1887

Abstract

Two bacterial strains, SP1S1-4 and SP2S1-2, were isolated from sediment samples collected in the Stockholm archipelago in November 2021. Following whole-genome sequencing, these strains were identified as tentatively belonging to two novel genospecies, based on digital DNA–DNA hybridization, as implemented in the Type Strain Genome Server. , and were, in this order and within a narrow genomic relatedness range, their closest genotypic relatives. Additional sampling and sequencing efforts led to the retrieval of distinct isolates that were monophyletic with SP1S1-4 and SP2S1-2, respectively, based on phylogenomic analysis of whole-genome sequences. Comparative analyses of genome sequence data, which included -based average nucleotide identity, core genome-based and core proteome-based phylogenomics, in addition to MALDI-TOF MS-based protein profiling, confirmed the distinctness of the putative novel genospecies with respect to their closest genotypic relatives. A comprehensive phenotypic characterisation of SP1S1-4 and SP2S1-2 revealed only minor differences with respect to the type strains of , and . Based on the collective phylogenomic, proteomic, and phenotypic evidence presented here, we describe two novel genospecies within the genus , for which the names sp. nov. and sp. nov. are proposed. The type strains are, respectively, SP2S1-2 (=CCUG 76457=CECT 30688), with a draft genome sequence of 5 041 805 bp and a G+C content of 46.3 mol%, and SP1S1-4 (=CCUG 76453=CECT 30684), with a draft genome sequence of 4 920147 bp and a G+C content of 46.0 mol%. Our findings suggest the existence of a species complex formed by the species , , sp. nov., and sp. nov., with falling in the periphery, where distinct genomic species clusters could be identified. However, this does not exclude the possibility of a continuum of genomic diversity within this sedimental ecosystem, as discussed herein with additional sequenced isolates.

Funding
This study was supported by the:
  • ERA-NET AquaticPollutants Joint Translational Call (Award PARRTAE (Ref. ID. 351))
    • Principle Award Recipient: SjölingÅsa
  • Karolinska Institutet (Award Junior Investigator Award for SDG-related research Ref. 2022-00021)
    • Principle Award Recipient: AlbertoJ Martin-Rodriguez
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2024-08-16
2024-11-05
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References

