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Shewanella subflava sp. nov., a novel multi-resistant bacterium, isolated from the estuary of the Fenhe River into the Yellow River

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Abstract

A aerobic, gram-negative, rod-shaped and polar-flagellum bacterial strain, designated as FYR11-62T, was isolated from the estuary of the Fenhe River into the Yellow River in Shanxi Province, China. The isolate was able to grow at 4–37 °C (optimum, 25 °C), pH 5.5–9.5 (optimum, pH 7.5) and in the presence of 0–7.0% (w/v) NaCl (optimum, 1.0% NaCl). Phylogenetic analyses based on 16S rRNA genes and 1597 single-copy orthologous clusters indicated that strain FYR11-62T affiliated with the genus Shewanella and shared the highest 16S rRNA gene sequence similarity to Shewanella aestuarii SC18T (98.3%) and Shewanella gaetbuli TF-27T (97.3%), respectively. The major fatty acids were summed feature 3 (C16:1 ω7c and/or C16:1 ω6c), C16:0 and iso-C15:0. The major polar lipids were phosphatidylethanolamine and phosphatidylglycerol. The main quinones were Q-7 and Q-8. The genomic DNA G + C content was 41.6%. Gene annotation showed that strain FYR11-62T possessed 30 antibiotic resistance genes, implying its multiple antidrug resistance. The average nucleotide identity and digital DNA–DNA hybridization values between strain FYR11-62T and its closely related species were all below the thresholds for species delineation. The phylogenetic position together with the results of the analysis of morphological, physiological and genomic features support the classification of strain FYR11-62T (= MCCC 1K07242T = KCTC 92244T) as a novel species of the genus Shewanella, for which the name Shewanella subflava sp. nov. is proposed.

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Data availability

The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequence and the genome sequence of strain FYR11-62T are OP662613 and JAPDMX000000000, respectively. The datasets generated or analysed during the current study are available from the corresponding author on reasonable request or on NCBI repository. The novel strain has been deposited to MCCC 1K07242 and KCTC 92244.

References

  • Alves VBA, Carvalho E, Madureira PA et al (2020) First isolation and whole-genome sequencing of a Shewanella algae strain from a swine farm in Brazil. BMC Microbiol 20:360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amos GCA, Zhang L, Hawkey PM et al (2014) Functional metagenomic analysis reveals rivers are a reservoir for diverse antibiotic resistance genes. Vet Microbiol 171:441–447

    Article  CAS  PubMed  Google Scholar 

  • Anzai Y, Kim H, Park JY et al (2000) Phylogenetic affiliation of the pseudomonads based on 16S rRNA sequence. Int J Syst Evol Microbiol 50:1563–1589

    Article  CAS  PubMed  Google Scholar 

  • Aziz RK, Bartels D, Best AA et al (2008) The RAST server: rapid annotations using subsystems technology. BMC Genom 9:75

    Article  Google Scholar 

  • Bae SS, Jung Y, Baek K (2020) Shewanella maritima sp. nov., a facultative anaerobic marine bacterium isolated from seawater, and emended description of Shewanella intestini. Int J Syst Evol Microbiol 70:1288–1293

    Article  CAS  PubMed  Google Scholar 

  • Brettar I, Christen R, Höfle MG (2002) Shewanella denitrificans sp. nov., a vigorously denitrifying bacterium isolated from the oxic-anoxic interface of the Gotland Deep in the central Baltic Sea. Int J Syst Evol Microbiol 52:2211–2217

    CAS  PubMed  Google Scholar 

  • Chun J, Oren A, Ventosa A et al (2018) Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 68:461–466

    Article  CAS  PubMed  Google Scholar 

  • Collins MD, Jones D (1980) Lipids in the classification and identification of coryneform bacteria containing peptidoglycans based on 2, 4-diaminobutyric acid. Appl Bacteriol 48:459–470

