater of the Atlantic Ocean

Guizhen Li • Qiliang Lai • Xiupian Liu • Fengqin Sun • Zongze Shao

Received: 19 December 2013 / Accepted: 11 February 2014 / Published online: 25 February 2014 Ó Springer International Publishing Switzerland 2014

Abstract A taxonomic study was carried out on strain isoporae LMG 25204T (97.0 %); other species of 22II-S10sT, which was isolated from the surface seawa- genus Roseivivax shared 95.2–96.7 % sequence terof the Atlantic Ocean. The bacterium was found to similarity. The DNA–DNA hybridization estimate be Gram-negative, oxidase and catalase positive, rod values between strain 22II-S10sT and the two type shaped and motile by subpolar ﬂagella. The isolate was strains (R. halodurans JCM 10272T and R. isoporae capable of gelatine hydrolysis but unable to reduce LMG 25204T) were 22.00 and 21.40 %. The principal nitrate to nitrite or degrade Tween 80 or aesculin. Growth fattyacidswereidentiﬁedasSummedFeature8 was observed at salinities of 0.5–18 % (optimum, (C18:1x7c/x6c) (67.4 %), C18:0 (7.2 %), C19:0 cyclo 2–12 %), at pH of 3–10 (optimum, 7) and at tempera- x8c (7.1 %), C18:1x7c 11-methyl (6.8 %) and C16:0 tures of 10–41 °C(optimum28°C). Phylogenetic (5.9 %). The respiratory quinone was determined to be analysis based on 16S rRNA gene sequences indicated Q-10 (100 %). Phosphatidylcholine, phosphatidyletha- that strain 22II-S10sT belongs to the genus Roseivivax, nolamine, phosphatidylglycerol, an aminolipid, a glyco- with highest sequence similarity to Roseivivax halodu- lipid and three phospholipids were present. The G?C rans JCM 10272T (97.2 %), followed by Roseivivax content of the chromosomal DNA was determined to be 67.5 mol%. The combined genotypic and phenotypic data show that strain 22II-S10sT represents a novel species within the genus Roseivivax, for which the name Rosei- Guizhen Li and Qiliang Lai contributed equally to this work. vivax atlanticus sp. nov. is proposed, with the type strain T T T Electronic supplementary material The online version of 22II-S10s (= MCCC 1A09150 = LMG 27156 ). this article (doi:10.1007/s10482-014-0140-5) contains supplementary material, which is available to authorized users. Keywords Roseivivax atlanticus sp. nov. G. Li Q. Lai X. Liu F. Sun Z. Shao (&) Atlantic Ocean Surface seawater DDH State Key Laboratory Breeding Base of Marine Genetic Taxonomy Resources, Key Laboratory of Marine Genetic Resources, Third Institute of Oceanography, SOA, Key Laboratory of Abbreviation Marine Genetic Resources of Fujian Province, Collaborative Innovation Center of Deep Sea Biology, MCCC Marine Culture Collection of China Xiamen 361005, China e-mail: [email protected] Introduction

G. Li Q. Lai Life Science College, Xiamen University, During an investigation of bacterial diversity in Xiamen 361005, China the surface seawater of the Atlantic Ocean, strain 123 Author's personal copy

864 Antonie van Leeuwenhoek (2014) 105:863–869

22II-S10sT was isolated and characterized taxo- N,N,N0,N0-tetramethyl-1,4-phenylenediamine. Catalase nomically along with many other bacterial isolates. activity was determined by bubble production in 10 %

