Aestuariisphingobium litorale gen. nov., sp. nov., a novel proteobacterium isolated from a water sample of Pearl River estuary

Li, Xin; Li, Jia-Ling; Zhang, Xiao-Tong; Duan, Li; Asem, Mipeshwaree Devi; Xiao, Min; Mou, Xiaozhen; Salam, Nimaichand; Li, Wen-Jun

doi:10.1007/s10482-019-01268-6

Original Paper
Published: 25 April 2019

Aestuariisphingobium litorale gen. nov., sp. nov., a novel proteobacterium isolated from a water sample of Pearl River estuary

Xin Li¹^na1,
Jia-Ling Li¹^na1,
Xiao-Tong Zhang¹^na1,
Li Duan¹,
Mipeshwaree Devi Asem¹,
Min Xiao¹,
Xiaozhen Mou²,
Nimaichand Salam¹ &
Wen-Jun Li ORCID: orcid.org/0000-0002-1233-736X^1,3

Antonie van Leeuwenhoek volume 112, pages 1357–1367 (2019)Cite this article

309 Accesses
8 Citations
Metrics details

Abstract

Strain SYSU M10002^T was isolated from a water sample collected from the coastal region of Pearl River estuary, Guangdong Province, southern China. The taxonomic position of the isolate was investigated by polyphasic taxonomic approaches. The isolate was found to be Gram-negative, non-motile, short rods and aerobic. The strain was able to grow at 14–37 °C, pH 6.0–10.0 and in the presence of up to 0.5% (w/v) NaCl. Phylogenetic analysis based on 16S rRNA gene sequences indicated that strain SYSU M10002^T is a member of the family Sphingomonadaceae, with high sequence similarity to Sphingorhabdus buctiana T5^T (95.1%). Overall genomic related indices between the genome of strain SYSU M10002^T and those of related strains were low to moderate (AAI values < 64.3%; POCP values < 58%), indicating that strain SYSU M10002^T represents a novel lineage within the family Sphinogomonadaceae. Strain SYSU M10002^T contained homospermidine as its polyamine. The major polar lipids were diphosphatidylglycerol, phosphatidylcholine, phosphatidylethanolamine, phosphatidylglycerol, sphingoglycolipid, two unidentified phospholipids and an unidentified aminolipid. Ubiquinone Q-9 (44.9%) and Q-10 (43.2%) were the dominant respiratory quinones, along with a minor amount of Q-8 (11.9%). The predominant cellular fatty acids (> 10%) identified were summed feature 3 (C_16:1ω7c and/or C_16:1ω6c), summed feature 8 (C_18:1ω7c) and C_14:0 2-OH. The genomic DNA G+C content was 64.0%. Based on the analyses of the phenotypic, genotypic and phylogenetic characteristics, strain SYSU M10002^T is determined to represent a novel species of a novel genus, for which the name Aestuariisphingobium litorale gen. nov., sp. nov. is proposed. The type strain of the species is SYSU M10002^T (= KCTC 52944^T = NBRC 112961^T).

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (USA)
Tax calculation will be finalised during checkout.

