Abstract
A marine bacterial strain, named NTOU-MSR1T, was isolated from marine sediment of northern coast of Taiwan. This bacterium was Gram-stain-negative, aerobic, and motile, with a single flagellum. Its rod-shaped cells measured approximately 0.5–0.6 µm in width and 1.8–2.0 μm in length. NTOU-MSR1T grew at temperatures ranging from 10 to 45 °C, optimally at 30 °C. The pH range for growth was 7.0–10.0, with optimal growth at pH 7.0–8.0. It tolerated NaCl concentrations up to 12%. The cell membrane predominantly contained fatty acids such C16:1ω7c, C18:1ω7c, and C16:0. The overall genome relatedness indices indicated that strain NTOU-MSR1T had an average nucleotide identity (ANI) of 87.88% and a digital DNA-DNA hybridization (dDDH) value of 35.40% compared to its closest related species, O. marisflavi 102-Na3T. These values fell below the 95% and 70% threshold for species delineation, respectively. These findings suggested that the strain NTOU-MSR1T was a new member of the Oceanimonas genus. Its genomic DNA had a G + C content of 61.0 mol%. Genomic analysis revealed genes associated with the catechol branch of β- ketoadipate pathway for degrading polycyclic aromatic hydrocarbons, resistance to heavy metal, biosynthesis of polyhydroxybutyrate and the production of glycoside hydrolases (GH19, GH23, and GH103) for chitin and glycan digestion. Additionally, NTOU-MSR1T was capable of synthesizing biosurfactants and potentially degrading plastic. The proposed name for this new species is Oceanimonas pelagia, with the type strain designated as NTOU-MSR1T (= BCRC 81403T = JCM 36023T).
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The bacterium Oceanimonas pelagia NTOU-MSR1T has been deposited in the BCRC collection with the accession number BCRC 81403, and in the JCM collection with the accession number JCM 36023. The 16S rRNA sequence and the complete whole genome sequence of Oceanimonas pelagia NTOU-MSR1T have been deposited in the GenBank database under accession numbers OQ450183 and CP118224. The supplementary file is available in the online edition of this article.
References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Arndt D, Grant JR, Marcu A, Sajed T, Pon A, Liang Y, Wishart DS (2016) PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 44(W1):W16–W21. https://doi.org/10.1093/nar/gkw387
Baumann L, Baumann P, Mandel M, Allen RD (1972) Taxonomy of aerobic marine eubacteria. J Bacteriol 110(1):402–429. https://doi.org/10.1128/jb.110.1.402-429.1972
Bertelli C, Laird MR, Williams KP, Lau BY, Hoad G, Winsor GL, Brinkman FSL, Simon Fraser University Research Computing Group (2017) IslandViewer 4: expanded prediction of genomic islands for larger-scale datasets. Nucleic Acids Res 45(W1):W30–W35. https://doi.org/10.1093/nar/gkx343
Blin K, Shaw S, Augustijn HE, Reitz ZL, Biermann F, Alanjary M, Fetter A, Terlouw BR, Metcalf WW, Helfrich EJN, van Wezel GP, Medema MH, Weber T (2023) antiSMASH 7.0: new and improved predictions for detection, regulation, chemical structures and visualisation. Nucleic Acids Res 51(W1):W46–W50. https://doi.org/10.1093/nar/gkad344
Brown GR, Sutcliffe IC, Cummings SP (2001) Reclassification of [Pseudomonas] doudoroffii (Baumann et al. 1983) into the genus Oceanomonas gen. nov. as Oceanomonas doudoroffii comb. Nov., and description of a phenol-degrading bacterium from estuarine water as Oceanomonas baumannii sp nov. Int J Syst Evolut Microbiol 51(1):67–72. https://doi.org/10.1099/00207713-51-1-67
Brown GR, Sutcliffe IC, Cummings SP (2003) Combined solvent and water activity stresses on turgor regulation and membrane adaptation in Oceanimonas baumannii ATCC 700832. Antonie Van Leeuwenhoek 83(3):275–283. https://doi.org/10.1023/a:1023348928376
Chatterjee S, Roy B, Roy D, Banerjee R (2010) Enzyme-mediated biodegradation of heat treated commercial polyethylene by Staphylococcal species. Polym Degrad Stab 95(2):195–200
Cooper DG, Goldenberg BG (1987) Surface-active agents from two bacillus species. Appl Environ Microbiol 53(2):224–229. https://doi.org/10.1128/aem.53.2.224-229.1987