Comparative 16S rRNA gene sequence analysis (v/v) H2O2 solution. Cell motility was observed by the indicated that strain 22II-S10sT belongs to the genus hanging-drop method (Skerman 1967). The growth Roseivivax. The genus Roseivivax was proposed by temperature, pH range and tolerance to NaCl were tested Suzuki and colleagues (Suzuki et al. 1999) and according to the methods described (Li et al. 2013). presently comprises six species: Roseivivax halodu- Hydrolysis of starch, dried skimmed milk, cellulose and rans and Roseivivax halotolerans (Suzuki et al. Tweens20,40,60and80weretestedonmarineagar 1999), Roseivivax lentus (Park et al. 2010), Rosei- 2216 plates supplemented with 0.2 % (w/v) soluble vivax isoporae (Chen et al. 2012), Roseivivax starch, 0.5 % dried skimmed milk, 0.8 % cellulose or sediminis (Xiao et al. 2012) and Roseivivax paciﬁcus 0.5 % (v/v) Tweens 20, 40, 60 or 80, 0.2 % DNA (Wu et al. 2013). Consequently, the aim of the according to standard methods (Dong and Cai 2001). present work was to determine the exact taxonomic Antibiotic susceptibility tests were performed using the position of strain 22II-S10sT by using a polyphasic disc diffusion method as described previously (Shieh approach. et al. 2003). API 20NE, API 20E, and API ZYM strips (bioMe´rieux) were carried out according to the manufacturer’s instructions, with the single modiﬁcation of Materials and methods adjusting the NaCl concentration to 3.0 % in all tests.

Bacterial strains, isolation, and cultivation Determination of 16S rRNA gene sequence and phylogenetic analysis Surface seawater was sampled at site (W14.4°, S14.1°) in 2011 during cruise DY-115A of the South Atlantic Genomic DNA was extracted using a kit (SBS Ocean on the R/V ‘‘Da-Yang Yi-Hao’’. The surface Genetech Co., Ltd. China) and the 16S rRNA gene seawater was diluted and spread on marine agar 2216 was ampliﬁed by PCR using primers described medium (BD Difco). After one month of aerobic previously (Liu and Shao 2005). Sequence similarity incubation at 25 °C, the colonies were picked. Purity was determined using the EzTaxon-e server (Kim was conﬁrmed by the uniformity of cell morphology et al. 2012). Sequences of related taxa were obtained after repeated restreaking. For morphological and from the GenBank database. Phylogenetic analysis biochemical characterization, strain 22II-S10sT was was performed using MEGA version 5.0 (Tamura cultivated on marine agar 2216 medium (BD Difco) et al. 2011) with distance options according to the unless otherwise indicated. R. halotolerans JCM Kimura two-parameter model and clustering with 10271T, R. halodurans JCM 10272T and R. isoporae the neighbour-joining (Saitou and Nei 1987), min- LMG 25204T were obtained from JCM (Japan Collec- imum evolution (Rzhetsky and Nei 1992), and tion of Microorganisms) and LMG (Laboratorium maximum likelihood (Felsenstein 1981) methods, Microbiologie, Universiteit Gent, Belgium) as refer- and supported with bootstrap values based on 1,000 ence strains and cultured under the same conditions for replications. comparative testing. Genome sequencing and DNA–DNA Phenotypic characterization hybridization (DDH) estimation

Gram staining was performed using a Gram staining kit The genome sequences strain 22II-S10sT, R. halodu- (Hangzhou Tianhe Microorganism Reagent Co.) accord- rans JCM 10272T and R. isoporae LMG 25204T were ing to the manufacturer’s instructions. The cell mor- determined by Shanghai Majorbio Bio-pharm Tech- phology, size, and ﬂagellation pattern were observed by nology Co., Ltd. (Shanghai, China), using Solexa transmission electron microscopy (JEM-1230, JEOL) of paired-end (500 bp library) sequencing technology. cells negatively stained with phosphotungstic acid after The G?C content of the chromosomal DNA of strain culture on marine agar at 28 °C for 1 day. Oxidase 22II-S10sT was determined according to draft genome activity was evaluated by the oxidation of 1 % (w/v) sequence. 123 Author's personal copy