References

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/s0022-2836(05)80360-2
Article CAS PubMed Google Scholar
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppiq JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richarcharson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene Ontology: tool for the unification of biology. The gene ontology consortium. Nat Genet 25:25–29. https://doi.org/10.1038/75556
Article CAS PubMed PubMed Central Google Scholar
Balkwill DL, Fredrickson JK, Romine MF (2006) Sphingomonas and related genera. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes: volume 7: Proteobacteria: Delta, Epsilon Subclass. Springer, New York, pp 605–629. https://doi.org/10.1007/0-387-30747-8_23
Busse J, Auling G (1988) Polyamine pattern as a chemotaxonomic marker within the Proteobacteria. Syst Appl Microbiol 11:1–8. https://doi.org/10.1016/S0723-2020(88)80040-7
Article CAS Google Scholar
Busse H-J, Bunka S, Hensel A, Lubitz W (1997) Discrimination of members of the family Pasteurellaceae based on polyamine patterns. Int J Syst Evol Microbiol 47:698–708. https://doi.org/10.1099/00207713-47-3-698
CAS Article Google Scholar
Chen H, Piao A-L, Tan X, Nogi Y, Yeo J, Lu H, Feng Q-Q, Lv J (2018) Sphingorhabdus buctiana sp. nov., isolated from fresh water, and reclassification of Sphingopyxis contaminans as Sphingorhabdus contaminans comb. nov. Antonie Van Leeuwenhoek 111:323–331. https://doi.org/10.1007/s10482-017-0954-z
Article CAS PubMed Google Scholar
Collins MD, Pirouz T, Goodfellow M, Minnikin DE (1977) Distribution of menaquinones in actinomycetes and corynebacteria. J Gen Microbiol 100:221–230
Article CAS PubMed Google Scholar
Cui H-L, Lin Z-Y, Dong Y, Zhou P-J, Liu S-J (2007) Halorubrum litoreum sp. nov., an extremely halophilic archaeon from a solar saltern. Int J Syst Evol Microbiol 57:2204–2206. https://doi.org/10.1099/ijs.0.65268-0
Article CAS PubMed Google Scholar
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376. https://doi.org/10.1007/bf01734359
Article CAS PubMed Google Scholar
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.2307/2408678
Article PubMed Google Scholar
Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A, Salazar GA, Tate J, Bateman A (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44:D279–D285. https://doi.org/10.1093/nar/gkv1344
Article CAS PubMed Google Scholar
Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:406–416. https://doi.org/10.2307/2412116
Article Google Scholar
Gich F, Overmann J (2006) Sandarakinorhabdus limnophila gen. nov., sp. nov., a novel bacteriochlorophyll a-containing, obligately aerobic bacterium isolated from freshwater lakes. Int J Syst Evol Microbiol 56:847–854. https://doi.org/10.1099/ijs.0.63970-0
Article CAS PubMed Google Scholar
Glöckner FO, Zaichikov E, Belkova N, Denissova L, Pernthaler J, Pernthaler A, Amann R (2000) Comparative 16S rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of Actinobacteria. Appl Environ Microbiol 66:5053–5065. https://doi.org/10.1128/aem.66.11.5053-5065.2000
Article PubMed PubMed Central Google Scholar
Gonzalez C, Gutierrez C, Ramirez C (1978) Halobacterium vallismortis sp. nov., an amylolytic and carbohydrate-metabolizing, extremely halophilic bacterium. Can J Microbiol 24:710–715
Article CAS PubMed Google Scholar
Groth I, Schumann P, Weiss N, Martin K, Rainey FA (1996) Agrococcus jenensis gen. nov., sp. nov., a new genus of actinomycetes with diaminobutyric acid in the cell wall. Int J Syst Evol Microbiol 46:234–239. https://doi.org/10.1099/00207713-46-1-234
CAS Article Google Scholar
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:91–98
Google Scholar
Harrison PG, Strulo B (2000) SPADES—a process algebra for discrete event simulation. J Logic Comput 10:3–42. https://doi.org/10.1093/logcom/10.1.3
Article Google Scholar
Hua Z-S, Qu Y-N, Zhu Q, Zhou E-M, Qi Y-L, Yin Y-R, Rao Y-Z, Tian Y, Li Y-X, Liu L, Castelle CJ, Hedlun BP, Shu W-S, Knight R, Li W-J (2018) Genomic inference of the metabolism and evolution of the archaeal phylum Aigarchaeota. Nat Commun 9:2832. https://doi.org/10.1038/s41467-018-05284-4
Article CAS PubMed PubMed Central Google Scholar
Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW, Hauser LJ (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119. https://doi.org/10.1186/1471-2105-11-119
Article CAS PubMed PubMed Central Google Scholar
Jogler M, Chen H, Simon J, Rohde M, Busse H-J, Klenk H-P, Tindall BJ, Overmann J (2013) Description of Sphingorhabdus planktonica gen. nov., sp. nov. and reclassification of three related members of the genus Sphingopyxis in the genus Sphingorhabdus gen. nov. Int J Syst Evol Microbiol 63:1342–1349. https://doi.org/10.1099/ijs.0.043133-0
Article PubMed Google Scholar
Kalnenieks U (2006) Physiology of Zymomonas mobilis: some unanswered questions. In: Poole RK (ed) Advances in microbial physiology, vol 51. Academic Press, Cambridge, pp 73–117. https://doi.org/10.1016/s0065-2911(06)51002-1
Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K (2017) KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res 45:D353–D361. https://doi.org/10.1093/nar/gkw1092
Article CAS PubMed Google Scholar