Fisner M, Taniguchi S, Moreira F, Bícego MC, Turra A (2013) Polycyclic aromatic hydrocarbons (PAHs) in plastic pellets: variability in the concentration and composition at different sediment depths in a sandy beach. Mar Pollut Bull 70(1–2):219–226. https://doi.org/10.1016/j.marpolbul.2013.03.008
Giachino A, Waldron KJ (2020) Copper tolerance in bacteria requires the activation of multiple accessory pathways. Mol Microbiol 114(3):377–390. https://doi.org/10.1111/mmi.14522
Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57(Pt 1):81–91. https://doi.org/10.1099/ijs.0.64483-0
Howard G, Hilliard N (1999) Use of Coomassie blue-polyurethane interaction inscreening of polyurethanase proteins andpolyurethanolytic bacteria. Int Biodeterior Biodegr 43(1–2):23–30. https://doi.org/10.1016/S0964-8305(98)00062-6
Huang YT, Liu PY, Shih PW (2021) Homopolish: a method for the removal of systematic errors in nanopore sequencing by homologous polishing. Genome Biol 22(1):95. https://doi.org/10.1186/s13059-021-02282-6
Ibrahim MH, Steinbüchel A (2010) Zobellella denitrificans strain MW1, a newly isolated bacterium suitable for poly(3-hydroxybutyrate) production from glycerol. J Appl Microbiol 108(1):214–225. https://doi.org/10.1111/j.1365-2672.2009.04413.x
Ivanova EP, Onyshchenko OM, Christen R, Zhukova NV, Lysenko AM, Shevchenko LS, Buljan V, Hambly B, Kiprianova EA (2005) Oceanimonas smirnovii sp. Nov., a novel organism isolated from the Black Sea. Syst Appl Microbiol 28(2):131–136. https://doi.org/10.1016/j.syapm.2004.11.002
Jansen B, Schumacher-Perdreau F, Peters G, Pulverer G (1991) Evidence for degradation of synthetic polyurethanes by Staphylococcus epidermidis. Zentralblatt fur Bakteriologie: Int J Med Microbiol 276(1):36–45. https://doi.org/10.1016/s0934-8840(11)80216-1
Joshi G, Goswami P, Verma P, Prakash G, Simon P, Vinithkumar NV, Dharani G (2022) Unraveling the plastic degradation potentials of the plastisphere-associated marine bacterial consortium as a key player for the low-density polyethylene degradation. J Hazard Mater 425:128005. https://doi.org/10.1016/j.jhazmat.2021.128005
Kolmogorov M, Bickhart DM, Behsaz B, Gurevich A, Rayko M, Shin SB, Kuhn K, Yuan J, Polevikov E, Smith TPL, Pevzner PA (2020) metaFlye: scalable long-read metagenome assembly using repeat graphs. Nat Methods 17(11):1103–1110. https://doi.org/10.1038/s41592-020-00971-x
Konstantinidis KT, Tiedje JM (2005) Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci USA 102(7):2567–2572. https://doi.org/10.1073/pnas.0409727102
Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19(9):1639–1645. https://doi.org/10.1101/gr.092759.109
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(2):1100–1103. https://doi.org/10.1099/ijsem.0.000760
Lee DW, Lee H, Kwon BO, Khim JS, Yim UH, Park H, Park B, Choi IG, Kim BS, Kim JJ (2018) Oceanimonas marisflavi sp. nov., a polycyclic aromatic hydrocarbon-degrading marine bacterium. Int J Syst Evolut Microbiol 68(9):2990–2995. https://doi.org/10.1099/ijsem.0.002932
Letunic I, Bork P (2021) Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49(W1):W293–W296. https://doi.org/10.1093/nar/gkab301
Li J, Li Z, Cao M, Liu J (2021) Expression and characterization of catechol 1,2-dioxygenase from Oceanimonas marisflavi 102-Na3. Protein Expr Purif 188:105964. https://doi.org/10.1016/j.pep.2021.105964
Mato Y, Isobe T, Takada H, Kanehiro H, Ohtake C, Kaminuma T (2001) Plastic resin pellets as a transport medium for toxic chemicals in the marine environment. Environ Sci Technol 35(2):318–324. https://doi.org/10.1021/es0010498
Meier-Kolthoff JP, Göker M (2019) TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 10(1):2182. https://doi.org/10.1038/s41467-019-10210-3
Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinf 14:60. https://doi.org/10.1186/1471-2105-14-60
Meier-Kolthoff JP, Carbasse JS, Peinado-Olarte RL, Göker M (2022) TYGS and LPSN: a database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Res 50(D1):D801–D807. https://doi.org/10.1093/nar/gkab902