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DNA–DNA hybridization (DDH) estimate values 16S rRNA gene sequence analysis among them were analyzed using the genome-to- genome distance calculator (GGDC2.0) (Auch et al. A nearly full-length 16S rRNA gene sequence (1,426 2010a, b; Meier-Kolthoff et al. 2013). nt, GenBank accession number KF906718.) from strain 22II-S10sT was determined. The 22II-S10sT Determination of fatty acid, isoprenoid 16S rRNA gene showed the highest sequence simi- ubiquinone, and polar lipid compositions larity to R. halodurans JCM 10272T (97.2 %), followed by R. isoporae LMG 25204T (97.0 %); other Fatty acids in whole cells grown on marine agar 2216 species of the genus Roseivivax shared 95.2–96.7 % medium at 28 °C for 48 h were saponified, methyl- sequence similarity. As shown in Fig. 1, a phyloge- ated, and extracted using the standard MIDI (Sherlock netic tree was constructed based on the 16S rRNA Microbial Identification System, version 6.0B) proto- gene sequences of all six species of the genus col. Three reference type strains (R. halodurans JCM Roseivivax and representatives of related genera of 10272T, R. isoporae LMG 25204T and R. halotolerans the family Rhodobacteraceae. This analysis showed JCM 10271T) were tested at the same time under the that strain 22II-S10sT formed a clade with R. halodu- same conditions. The fatty acids were analysed by gas rans JCM 10272T and R. isoporae LMG 25204T chromatography (Agilent Technologies 6850) and within the genus Roseivivax. This topology was identified using the TSBA6.0 database of the Micro- confirmed by the maximum-likelihood and minimum bial Identification System (Sasser 1990). Analysis of evolution trees (Supplementary Fig. S2 and S3). the respiratory quinone and polar lipids were carried out by the Identification Service of the DSMZ, Genome sequencing and DDH estimate Braunschweig, Germany. A total of 500Mbp clean data for each strain was generated to reach about 100-fold depth of coverage with Results and discussion an Illumina/Solexa Genome Analyzer IIx (Illumina, SanDiego, CA, USA). The clean data was assembled by Phenotypic characteristics SOAPdenovo2 (Luo et al. 2012). The Genbank accession numbers for strain 22II-S10sT, R. halodurans JCM Strain 22II-S10sT was observed to be Gram-negative, 10272T and R. isoporae LMG 25204T are AQQW0 non-spore-forming, rod-shaped, 0.4–0.6 lm in width 0000000, JALZ00000000 and JAME00000000 respec- and 1.0–1.3 lm in length, and motile by subpolar tively. The estimated DDH values between strain 22II- flagella (see Supplementary Fig. S1). The strain was S10sT and two closely related type strains (R. halodurans found to be able to hydrolyze DNA, but not to JCM 10272T and R. isoporae LMG 25204T)were hydrolyze Tweens 20, 40, 60, 80, starch, dried 22.00 % and 21.40 %, values which are below the skimmed milk and cellulose. Moderately halophilic, standard criteria (70 %) (Wayne et al. 1987). The 22II-S10sT was found to grow in 0.5–18.0 % NaCl estimated DDH value between R. halodurans JCM (optimum 2–12 %), at 10–41 °C (optimum 28 °C) and 10272T and R. isoporae LMG 25204T was 21.50 %. at pH of 3.0–10.0 (optimum 6.0). On marine agar These results confirmed that strain 22II-S10sT represents 2216, strain 22II-S10sT forms smooth grey-white a novel species of the genus Roseivivax. colonies with convex and regular edges of 0.5–1 mm The chromosomal DNA G?C content of new isolate in diameter after 2 days incubation at 28 °C. Strain 22II-S10sT was estimated from the genome sequence 22II-S10sT is sensitive to amikacin (30 lg/per disk, data to be 67.5 mol%, which is within the range reported OXOID), ampicillin (10), gentamicin (10), penicillin for the genus Roseivivax (59.7–68.7 mol%) (Wu et al. G (10), streptomycin (10) and vancomycin (30); 2013). resistant to clindamycin (2), metronidazole (5), linco- mycin (2) and polymyxin B (30 IU). Other character- Chemotaxonomic characteristics istics are given in the species description. Table 1 shows the characteristics that distinguish strain 22II- The principal fatty acids of strain 22II-S10sT were T S10s from related species of the genus Roseivivax. identified as Summed Feature 8 (C18:1x7c/x6c as 123 Author's personal copy