Kim MK, Schubert K, Im W-T, Kim K-H, Lee S-T, Overmann J (2007) Sphingomonas kaistensis sp. nov., a novel alphaproteobacterium containing pufLM genes. Int J Syst Evol Microbiol 57:1527–1534. https://doi.org/10.1099/ijs.0.64579-0
Article CAS PubMed Google Scholar
Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge
Book Google Scholar
Kosako Y, Yabuuchi E, Naka T, Fujiwara N, Kobayashi K et al (2000) Proposal of Sphingomonadaceae fam. nov., consisting of Sphingomonas Yabuuchi et al. 1990, Erythrobacter Shiba and Shimidu 1982, Erythromicrobium Yurkov et al. 1994, Porphyrobacter Fuerst et al. 1993, Zymomonas Kluyver and van Niel 1936, and Sandaracinobacter Yurkov et al. 1997, with the type genus Sphingomonas Yabuuchi et al. 1990. Microbiol Immunol 44:563–575. https://doi.org/10.1111/j.1348-0421.2000.tb02535.x
Article CAS PubMed Google Scholar
Kovacs N (1956) Identification of Pseudomonas pyocyanea by the oxidase reaction. Nature 178:703–704. https://doi.org/10.1038/178703a0
Article CAS PubMed Google Scholar
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Article CAS PubMed PubMed Central Google Scholar
Leifson E (1960) Atlas of bacterial flagellation. Academic Press, New York
Book Google Scholar
Li W-J, Xu P, Schumann P, Zhang Y-Q, Pukall R, Xu L-H, Stackebrandt E, Jiang C-L (2007) Georgenia ruanii sp. nov., a novel actinobacterium isolated from forest soil in Yunnan (China), and emended description of the genus Georgenia. Int J Syst Evol Microbiol 57:1424–1428. https://doi.org/10.1099/ijs.0.64749-0
Article PubMed Google Scholar
Mac Faddin JF (1976) Biochemical tests for identification of medical bacteria. Williams & Wilkins Co., Baltimore
Google Scholar
Ming H, Nie G-X, Jiang H-C, Yu T-T, Zhou E-M, Feng H-G, Tang S-K, Li W-J (2012) Paenibacillus frigoriresistens sp. nov., a novel psychrotroph isolated from a peat bog in Heilongjiang, Northern China. Antonie van Leeuwenhoek 102:297–305. https://doi.org/10.1007/s10482-012-9738-7
Article CAS PubMed Google Scholar
Minnikin DE, Collins MD, Goodfellow M (1979) Fatty acid and polar lipid composition in the classification of Cellulomonas, Oerskovia and related taxa. J Appl Bacteriol 47:87–95. https://doi.org/10.1111/j.1365-2672.1979.tb01172.x
Article CAS Google Scholar
Nie G-X, Ming H, Li S, Zhou E-M, Cheng J, Tang X, Feng H-G, Tang S-K, Li W-J (2012) Amycolatopsis dongchuanensis sp. nov., an actinobacterium isolated from soil. Int J Syst Evol Microbiol 62:2650–2656. https://doi.org/10.1099/ijs.0.038125-0
Article CAS PubMed Google Scholar
Qin Q-L, Xie B-B, Zhang X-Y, Chen X-L, Zhou B-C, Zhou J, Oren A, Zhang Y-X (2014) A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 196:2210–2215. https://doi.org/10.1128/jb.01688-14
Article PubMed PubMed Central Google Scholar
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
CAS PubMed Google Scholar
Sasser M (2001) Identification of bacteria by gas chromatography of cellular fatty acids. http://www.microbialid.com/PDF/TechNote_101.pdf
Sheu S-Y, Liu L-P, Young C-C, Chen W-M (2017) Novosphingobium fontis sp. nov., isolated from a spring. Int J Syst Evol Microbiol 67:2423–2429. https://doi.org/10.1099/ijsem.0.001973
Article CAS PubMed Google Scholar
Sly LI, Cahill MM (1997) Transfer of Blastobacter natatorius (Sly 1985) to the genus Blastomonas gen. nov. as Blastomonas natatoria comb. nov. Int J Syst Evol Microbiol 47:566–568. https://doi.org/10.1099/00207713-47-2-566
CAS Article Google Scholar
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Article CAS PubMed PubMed Central Google Scholar
Takeuchi M, Kawai F, Shimada Y, Yokota A (1993) Taxonomic study of polyethylene glycol-utilizing bacteria: emended description of the genus Sphingomonas and new descriptions of Sphingomonas macrogoltabidus sp. nov., Sphingomonas sanguis sp. nov. and Sphingomonas terrae sp. nov. Syst Appl Microbiol 16:227–238. https://doi.org/10.1016/S0723-2020(11)80473-X
Article CAS Google Scholar
Takeuchi M, Hamana K, Hiraishi A (2001) Proposal of the genus Sphingomonas sensu stricto and three new genera, Sphingobium, Novosphingobium and Sphingopyxis, on the basis of phylogenetic and chemotaxonomic analyses. Int J Syst Evol Microbiol 51:1405–1417. https://doi.org/10.1099/00207713-51-4-1405
Article CAS PubMed Google Scholar
Tatusov RL, Natale DA, Garkavtsev IV, Tatusova TA, Shankavaram UT, Rao BS, Kiryutin B, Galperin MY, Fedorova ND, Koonin EV (2001) The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29:22–28. https://doi.org/10.1093/nar/29.1.22
Article CAS PubMed PubMed Central Google Scholar
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. https://doi.org/10.1093/nar/25.24.4876
Article CAS PubMed PubMed Central Google Scholar
Tindall BJ, Sikorski J, Smibert RA, Krieg NR (2007) Phenotypic characterization and the principles of comparative systematics. In: Reddy CA, Beveridge TJ, Breznak JA, Marzluf GA, Schmidt TM, Snyder LR (eds) Methods for general and molecular microbiology, 3rd edn. American Society of Microbiology, Washington DC, pp 330–393. https://doi.org/10.1128/9781555817497.ch15
Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617. https://doi.org/10.1099/ijsem.0.001755
Article CAS PubMed PubMed Central Google Scholar
Zwart G, Crump BC, Kamst-van Agterveld MP, Hagen F, Han S-K (2002) Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers. Aquat Microb Ecol 28:141–155
Article Google Scholar

