1887

Abstract

Mangrove bacteria largely compose the microbial community of the coastal ecosystem and are directly associated with nutrient cycling. In the present study, 12 Gram-negative and motile strains were isolated from a mangrove wetland in Zhangzhou, China. Pairwise comparisons (based on 16S rRNA gene sequences) and phylogenetic analysis indicated that these 12 strains belong to the genus . The 16S rRNA gene sequence similarities among the 12 strains and their related type strains ranged from 98.8 to 99.8 %, but they still could not be considered as known species. The digital DNA–DNA hybridization (dDDH) and average nucleotide identity (ANI) values between the 12 strains and their related type strains were below the cut-off values (ANI 95–96% and dDDH 70 %) for prokaryotic species delineation. The DNA G+C contents of the present study strains ranged from 44.4 to 53.8 %. The predominant menaquinone present in all strains was MK-7. The present study strains (except FJAT-53532) also contained ubiquinones (Q-8 and Q-7). The polar lipid phosphatidylglycerol and fatty acid iso-C was noticed in all strains. Based on phenotypic, chemotaxonomic, phylogenetic and genomic comparisons, we propose that these 12 strains represent 10 novel species within the genus , with the names sp. nov. (FJAT-53749=GDMCC 1.2398=KCTC 82649), sp. nov. (FJAT-52072=MCCC 1K05363=KCTC 82447), sp. nov. (FJAT-53764=GDMCC 1.2349=KCTC 82648), sp. nov. (FJAT-53870=GDMCC 1.2346= KCTC 82640), sp. nov. (FJAT-53555=GDMCC 1.2344=KCTC 82645), sp. nov. (FJAT-53532=GDMCC 1.2343=KCTC 82644), sp. nov. (FJAT-54031=GDMCC 1.2347=KCTC 82642), sp. nov. (FJAT-53681=GDMCC 1.2345=KCTC 82641), sp. nov. (FJAT-51860=GDMCC 1.2342=KCTC 82650) and sp. nov. (FJAT-51754=GDMCC 1.2341= KCTC 82647).

Funding
This study was supported by the:
  • National Natural Science Foundation of China (Award 42007221)
    • Principle Award Recipient: Guo-HongLiu
  • National Natural Science Foundation of China (Award U21A20295)
    • Principle Award Recipient: Shun-GuiZhou
  • King Saud University (Award RSP2023R205)
    • Principle Award Recipient: HendA. Alwathnani
  • Fujian Academy of Agricultural Sciences (Award GJYS202203)
    • Principle Award Recipient: Guo-HongLiu
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2023-06-16
2024-05-03
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References

  1. MacDonell MT, Colwell RR. Phylogeny of the Vibrionaceae, and recommendation for two new genera, Listonella and Shewanella. Syst Appl Microbiol 1985; 6:171–182 [View Article]
    [Google Scholar]
  2. Bowman JP. Genus XIII. Shewanella MacDonell and Colwell. 355VP (Effective publication: MacDonell and Colwell 1985, 180). In Brenner DJ, Krieg NR, Staley JT, Garrity GM. eds Bergey′s Manual of Systematic BacteriologyThe Proteobacteria, Part B, The Gammaproteobacteria, 2nd edn. vol 2 New York: Springer; 2005 pp 480–491
    [Google Scholar]
  3. Parte AC, Sardà Carbasse J, Meier-Kolthoff JP, Reimer LC, Göker M. List of Prokaryotic names with Standing in Nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol 2020; 70:5607–5612 [View Article] [PubMed]
    [Google Scholar]
  4. Satomi M, Vogel BF, Venkateswaran K, Gram L. Description of Shewanella glacialipiscicola sp. nov. and Shewanella algidipiscicola sp. nov., isolated from marine fish of the Danish Baltic Sea, and proposal that Shewanella affinis is a later heterotypic synonym of Shewanella colwelliana. Int J Syst Evol Microbiol 2007; 57:347–352 [View Article] [PubMed]
    [Google Scholar]
  5. Liu G-H, Zhang Q, Narsing Rao MP, Yang S, Tang R et al. 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 2021; 114:2123–2131 [View Article] [PubMed]
    [Google Scholar]
