Abstract
A novel moderately halophilic bacterial strain, designated Z330T, was isolated from the egg of a marine invertebrate of the genus Onchidium collected in the South China Sea. The 16S rRNA gene sequence of strain Z330T exhibited the highest similarity value to that of the type strain Paracoccus fistulariae KCTC 22803T (97.6%), Paracoccus seriniphilus NBRC 100798T (97.6%) and Paracoccus aestuarii DSM 19484T (97.6%). Phylogenomic and 16S rRNA phylogenetic analysis showed that strain Z330T was most closely related to P. seriniphilus NBRC 100798T and P. fistulariae KCTC 22803T. Strain Z330T grew optimally at 28–30 °C, pH 7.0–8.0 with the presence of 5.0–7.0% (w/v) NaCl. In addition, growth of strain Z330T occurred at 0.5–16% NaCl, indicated strain Z330T was a moderately halophilic and halotolerant bacterium of genus Paracoccus. The predominant respiratory quinone in strain Z330T was identified as ubiquinone-10. The major polar lipids of strain Z330T were phosphatidylcholine, phosphatidylglycerol, diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylmonomethylethanolamine, glycolipid and six unidentified polar lipids. The major fatty acids of strain Z330T was summed feature 8 (C18:1 ω6c and/or C18:1 ω7c). The draft genome sequence of strain Z330T includes 4,084,570 bp in total (N50 = 174,985 bp) with a medium read coverage of 463.6 × and 83 scaffolds. The DNA G + C content of strain Z330T was 60.5%. In silico DNA–DNA hybridization with the four type strains showed 20.5, 22.3, 20.1 and 20.1% relatedness to Paracoccus fistulariae KCTC 22803T, Paracoccus seriniphilus NBRC 100798T, Paracoccus aestuarii DSM 19484T and Paracoccus denitrificans 1A10901T, respectively. And the average nucleotide identity (ANIb) values between strain Z330T and these four type strains were 76.2, 80.0, 75.8 and 73.8%, respectively, lower than the 95–96% threshold value for dividing prokaryotic species. On the basis of the phenotypic, phylogenetic, phylogenomic and chemotaxonomic properties, a novel species of the genus Paracoccus, Paracoccus onchidii sp. nov. is proposed with the type strain Z330T (= KCTC 92727T = MCCC 1K08325T).
Similar content being viewed by others
Abbreviations
- R2A:
-
Reasoner’s 2A agar
- MA:
-
Marine agar
- MB:
-
Marine broth
- ANI:
-
Average nucleotide identity
- dDDH:
-
Digital DNA–DNA hybridization
- TLC:
-
Thin-layer chromatography
References
Argüelles JC (2000) Physiological roles of trehalose in bacteria and yeasts: a comparative analysis. Arch Microbiol 174:217–224. https://doi.org/10.1007/s002030000192
Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: rapid annotations using subsystems technology. BMC Genom 9:75. https://doi.org/10.1186/1471-2164-9-75
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. https://doi.org/10.1089/cmb.2012.0021
Beveridge TJ, Lawrence JR, Murray RG (2007) Sampling and staining for light microscopy. In: Reddy CA, Beveridge TJ, Breznak JA, Marzluf GA, Schmidt TM, Snyder LR (eds) Methods for general and molecular microbiology. ASM Press, Washington
Blin K, Shaw S, Kloosterman AM, Charlop-Powers Z, van Wezel GP, Medema MH, Weber T (2021) antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Res 49:W29-w35. https://doi.org/10.1093/nar/gkab335
Chen WM, Li YS, Young CC, Sheu SY (2017) Paracoccus mangrovi sp. nov., isolated from a mangrove. Int J Syst Evol Microbiol 67:2689–2695. https://doi.org/10.1099/ijsem.0.001993