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Table 1 Physiological characteristics of strain 22II-S10sT and 10271T (Suzuki et al. 1999); 5, R. sediminis YIM D21T (Xiao the species of the genus Roseivivax Strains: 1, 22II-S10sT;2,R. et al. 2012); 6, R. lentus S5-5T (Park et al. 2010); 7, R. paciﬁcus halodurans JCM 10272T (Suzuki et al. 1999); 3, R. isoporae 22DY03T (Wu et al. 2013) LMG 25204T (Chen et al. 2012); 4, R. halotolerans JCM

Characteristic 1 2 3 4 5 6 7

Source Surface Salt lake Reef-building Salt lake Slat mine Tidal ﬂat Deep sea seawater coral sediment Presence of ﬂagella ?? ? ?- - - Temperature range 10–41 (27–30) 10–40 (30–40) (27–30) 15–42 (28) 10–40 (30) 10–40 (30–35) (optimum) (°C) (28) NaCl range (optimum) 0.5–15 0–20 0–15 0.5–20 1–15 2–13 (2) 0.5–15 (%, w/v) (2–12) pH range (optimum) 3–10 (6) (7.5–8.0) 7–11 (7.5–8) (7.5–8.0) 6.5–8.5 (7.5–8.0) (7.5–8) 5.5–8.5 (7) Reduction of nitrate to nitrite -? - -- ? - Glucose fermentation ?? - -- - ? Urease ?- - ?? - ? Hydrolysis of Aesculin -? w ?? - ? Gelatin -- - ?- - - Tween 80 -- ? -- ? - API ZYM Acid phosphatase ?? ? ?? - ? Naphtol-AS-Bl- ?- - w ??? phosphoamidase Valine aminopeptidase ?? ? ?? - ? a-chymotrypsin ?- ww--- Cystine aminopeptidase w w w ?? - w Lipase (C14) w w w w --- a-alactosidase -- ? -? - ? a-glucosidase - w ??--? b-galactosidase -- ? ?- - ? b-glucosidase - ww ?- - ? Lipid Phosphatidylglycerol (PG) ? ND ? ND -?? Phosphatidylethanolamine ? ND ? ND ??? (PE) Phosphatidylcholine (PC) ? ND ? ND ?-? Diphosphatidylglycerol - ND ? ND ?-? (DPG) Phosphatidyl- - ND ? ND --- dimethylethanolamine (PDME) DNA G?C content (mol%) 67.5 64.4 (66.4*) 68.8 (69.8*) 59.7 67.7 68.2 64.6

The data of API 20NE, API 20E and API ZYM for strain 1 to strain 4 were obtained in this study. Characteristics are scored as: ? positive, - negative, w weakly positive, ND no data * The DNA G?C data from draft genome sequence

deﬁned by the MIDI system; 67.4 %), C18:0 (7.2 %), (C18:1x7c/x6c (27.5–81.2 %); Table S1). This was C19:0 cyclo x8c (7.1 %), C18:1x7c 11-methyl (6.8 %) similar to the former study (Chen et al. 2012). The fatty T and C16:0 (5.9 %). In addition, the major fatty acids acid proﬁle of strain 22II-S10s is in good agreement of all Roseivivax species are Summed Feature 8 with those of members of the genus Roseivivax,butit