  6. Zhang Q, Liu G, Narsing Rao MP, Tang R, Yang S et al. Shewanella cyperi sp. nov., a facultative anaerobic bacterium isolated from mangrove sediment. Int J Syst Evol Microbiol 2021; 71:4940 [View Article] [PubMed]
    [Google Scholar]
  7. Lemaire ON, Méjean V, Iobbi-Nivol C. The Shewanella genus: ubiquitous organisms sustaining and preserving aquatic ecosystems. FEMS Microbiol Rev 2020; 44:155–170 [View Article] [PubMed]
    [Google Scholar]
  8. Altun S, Duman M, Ay H, Saticioglu IB. Shewanella oncorhynchi sp. nov., a novel member of the genus Shewanella, isolated from Rainbow Trout (Oncorhynchus mykiss). Int J Syst Evol Microbiol 2022; 72:5460 [View Article]
    [Google Scholar]
  9. Zou L, Huang Y, Long Z, Qiao Y. On-going applications of Shewanella species in microbial electrochemical system for bioenergy, bioremediation and biosensing. World J Microbiol Biotechnol 2019; 35:9 [View Article]
    [Google Scholar]
  10. Rajput VD, Minkina T, Kimber RL, Singh VK, Shende S et al. Insights into the biosynthesis of nanoparticles by the genus Shewanella. Appl Environ Microbiol 2021; 87:e0139021 [View Article] [PubMed]
    [Google Scholar]
  11. Ikeda S, Takamatsu Y, Tsuchiya M, Suga K, Tanaka Y et al. Shewanella oneidensis MR-1 as a bacterial platform for electro-biotechnology. Essays Biochem 2021; 65:355–364 [View Article] [PubMed]
    [Google Scholar]
  12. Tong T, Li R, Wu S, Xie S. The distribution of sediment bacterial community in mangroves across China was governed by geographic location and eutrophication. Mar Pollut Bull 2019; 140:198–203 [View Article] [PubMed]
    [Google Scholar]
  13. Liu G-H, Liu D-Q, Wang P, Chen Q-Q, Che J-M et al. Temperature drives the assembly of Bacillus community in mangrove ecosystem. Sci Total Environ 2022; 846:157496 [View Article]
    [Google Scholar]
  14. Liu Y, Shang X-X, Yi Z-W, Gu L, Zeng R-Y. Shewanella mangrovi sp. nov., an acetaldehyde-degrading bacterium isolated from mangrove sediment. Int J Syst Evol Microbiol 2015; 65:2630–2634 [View Article]
    [Google Scholar]
  15. Martín-Rodríguez AJ, Meier-Kolthoff JP. Whole genome-based taxonomy of Shewanella and Parashewanella. Int J Syst Evol Microbiol 2022; 72: [View Article]
    [Google Scholar]
  16. Narsing Rao MP, Dong Z-Y, Kan Y, Dong L, Li S et al. Description of Paenibacillus tepidiphilus sp. nov., isolated from a tepid spring. Int J Syst Evol Microbiol 2020; 70:1977–1981 [View Article]
    [Google Scholar]
  17. KOVACS N. Identification of Pseudomonas pyocyanea by the oxidase reaction. Nature 1956; 178:703–704 [View Article] [PubMed]
    [Google Scholar]
  18. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017; 67:1613–1617 [View Article] [PubMed]
    [Google Scholar]
  19. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 1994; 22:4673–4680 [View Article]
    [Google Scholar]
  20. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980; 16:111–120 [View Article] [PubMed]
    [Google Scholar]
  21. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article] [PubMed]
    [Google Scholar]
  22. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article] [PubMed]
    [Google Scholar]
  23. Fitch WM. Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 1971; 20:406 [View Article]
    [Google Scholar]
  24. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article] [PubMed]
    [Google Scholar]
  25. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article] [PubMed]
    [Google Scholar]
  26. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article] [PubMed]
    [Google Scholar]
  27. Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010; 11:119 [View Article]
    [Google Scholar]