Collins M (1985) Isoprenoid quinone analyses in bacterial classification and identification. In: Goodfellow M, Minnikin DE (eds) Chemical methods in bacterial systematics. Academic Press, London, pp 267–287
Davis DH, Doudoroff M, Stanier RY, Mandel M (1969) Proposal to reject the genus Hydrogenomonas: taxonomic implications. Int J Syst Bacteriol 19:375–390
Delcher AL, Bratke KA, Powers EC, Salzberg SL (2007) Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23:673–679. https://doi.org/10.1093/bioinformatics/btm009
Dong X, Zhang G, Xiong Q, Liu D, Wang D, Liu Y, Wu G, Li P, Luo Y, Zhang R (2018) Paracoccus salipaludis sp. nov., isolated from saline-alkaline soil. Int J Syst Evol Microbiol 68:3812–3817. https://doi.org/10.1099/ijsem.0.003065
Eronen-Rasimus E, Hultman J, Hai T, Pessi IS, Collins E, Wright S, Laine P, Viitamäki S, Lyra C, Thomas DN, Golyshin PN, Luhtanen AM, Kuosa H, Kaartokallio H (2021) Sea-ice bacteria Halomonas sp. strain 363 and Paracoccus sp. strain 392 produce multiple types of poly-3-hydroxyalkaonoic acid (PHA) storage polymers at low temperature. Appl Environ Microbiol 87:e0092921. https://doi.org/10.1128/aem.00929-21
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376. https://doi.org/10.1007/bf01734359
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Biol 20:406–416
Jandhyala SM, Talukdar R, Subramanyam C, Vuyyuru H, Sasikala M, Nageshwar Reddy D (2015) Role of the normal gut microbiota. World J Gastroenterol 21:8787–8803. https://doi.org/10.3748/wjg.v21.i29.8787
Kates M (1986) Techniques of lipidology. Elsevier, Amsterdam, pp 106–107, 241–246
Knobloch S, Jóhannsson R, Marteinsson V (2019) Co-cultivation of the marine sponge Halichondria panicea and its associated microorganisms. Sci Rep 9:10403. https://doi.org/10.1038/s41598-019-46904-3
Kumar P, Jun HB, Kim BS (2018) Co-production of polyhydroxyalkanoates and carotenoids through bioconversion of glycerol by Paracoccus sp. strain LL1. Int J Biol Macromol 107:2552–2558. https://doi.org/10.1016/j.ijbiomac.2017.10.147
Lee I, Ouk Kim Y, Park SC, Chun J (2016) OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 66:1100–1103. https://doi.org/10.1099/ijsem.0.000760
Lee JY, Hyun DW, Yun JH, Jung MJ, Shin NR, Bae JW (2019) Paracoccus tegillarcae sp. nov., isolated from the gastrointestinal tract of a blood cockle (Tegillarca granosa). Int J Syst Evol Microbiol 69:2815–2822. https://doi.org/10.1099/ijsem.0.003561
Letunic I, Bork P (2021) Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49:W293-w296. https://doi.org/10.1093/nar/gkab301
Li R, Zhu H, Ruan J, Qian W, Fang X, Shi Z, Li Y, Li S, Shan G, Kristiansen K, Li S, Yang H, Wang J, Wang J (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20:265–272. https://doi.org/10.1101/gr.097261.109
Liang J, Yin Q, Zheng X, Wang Y, Song ZM, Zhang Y, Hao L, Xu Y (2021) Muricauda onchidii sp. nov., isolated from a marine invertebrate from South China Sea, and transfers of Flagellimonas algicola, Flagellimonas pacifica and Flagellimonas maritima to Muricauda algicola comb. nov., Muricauda parva nom. nov. and Muricauda aurantiaca nom. nov., respectively, and emended description of the genus Muricauda. Int J Syst Evol Microbiol. https://doi.org/10.1099/ijsem.0.004982
Liu ZP, Wang BJ, Liu XY, Dai X, Liu YH, Liu SJ (2008) Paracoccus halophilus sp. nov., isolated from marine sediment of the South China Sea, China, and emended description of genus Paracoccus Davis 1969. Int J Syst Evol Microbiol 58:257–261. https://doi.org/10.1099/ijs.0.65237-0