    Article  CAS  Google Scholar 

  • Duan J, Guo W (2022) The complete genome sequence of Shewanella inventionis D1489 reveals its potential for the production of eicosapentaenoic acid. Mar Genom 62:100932

    Article  CAS  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

  • Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. System Zool 20:406–416

    Article  Google Scholar 

  • Fu L, Wang C, Liu N et al (2018) Quorum sensing system-regulated genes affect the spoilage potential of Shewanella baltica. Food Res Int 107:1–9

    Article  CAS  PubMed  Google Scholar 

  • Goris J, Konstantinidis KT, Klappenbach JA et al (2007) DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91

    Article  CAS  PubMed  Google Scholar 

  • Holmes AH, Moore LS, Sundsfjord A et al (2016) Understanding the mechanisms and drivers of antimicrobial resistance. Lancet 387:176–187

    Article  CAS  PubMed  Google Scholar 

  • Huang YT, Tang YY, Cheng JF et al (2018) Genome analysis of multidrug-resistant Shewanella algae isolated from human soft tissue sample. Front Pharmacol 9:419

    Article  PubMed  PubMed Central  Google Scholar 

  • Jackman SD, Vandervalk BP, Mohamadi H et al (2017) ABySS 2.0: resource-efficient assembly of large genomes using a bloom filter. Genome Res 27:768–777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282

    CAS  PubMed  Google Scholar 

  • Jørgensen BR, Huss HH (1989) Growth and activity of Shewanella putrefaciens isolated from spoiling fish. Int J Food Microbiol 9:51–62

    Article  PubMed  Google Scholar 

  • Kim J, Yoo H, Lee D et al (2016) Shewanella algicola sp. nov., a marine bacterium isolated from brown algae. Int J Syst Evol Microbiol 66:2218–2224

    Article  CAS  PubMed  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Koichiro T, Glen S, Sudhir K (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38:3022–3027

    Article  Google Scholar 

  • Langdon A, Crook N, Dantas G (2016) The effects of antibiotics on the microbiome throughout development and alternative approaches for therapeutic modulation. Genome Med 8:39

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu GH, Zhang Q, Narsing Rao MP et al (2021) Stress response mechanisms and description of three novel species Shewanella avicenniae sp. nov., Shewanella sedimentimangrovi sp. nov. and Shewanella yunxiaonensis sp. nov., isolated from mangrove ecosystem. Antonie Van Leeuwenhoek 114:2123–2131

    Article  CAS  PubMed  Google Scholar 

  • Meier-Kolthoff JP, Auch AF, Klenk HP (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 14:60

    Article  Google Scholar 

  • Minnikin DE, O’Donnell AG, Goodfellow M et al (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–324

    Article  CAS  Google Scholar 

  • Moriya IM, Okuda S et al (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:182–185

    Article  Google Scholar 

  • Murray RGE, Doetsch RN et al (1994) Determinative and cytological light microscopy. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, pp 21–41

    Google Scholar 

  • Nouioui I, Tarhriz V, Kim HM et al (2022) Shewanella azerbaijanica sp. Nov. a novel aquatic species with high bioremediation abilities. Arch Microbiol 204:496

    Article  CAS  PubMed  Google Scholar 

  • Park HY, Jeon CO (2013) Shewanella aestuarii sp. nov., a marine bacterium isolated from a tidal flat. Int J Syst Evol Microbiol 63:4683–4690

    Article  CAS  PubMed  Google Scholar 

  • Pruden A, Pei R, Storteboom H et al (2006) Antibiotic resistance genes as emerging contaminants: studies in northern Colorado. Environ Sci Technol 40:7445–7450

    Article  CAS  PubMed  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 

  • Satomi M, Vogel BF, Gram L et al (2006) Shewanella hafniensis sp. nov. and Shewanella morhuae sp. nov., isolated from marine fish of the Baltic Sea. Int J Syst Evol Microbiol 56:243–249