  28. Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K. KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res 2017; 45:D353–D361 [View Article] [PubMed]
    [Google Scholar]
  29. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:75 [View Article] [PubMed]
    [Google Scholar]
  30. Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997; 25:955–964 [View Article] [PubMed]
    [Google Scholar]
  31. Lagesen K, Hallin P, Rødland EA, Staerfeldt H-H, Rognes T et al. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 2007; 35:3100–3108 [View Article] [PubMed]
    [Google Scholar]
  32. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
    [Google Scholar]
  33. Yoon S-H, Ha S-M, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017; 110:1281–1286 [View Article] [PubMed]
    [Google Scholar]
  34. Meier-Kolthoff JP, Carbasse JS, Peinado-Olarte RL, Göker M. TYGS and LPSN: a database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Res 2022; 50:D801–D807 [View Article] [PubMed]
    [Google Scholar]
  35. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article] [PubMed]
    [Google Scholar]
  36. Price MN, Dehal PS, Arkin AP. FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS One 2010; 5:e9490 [View Article] [PubMed]
    [Google Scholar]
  37. Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 2018; 36:996–1004 [View Article] [PubMed]
    [Google Scholar]
  38. Chaumeil PA, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 2019; 36:1925–1927 [View Article] [PubMed]
    [Google Scholar]
  39. Collins MD, Pirouz T, Goodfellow M, Minnikin DE. Distribution of menaquinones in actinomycetes and corynebacteria. J Gen Microbiol 1977; 100:221–230 [View Article] [PubMed]
    [Google Scholar]
  40. Kroppenstedt RM. Separation of bacterial menaquinones by HPLC using Reverse Phase (RP18) and a silver loaded ion exchanger as stationary phases. J Liq Chromatogr 1982; 5:2359–2367 [View Article]
    [Google Scholar]
  41. Minnikin DE, Collins MD, Goodfellow M. Fatty acid and polar lipid composition in the classification of Cellulomonas, Oerskovia and related taxa. J Appl Bacteriol 1979; 47:87–95 [View Article]
    [Google Scholar]
  42. Collins MD, Jones D. Lipids in the classification and identification of coryneform bacteria containing peptidoglycans based on 2, 4-diaminobutyric acid. J Appl Bacteriol 1980; 48:459–470 [View Article]
    [Google Scholar]
  43. Sasser M. Technical Note 101: Identification of Bacteria by Gas Chromatography of Cellular Fatty Acids Newark DE: MIDI; 1990
    [Google Scholar]
  44. Kim M, Oh HS, Park SC, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014; 64:346–351 [View Article]
    [Google Scholar]
  45. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007; 57:81–91 [View Article] [PubMed]
    [Google Scholar]
  46. Ivanova EP, Flavier S, Christen R. Phylogenetic relationships among marine Alteromonas-like proteobacteria: emended description of the family Alteromonadaceae and proposal of Pseudoalteromonadaceae fam. nov., Colwelliaceae fam. nov., Shewanellaceae fam. nov., Moritellaceae fam. nov., Ferrimonadaceae fam. nov., Idiomarinaceae fam. nov. and Psychromonadaceae fam. nov. Int J Syst Evol Microbiol 2004; 54:1773–1788 [View Article] [PubMed]
    [Google Scholar]
  47. Gao H, Obraztova A, Stewart N, Popa R, Fredrickson JK et al. Shewanella loihica sp. nov., isolated from iron-rich microbial mats in the Pacific Ocean. Int J Syst Evol Microbiol 2006; 56:1911–1916 [View Article] [PubMed]
    [Google Scholar]
  48. Beblawy S, Bursac T, Paquete C, Louro R, Clarke TA et al. Extracellular reduction of solid electron acceptors by Shewanella oneidensis. Mol Microbiol 2018; 109:571–583 [View Article] [PubMed]
    [Google Scholar]