Download references

Acknowledgements

This research was supported by the Natural Science Foundation of China (No. 31528001). X. Mou was supported by the Ohio Board of Regents (sub-award no. 60049296). W.-J. Li was also supported by Guangdong Province Higher Vocational Colleges & Schools Pearl River Scholar Funded Scheme (2014).

Author information

Xin Li, Jia-Ling Li, and Xiao-Tong Zhang have contributed equally to this work.

Authors and Affiliations

State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, 510275, People’s Republic of China
Xin Li, Jia-Ling Li, Xiao-Tong Zhang, Li Duan, Mipeshwaree Devi Asem, Min Xiao, Nimaichand Salam & Wen-Jun Li
Department of Biological Sciences, Kent State University, Kent, OH, 44242, USA
Xiaozhen Mou
College of Fisheries, Henan Normal University, Xinxiang, 453007, People’s Republic of China
Wen-Jun Li

Authors

Xin Li
View author publications
You can also search for this author in PubMed Google Scholar
Jia-Ling Li
View author publications
You can also search for this author in PubMed Google Scholar
Xiao-Tong Zhang
View author publications
You can also search for this author in PubMed Google Scholar
Li Duan
View author publications
You can also search for this author in PubMed Google Scholar
Mipeshwaree Devi Asem
View author publications
You can also search for this author in PubMed Google Scholar
Min Xiao
View author publications
You can also search for this author in PubMed Google Scholar
Xiaozhen Mou
View author publications
You can also search for this author in PubMed Google Scholar
Nimaichand Salam
View author publications
You can also search for this author in PubMed Google Scholar
Wen-Jun Li
View author publications
You can also search for this author in PubMed Google Scholar

Contributions

N.S. and W.J.L. conceived the study. X.L., J.L.L, X.T.Z., N.S., L.D. and M.D.A. performed research. N.S., X.M. and M.X. analyzed data. X.L., N.S. and W.J.L. wrote the paper. All authors approved the manuscript.

Corresponding authors

Correspondence to Nimaichand Salam or Wen-Jun Li.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 600 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Li, X., Li, JL., Zhang, XT. et al. Aestuariisphingobium litorale gen. nov., sp. nov., a novel proteobacterium isolated from a water sample of Pearl River estuary. Antonie van Leeuwenhoek 112, 1357–1367 (2019). https://doi.org/10.1007/s10482-019-01268-6

Download citation

Received: 31 December 2018
Accepted: 19 April 2019
Published: 25 April 2019
Issue Date: 15 September 2019
DOI: https://doi.org/10.1007/s10482-019-01268-6

Keywords

Aestuariisphingobium litorale gen. nov., sp. nov.
Polyphasic taxonomy
Pearl River estuary