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Fig. 1 Neighbour-joining 79 Roseivivax atlanticus 22II-S10sT (KF906718) tree showing the 70 T phylogenetic positions of Roseivivax halodurans JCM 10272 (D85829) strain 22II-S10sT and the Roseivivax isoporae LMG 25204T (FJ593905) species of the genus Roseivivax sediminis YIM D21T (HQ615878) Roseivivax and T representatives of related Roseivivax pacificus 22DY03 (KC018453) T genera of the family Roseivivax halotolerans JCM 10271 (D85831) Rhodobacteraceae, based on Roseivivax lentus S5-5T (FJ875966) 16S rRNA gene sequences. Citreimonas salinaria CL-SP20T (AY962295) Filled circles indicate nodes T that were also recovered in 60 Citreicella thiooxidans CHLG1 (AY639887) maximum-likelihood and 79 Yangia pacifica DX5-10T (AJ877265) minimum evolution trees Roseovarius tolerans EL-172T (Y11551) based on the same T sequences. Bootstrap values Salinihabitans flavidus ISL-46 (FJ265707) (expressed as percentages of Sediminimonas qiaohouensis YIM B024T (EU878003) 1,000 replications) are Pontibaca methylaminivorans GRP21T (AJ505788) shown at branch points. Bar, T 0.005 nucleotide 65 Thalassobius aestuarii JC2049 (AY442178) T substitution rate (Knuc) 72 Lutimaribacter saemankumensis SMK-117 (EU336981) units. Stappias stellulata T T Roseisalinus antarcticus EL-88 (AJ605747) IAM 12621 (D88525) was T used as an outgroup Roseicitreum antarcticum ZS2-28 (FJ196006) Roseibacterium beibuensis JLT1202rT (JN247667) 62 Actibacterium mucosum CECT 7668T (HE590855) 59 Rhodovulum sulfidophilum DSM 1374T (D16423) Rubellimicrobium thermophilum C-lvk-R2A-2T (AJ844281) Stappia stellulata IAM 12621T (D88525)

0.005 can be differentiated from other species by the characteristics given in Table 1. Considering its low percentage of C18:1x7c 11-methyl, C19:0 cyclo calculated DDH values (B22.00 %) when compared x8c and Summed Feature 8 (C18:1x7c/x6c). with closest species, the isolate cannot be assigned to The respiratory quinone of strain 22II-S10sT was any previously recognized species. Therefore, strain determined to be Q-10 (100 %). This is consistent 22II-S10sT represents a novel species of the genus with the members of the genus Roseivivax (Wu et al. Roseivivax, for which the name Roseivivax atlanticus 2013). Strain 22II-S10sT was found to contain sp. nov. is proposed. phosphatidylcholine (PC), phosphatidylethanolamine (PE), phosphatidylglycerol (PG), an aminolipid, a Description of Roseivivax atlanticus sp. nov glycolipid and three phospholipids (shown in Sup- plementary Fig. S4). PC, PE and PG were also Roseivivax altanticus (at.lan’ti.cus. L. masc. adj. present in the R. isoporae LMG 25204T and R. atlanticus Atlantic, from the Atlantic Ocean) pacificus 22DY03T. Cells are Gram-negative, rod shaped, 0.4–0.6 lmin Taxonomic conclusion width and 1.0–1.3 lm in length, motile by subpolar flagella. Positive for oxidase, catalase, arginine dihydro- The results of the phylogenetic analysis, phenotypic lase (weak), urease, ornithine decarboxylase (weak), analysis and chemotaxonomic studies presented above citrate utilization (weak) and fermentation of D-glucose, support the view that strain 22II-S10sT should be rhamnose, melibiose, amygdalin and arabinose but assigned to the genus Roseivivax. However, the strain negative for reduction of nitrate to nitrite, denitrification, could be distinguished from the closely-related indole production, b-glucosidase (aesculin hydrolysis), species in the genus Roseivivax by some phenotypic b-galactosidase, lysine decarboxylase, H2S production, 123 Author's personal copy

868 Antonie van Leeuwenhoek (2014) 105:863–869 tryptophan deaminase, acetoin production (Voges Pros- Science Foundation of China (41276005/41176154/40906083), kauer), gelatinase, fermentation of mannitol, inositol, Public Welfare Project of SOA (201005032) and National Infrastructure of Natural Resources for Science and Technology sorbitol and saccharose. Can hydrolyze DNA but can’t Program of China (No. NIMR-2013-9 and NIMR-2014-9). hydrolyze Tweens 20, 40, 60 and 80, starch, dried skimmed milk, and cellulose. On marine agar 2216, forms smooth grey colonies with regular edges, slightly raised in the centre, of 0.5–1 mm in diameter after 48 h References incubation at 28 °C. Moderately halophilic, grows in 0.5–18 % NaCl (optimum 2–12 %) at 10–41 °C(opti- Auch AF, Klenk HP, Goker M (2010a) Standard operating procedure for calculating genome-to-genome distances mum 28 °C), at a pH range of 3.0–10.0 (optimum 7.0). based on high-scoring segment pairs. 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