  49. Lemaire ON, Honoré FA, Tempel S, Fortier EM, Leimkühler S et al. Shewanella decolorationis LDS1 chromate resistance. Appl Environ Microbiol 2019; 85:e00777-19 [View Article] [PubMed]
    [Google Scholar]
  50. Shi L, Rosso KM, Clarke TA, Richardson DJ, Zachara JM et al. Molecular underpinnings of Fe(III) oxide reduction by Shewanella oneidensis MR-1. Front Microbiol 2012; 3:50 [View Article] [PubMed]
    [Google Scholar]
  51. Jing X, Wu Y, Shi L, Peacock CL, Ashry NM et al. Outer membrane c -type cytochromes OmcA and MtrC play distinct roles in enhancing the attachment of Shewanella oneidensis MR-1 cells to goethite. Appl Environ Microbiol 2020; 86:e01941–20 [View Article]
    [Google Scholar]
  52. Heidelberg JF, Paulsen IT, Nelson KE, Gaidos EJ, Nelson WC et al. Genome sequence of the dissimilatory metal ion–reducing bacterium Shewanella oneidensis. Nat Biotechnol 2002; 20:1118–1123 [View Article]
    [Google Scholar]
  53. Driscoll ME, Romine MF, Juhn FS, Serres MH, Mccue LA et al. Identification of diverse carbon utilization pathways in Shewanella oneidensis MR-1 via expression profiling. Genome Inform 2007; 18:287–298 [View Article]
    [Google Scholar]
  54. Stine ZE, Altman BJ, Hsieh AL, Gouw AM, Dang CV. Deregulation of the cellular energetics of cancer cells. In McManus LM, Mitchell RN. eds Pathobiology of Human Disease 2014 pp 444–455 [View Article]
    [Google Scholar]
  55. Rodionov DA, Yang C, Li X, Rodionova IA, Wang Y et al. Genomic encyclopedia of sugar utilization pathways in the Shewanella genus. BMC Genomics 2010; 11:494 [View Article] [PubMed]
    [Google Scholar]
  56. Brettar I, Christen R, Höfle MG. 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 2002; 52:2211–2217 [View Article]
    [Google Scholar]
  57. Chen Y, Wang FP. Insights on nitrate respiration by Shewanella. Front Mar Sci 2015; 1:80 [View Article]
    [Google Scholar]
  58. Simpson PJL, Richardson DJ, Codd R. The periplasmic nitrate reductase in Shewanella: the resolution, distribution and functional implications of two NAP isoforms, NapEDABC and NapDAGHB. Microbiology 2010; 156:302–312 [View Article] [PubMed]
    [Google Scholar]
  59. Chen Y, Wang F, Xu J, Mehmood MA, Xiao X. Physiological and evolutionary studies of NAP systems in Shewanella piezotolerans WP3. ISME J 2011; 5:843–855 [View Article] [PubMed]
    [Google Scholar]
  60. Kuypers MMM, Marchant HK, Kartal B. The microbial nitrogen-cycling network. Nat Rev Microbiol 2018; 16:263–276 [View Article] [PubMed]
    [Google Scholar]
  61. Pandey CB, Kumar U, Kaviraj M, Minick KJ, Mishra AK et al. DNRA: a short-circuit in biological N-cycling to conserve nitrogen in terrestrial ecosystems. Sci Total Environ 2020; 738:139710 [View Article] [PubMed]
    [Google Scholar]
  62. Benini S. Carbohydrate-active enzymes: structure, activity, and reaction products. Int J Mol Sci 2020; 21:2727 [View Article] [PubMed]
    [Google Scholar]
  63. Qu W, Lin D, Zhang Z, Di W, Gao B et al. Metagenomics investigation of agarlytic genes and genomes in mangrove sediments in China: a potential repertory for carbohydrate-active enzymes. Front Microbiol 2018; 9:1864 [View Article] [PubMed]
    [Google Scholar]
  64. Nichols CAM, Guezennec J, Bowman JP. Bacterial exopolysaccharides from extreme marine environments with special consideration of the Southern Ocean, sea ice, and deep-sea hydrothermal vents: a review. Mar Biotechnol 2005; 7:253–271 [View Article] [PubMed]
    [Google Scholar]
  65. Colin R, Ni B, Laganenka L, Sourjik V. Multiple functions of flagellar motility and chemotaxis in bacterial physiology. FEMS Microbiol Rev 2021; 45:fuab038 [View Article] [PubMed]
    [Google Scholar]
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