    Article  CAS  PubMed  Google Scholar 

  • Shi L, Rosso KM, Clarke TA et al (2012) Molecular underpinnings of Fe(III) oxide reduction by Shewanella oneidensis MR-1. Front Microbiol 3:50

    Article  PubMed  PubMed Central  Google Scholar 

  • Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Gerhardt P, Murray RGE, Wood WA, Krige NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, pp 607–654

    Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    CAS  PubMed  Google Scholar 

  • Tatiana T, Michael DC, Azat B et al (2016) NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 44:6614–6624

    Article  Google Scholar 

  • Uhrynowski W, Radlinska M, Drewniak L (2019) Genomic analysis of Shewanella sp. O23S–The natural host of the pSheB plasmid carrying genes for arsenic resistance and dissimilatory reduction. Int J Mol Sci 20:1018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA et al (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Meng Z, Jiao W (2018) Hydrological and pollution processes in mining area of Fenhe River Basin in China. Environ Pollut 234:743–750

    Article  CAS  PubMed  Google Scholar 

  • Yoon JH, Kang KH, Oh TK et al (2004) Shewanella gaetbuli sp. nov., a slight halophile isolated from a tidal flat in Korea. Int J Syst Evol Microbiol 54:487–491

    Article  CAS  PubMed  Google Scholar 

  • Yoon J, Park S, Jung Y et al (2012) Shewanella seohaensis sp. nov., isolated from a tidal fat sediment. Antonie Van Leeuwenhoek 102:149–156

    Article  CAS  PubMed  Google Scholar 

  • Yoon SH, Ha SM, Lim J et al (2017) A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 110:1281–1286

    Article  CAS  PubMed  Google Scholar 

  • Yousfi K, Bekal S, Usongo V et al (2017) Current trends of human infections and antibiotic resistance of the genus Shewanella. Eur J Clin Microbiol Infect Dis 36:1353–1362

    Article  CAS  PubMed  Google Scholar 

  • Yun BR, Park S, Kim MK et al (2018) Shewanella saliphila sp. nov., Shewanella ulleungensis sp. nov. and Shewanella litoralis sp. nov., isolated from coastal seawater. Int J Syst Evol Microbiol 68:2960–2966

    Article  CAS  PubMed  Google Scholar 

  • Zhang Q, Liu G, Rao MPN et al (2021) Shewanella cyperi sp. Nov., a facultative anaerobic bacterium isolated from mangrove sediment. Int J Syst Evol Microbiol 71:004940

    Article  Google Scholar 

  • Zuckerkandl E, Pauling L (1965) Evolving genes and proteins. In: Bryson V, Vogel HJ (eds) Evolutionary divergence and convergence in proteins. Academic Press, New York, pp 97–166

    Google Scholar 

Download references

Acknowledgements

The authors are sincerely grateful to Mei-Ling Sun from Shandong University, State Key Laboratory of Microbial Technology and Yan-Jiao Zhang from Qingdao Agricultural University, School of Life Sciences for their skillful technical assistance.

Funding

This work was funded by the Basic Research Program of Shanxi Province (20210302124004), by the Scientific and Technological Innovation Programs of Shanxi Agricultural University (2020BQ39), by the Basic Research Program of Shanxi Province (20210302123368), by the Scientific and Technological Innovation Programs of Higher Education Institutions in Shanxi Province (2021L134) and by the Excellent Talents Come to Shanxi to Reward Scientific Research Projects (SXYBKY2019025).

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BL, JYS and YNW designed the experiments and wrote the manuscript. LG and KSD performed the genome analysis. HJN revised the manuscript. SFS and YL supervised the experiments.

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Correspondence to Shao-Fei Shen or Yi Li.

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Luo, B., Su, JY., Wang, YN. et al. Shewanella subflava sp. nov., a novel multi-resistant bacterium, isolated from the estuary of the Fenhe River into the Yellow River. Antonie van Leeuwenhoek 116, 511–519 (2023). https://doi.org/10.1007/s10482-023-01829-w

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