Lopanik NB, Targett NM, Lindquist N (2006) Isolation of two polyketide synthase gene fragments from the uncultured microbial symbiont of the marine bryozoan Bugula neritina. Appl Environ Microbiol 72:7941–7944. https://doi.org/10.1128/aem.01277-06
Lyu L, Zhi B, Lai Q, Shao Z, Yu Z (2020) Paracoccus xiamenensis sp. nov., isolated from seawater on the Xiamen. Int J Syst Evol Microbiol 70:4285–4290. https://doi.org/10.1099/ijsem.0.004284
Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 14:60. https://doi.org/10.1186/1471-2105-14-60
Meier-Kolthoff JP, Klenk HP, Göker M (2014) Taxonomic use of DNA G+C content and DNA–DNA hybridization in the genomic age. Int J Syst Evol Microbiol 64:352–356. https://doi.org/10.1099/ijs.0.056994-0
Meng XL, Ming H, Huang JR, Zhang LY, Cheng LJ, Zhao ZL, Ji WL, Li WJ, Nie GX (2019) Paracoccus halotolerans sp. nov., isolated from a salt lake. Int J Syst Evol Microbiol 69:523–528. https://doi.org/10.1099/ijsem.0.003190
Montalvo-Rodríguez R, Maupin-Furlow JA (2020) Insights through genetics of halophilic microorganisms and their viruses. Genes. https://doi.org/10.3390/genes11040388
Na SI, Kim YO, Yoon SH, Ha SM, Baek I, Chun J (2018) UBCG: up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J Microbiol 56:280–285. https://doi.org/10.1007/s12275-018-8014-6
Olaya-Abril A, Luque-Almagro VM, Manso I, Gates AJ, Moreno-Vivián C, Richardson DJ, Roldán MD (2018) Poly(3-hydroxybutyrate) hyperproduction by a global nitrogen regulator NtrB mutant strain of Paracoccus denitrificans PD1222. FEMS Microbiol Lett. https://doi.org/10.1093/femsle/fnx251
Oren A (2010) Industrial and environmental applications of halophilic microorganisms. Environ Technol 31:825–834. https://doi.org/10.1080/09593330903370026
Pan J, Sun C, Zhang XQ, Huo YY, Zhu XF, Wu M (2014) Paracoccus sediminis sp. nov., isolated from pacific ocean marine sediment. Int J Syst Evol Microbiol 64:2512–2516. https://doi.org/10.1099/ijs.0.051318-0
Parte AC (2018) LPSN—list of prokaryotic names with standing in nomenclature (bacterio.net), 20 years on. Int J Syst Evol Microbiol 68:1825–1829. https://doi.org/10.1099/ijsem.0.002786
Puri A, Bajaj A, Singh Y, Lal R (2022) Harnessing taxonomically diverse and metabolically versatile genus Paracoccus for bioplastic synthesis and xenobiotic biodegradation. J Appl Microbiol 132:4208–4224. https://doi.org/10.1111/jam.15530
Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106:19126–19131. https://doi.org/10.1073/pnas.0906412106
Romano G, Almeida M, Varela Coelho A, Cutignano A, Gonçalves LG, Hansen E, Khnykin D, Mass T, Ramšak A, Rocha MS, Silva TH, Sugni M, Ballarin L, Genevière AM (2022) Biomaterials and bioactive natural products from marine invertebrates: from basic research to innovative applications. Mar Drugs. https://doi.org/10.3390/md20040219
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Sang VT, Dat TTH, Vinh LB, Cuong LCV, Oanh PTT, Ha H, Kim YH, Anh HLT, Yang SY (2019) Coral and coral-associated microorganisms: a prolific source of potential bioactive natural products. Mar Drugs. https://doi.org/10.3390/md17080468
Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. Usfcc Newsl
Sun LN, Zhang J, Kwon SW, He J, Zhou SG, Li SP (2013) Paracoccus huijuniae sp. nov., an amide pesticide-degrading bacterium isolated from activated sludge of a wastewater biotreatment system. Int J Syst Evol Microbiol 63:1132–1137. https://doi.org/10.1099/ijs.0.044180-0
Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38:3022–3027. https://doi.org/10.1093/molbev/msab120
Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP, Zaslavsky L, Lomsadze A, Pruitt KD, Borodovsky M, Ostell J (2016) NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 44:6614–6624. https://doi.org/10.1093/nar/gkw569
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
Tindall BJ, Sikorski J, Smibert RA, Krieg NR (2007) Phenotypic characterization and the principles of comparative systematics. Am Soc Microbiol. https://doi.org/10.1128/9781555817497.ch15
Vargas C, Argandoña M, Reina-Bueno M, Rodríguez-Moya J, Fernández-Aunión C, Nieto JJ (2008) Unravelling the adaptation responses to osmotic and temperature stress in Chromohalobacter salexigens, a bacterium with broad salinity tolerance. Saline Syst 4:14. https://doi.org/10.1186/1746-1448-4-14
Wang Y, Tang SK, Lou K, Mao PH, Jin X, Jiang CL, Xu LH, Li WJ (2009) Paracoccus saliphilus sp. nov., a halophilic bacterium isolated from a saline soil. Int J Syst Evol Microbiol 59:1924–1928. https://doi.org/10.1099/ijs.0.005918-0
Wei Y, Cao J, Yao H, Mao H, Zhu K, Li M, Liu R, Fang J (2019) Paracoccus sediminilitoris sp. nov., isolated from a tidal flat sediment. Int J Syst Evol Microbiol 69:1035–1040. https://doi.org/10.1099/ijsem.0.003265
Wibowo JT, Kellermann MY, Versluis D, Putra MY, Murniasih T, Mohr KI, Wink J, Engelmann M, Praditya DF, Steinmann E, Schupp PJ (2019) Biotechnological potential of bacteria isolated from the sea cucumber Holothuria leucospilota and Stichopus vastus from Lampung, Indonesia. Mar Drugs. https://doi.org/10.3390/md17110635
Yin Q, Song ZM, Liang J, Wang Y, Zheng X, Li S, Xu Y (2020) Pseudooceanicola onchidii sp. nov., isolated from a marine invertebrate from the South China Sea. Int J Syst Evol Microbiol 70:1224–1230. https://doi.org/10.1099/ijsem.0.003905
Yin Q, Liang J, Zheng X, Wang Y, Song ZM, Zhang Y, Xu Y (2021) Algibacter onchidii sp. Nov., a symbiotic bacterium isolated from a marine invertebrate. Int J Syst Evol Microbiol. https://doi.org/10.1099/ijsem.0.005102
Yoon SH, Ha SM, Lim J, Kwon S, Chun J (2017a) A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 110:1281–1286. https://doi.org/10.1007/s10482-017-0844-4
Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017b) 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
Zhuang X, Han Z, Bai Z, Zhuang G, Shim H (2010) Progress in decontamination by halophilic microorganisms in saline wastewater and soil. Environ Pollut 158:1119–1126. https://doi.org/10.1016/j.envpol.2010.01.007
Zou YJ, Yang LF, Wang L, Yang SS (2008) Cloning and characterization of a Na+/H+ antiporter gene of the moderately halophilic bacterium Halobacillus aidingensis AD-6T. J Microbiol 46:415–421. https://doi.org/10.1007/s12275-008-0009-2
Funding
This work was supported by grants from the Shenzhen Science and Technology Program (JCYJ20210324093409025).
Author information
Authors and Affiliations
Contributions
SSX: investigation, conceptualization, formal analysis, writing—original draft, writing—review and editing, project administration. QLL: investigation and formal analysis. ZZL: project administration, conceptualization, formal analysis, writing—review and editing. YX: funding acquisition.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Xu, Ss., Lai, Ql., Liu, Zz. et al. Paracoccus onchidii sp. nov., a moderately halophilic bacterium isolated from a marine invertebrate from the South China Sea. Antonie van Leeuwenhoek 116, 801–815 (2023). https://doi.org/10.1007/s10482-023-01848-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-023-01848-7