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 (seoul, Korea) 56(4):280–285. https://doi.org/10.1007/s12275-018-8014-6
Nademo ZM, Shibeshi NT, Gemeda MT (2023) Isolation and screening of low-density polyethylene (LDPE) bags degrading bacteria from Addis Ababa municipal solid waste disposal site “Koshe.” Ann Microbiol 73(1):6. https://doi.org/10.1186/s13213-023-01711-0
Nigam A (2007) Lab manual in biochemistry, immunology and biotechnology. Tata McGraw-Hill Education, Newyork
Notification that new names and new combinations have appeared in volume 51, part 1, of the IJSEM. (2001). International journal of systematic and evolutionary microbiology, 51(Pt 2), 269. https://doi.org/10.1099/00207713-51-2-269
Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 25(7):1043–1055. https://doi.org/10.1101/gr.186072.114
Payne DE, Martin NR, Parzych KR, Rickard AH, Underwood A, Boles BR (2013) Tannic acid inhibits staphylococcus aureus surface colonization in an IsaA-dependent manner. Infect Immun 81(2):496–504. https://doi.org/10.1128/IAI.00877-12
Ramezani M, Amoozegar MA, Ventosa A (2015) Screening and comparative assay of poly-hydroxyalkanoates produced by bacteria isolated from the Gavkhooni Wetland in Iran and evaluation of poly-β-hydroxybutyrate production by halotolerant bacterium Oceanimonas sp. GK1. Ann Microbiol 65:517–526. https://doi.org/10.1007/s13213-014-0887-y
Saini N, Bhadury P (2022) Genome analysis of a plastisphere-associated Oceanimonas sp NSJ1 sequenced on Nanopore MinION platform. IOP SciNotes 3(4):044601. https://doi.org/10.1088/2633-1357/ac986e
Sasser, M. (1990). Identification of bacteria by gas chromatography of cellular fatty acids, MIDI technical note 101. Newark, DE: MIDI inc.
Stapleton MR, Horsburgh MJ, Hayhurst EJ, Wright L, Jonsson IM, Tarkowski A, Kokai-Kun JF, Mond JJ, Foster SJ (2007) Characterization of IsaA and SceD, two putative lytic transglycosylases of Staphylococcus aureus. J Bacteriol 189(20):7316–7325. https://doi.org/10.1128/JB.00734-07
Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38(7):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(14):6614–6624. https://doi.org/10.1093/nar/gkw569
Thompson JD, Gibson TJ, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protocols Bioinf 1:2–3. https://doi.org/10.1002/0471250953.bi0203s00
Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, Cuomo CA, Zeng Q, Wortman J, Young SK, Earl AM (2014) Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9(11):e112963. https://doi.org/10.1371/journal.pone.0112963
Zhou Z, Tran PQ, Breister AM, Liu Y, Kieft K, Cowley ES, Karaoz U, Anantharaman K (2022) METABOLIC: high-throughput profiling of microbial genomes for functional traits, metabolism, biogeochemistry, and community-scale functional networks. Microbiome 10(1):33. https://doi.org/10.1186/s40168-021-01213-8
Acknowledgements
The authors thank the Electron Microscopy Center of Institute of Marine Biology at National Taiwan Ocean University for technical assistance and the Biological Resource Center (BCRC) for their technical expertise in conducting fatty acid identification for this study.
Funding
This study was supported by the National Science and Technology Council of Taiwan (MOST 111–2628-M-019–001-MY3).
Author information
Authors and Affiliations
Contributions
YHT and HYN wrote the main manuscript content. YHT isolated and the bacterium and performed all experiments. HYH conducted the experiments to assess the bacterial plastic degradation potential. HYN and YHT prepare all figures, as well as the supplementary file, and reviewed the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no 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
Yang, HT., Huang, YH. & Ho, YN. Oceanimonas pelagia sp. nov., a novel biosurfactant-producing and plastic-degrading potential bacterium isolated from marine coastal sediment. Antonie van Leeuwenhoek 117, 49 (2024). https://doi.org/10.1007/s10482-024-01948-y
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10482-024-01948-y