  1. 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]
  2. Martín-Rodríguez AJ. Respiration-induced biofilm formation as a driver for bacterial niche colonization. Trends Microbiol 2023; 31:120–134 [View Article] [PubMed]
    [Google Scholar]
  3. Fredrickson JK, Romine MF, Beliaev AS, Auchtung JM, Driscoll ME et al. Towards environmental systems biology of Shewanella. . Nat Rev Microbiol 2008; 6:592–603 [View Article] [PubMed]
    [Google Scholar]
  4. Martín-Rodríguez AJ, Reyes-Darias JA, Martín-Mora D, González JM, Krell T et al. Reduction of alternative electron acceptors drives biofilm formation in Shewanella algae. NPJ Biofilms Microbiomes 2021; 7:9 [View Article] [PubMed]
    [Google Scholar]
  5. 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]
  6. Wayne LG. International committee on systematic bacteriology: announcement of the report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Zentralbl Bakteriol Mikrobiol Hyg A 1988; 268:433–434 [View Article] [PubMed]
    [Google Scholar]
  7. 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]
  8. 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]
  9. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 2009; 106:19126–19131 [View Article] [PubMed]
    [Google Scholar]
  10. Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun 2018; 9:5114 [View Article] [PubMed]
    [Google Scholar]
  11. Murray CS, Gao Y, Wu M. Re-evaluating the evidence for a universal genetic boundary among microbial species. Nat Commun 2021; 12:4059 [View Article] [PubMed]
    [Google Scholar]
  12. Rodriguez-R LM, Jain C, Conrad RE, Aluru S, Konstantinidis KT. Reply to: “re-evaluating the evidence for a universal genetic boundary among microbial species.”. Nat Commun 2021; 12:4060 [View Article] [PubMed]
    [Google Scholar]
  13. Martín-Rodríguez AJ, Thorell K, Joffré E, Jensie-Markopoulos S, Moore ERB et al. Shewanella septentrionalis sp. nov. and Shewanella holmiensis sp. nov., isolated from Baltic Sea water and sediments. Int J Syst Evol Microbiol 2023; 73: [View Article] [PubMed]
    [Google Scholar]
  14. Näslund J, Nascimento FJ, Gunnarsson JS. Meiofauna reduces bacterial mineralization of naphthalene in marine sediment. ISME J 2010; 4:1421–1430 [View Article] [PubMed]
    [Google Scholar]
  15. Petit RA, Read TD. Bactopia: a flexible pipeline for complete analysis of bacterial genomes. mSystems 2020; 5:e00190-20 [View Article]
    [Google Scholar]
  16. Jaén-Luchoro D, Gonzales-Siles L, Karlsson R, Svensson-Stadler L, Molin K et al. Corynebacterium sanguinis sp. nov., a clinical and environmental associated corynebacterium. Syst Appl Microbiol 2020; 43:126039 [View Article] [PubMed]
    [Google Scholar]
  17. Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 2019; 10:2182 [View Article] [PubMed]
    [Google Scholar]
  18. 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]
  19. Lefort V, Desper R, Gascuel O. FastME 2.0: a comprehensive, accurate, and fast distance-based phylogeny inference program. Mol Biol Evol 2015; 32:2798–2800 [View Article] [PubMed]
    [Google Scholar]
  20. Farris JS. Estimating phylogenetic trees from distance matrices. Am Nat 1972; 106:645–667 [View Article]
    [Google Scholar]
  21. Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 2016; 32:929–931 [View Article] [PubMed]
    [Google Scholar]
  22. Tonkin-Hill G, MacAlasdair N, Ruis C, Weimann A, Horesh G et al. Producing polished prokaryotic pangenomes with the Panaroo pipeline. Genome Biol 2020; 21:180 [View Article] [PubMed]
    [Google Scholar]
  23. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  24. 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]
  25. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 2021; 49:W293–W296 [View Article] [PubMed]
    [Google Scholar]
  26. Kim D, Park S, Chun J. Introducing EzAAI: a pipeline for high throughput calculations of prokaryotic average amino acid identity. J Microbiol 2021; 59:476–480 [View Article] [PubMed]
    [Google Scholar]
  27. Eren AM, Esen ÖC, Quince C, Vineis JH, Morrison HG et al. Anvi'o: an advanced analysis and visualization platform for 'omics data. PeerJ 2015; 3:e1319 [View Article] [PubMed]
    [Google Scholar]
  28. 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] [PubMed]
    [Google Scholar]
  29. Tatusov RL, Galperin MY, Natale DA, Koonin EV. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 2000; 28:33–36 [View Article] [PubMed]
    [Google Scholar]
  30. Galperin MY, Wolf YI, Makarova KS, Vera Alvarez R, Landsman D et al. COG database update: focus on microbial diversity, model organisms, and widespread pathogens. Nucleic Acids Res 2021; 49:D274–D281 [View Article] [PubMed]
    [Google Scholar]
  31. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods 2015; 12:59–60 [View Article] [PubMed]
    [Google Scholar]
  32. van Dongen S, Abreu-Goodger C. Using MCL to extract clusters from networks. Methods Mol Biol 2012; 804:281–295 [View Article] [PubMed]
    [Google Scholar]
  33. Pritchard L, Glover RH, Humphris S, Elphinstone JG, Toth IK. Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens. Anal Methods 2016; 8:12–24 [View Article]
    [Google Scholar]
  34. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article] [PubMed]
    [Google Scholar]
  35. Shu LJ, Yang YL. Bacillus classification based on matrix-assisted laser desorption ionization time-of-flight mass spectrometry-effects of culture conditions. Sci Rep 2017; 7:15546 [View Article] [PubMed]
    [Google Scholar]
  36. Linkert M, Rueden CT, Allan C, Burel J-M, Moore W et al. Metadata matters: access to image data in the real world. J Cell Biol 2010; 189:777–782 [View Article] [PubMed]
    [Google Scholar]
  37. Karlsson OM, Jonsson PO, Lindgren D, Malmaeus JM, Stehn A. Indications of recovery from hypoxia in the inner Stockholm archipelago. Ambio 2010; 39:486–495 [View Article] [PubMed]
    [Google Scholar]
  38. van Helmond N, Lougheed BC, Vollebregt A, Peterse F, Fontorbe G et al. Recovery from multi-millennial natural coastal hypoxia in the Stockholm Archipelago, Baltic Sea, terminated by modern human activity. Limnol Oceanogr 2020; 65:3085–3097 [View Article] [PubMed]
    [Google Scholar]
  39. Palmer M, Steenkamp ET, Blom J, Hedlund BP, Venter SN. All ANIs are not created equal: implications for prokaryotic species boundaries and integration of ANIs into polyphasic taxonomy. Int J Syst Evol Microbiol 2020; 70:2937–2948 [View Article] [PubMed]
    [Google Scholar]
  40. Jensen A, Scholz CFP, Kilian M. Re-evaluation of the taxonomy of the Mitis group of the genus Streptococcus based on whole genome phylogenetic analyses, and proposed reclassification of Streptococcus dentisani as Streptococcus oralis subsp. dentisani comb. nov., Streptococcus tigurinus as Streptococcus oralis subsp. tigurinus comb. nov., and Streptococcus oligofermentans as a later synonym of Streptococcus cristatus. Int J Syst Evol Microbiol 2016; 66:4803–4820 [View Article] [PubMed]
    [Google Scholar]
  41. Hu S, Li K, Zhang Y, Wang Y, Fu L et al. New insights into the threshold values of multi-locus sequence analysis, average nucleotide identity and digital DNA-DNA hybridization in delineating Streptomyces species. Front Microbiol 2022; 13:910277 [View Article] [PubMed]
    [Google Scholar]
  42. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [View Article] [PubMed]
    [Google Scholar]
  43. Riesco R, Trujillo ME. Update on the proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2024; 74:006300 [View Article] [PubMed]
    [Google Scholar]
  44. Vos M, Hesselman MC, Te Beek TA, van Passel MWJ, Eyre-Walker A. Rates of lateral gene transfer in prokaryotes: high but why?. Trends Microbiol 2015; 23:598–605 [View Article] [PubMed]
    [Google Scholar]
  45. Martín-Rodríguez AJ, Suárez-Mesa A, Artiles-Campelo F, Römling U, Hernández M. Multilocus sequence typing of Shewanella algae isolates identifies disease-causing Shewanella chilikensis strain 6I4. FEMS Microbiol Ecol 2019; 95: [View Article] [PubMed]
    [Google Scholar]
  46. Thorell K, Meier-Kolthoff JP, Sjöling Å, Martín-Rodríguez AJ. Whole-genome sequencing redefines Shewanella taxonomy. Front Microbiol 2019; 10:1861 [View Article]
    [Google Scholar]
  47. Küpfer M, Kuhnert P, Korczak BM, Peduzzi R, Demarta A. Genetic relationships of Aeromonas strains inferred from 16S rRNA, gyrB and rpoB gene sequences. Int J Syst Evol Microbiol 2006; 56:2743–2751 [View Article] [PubMed]
    [Google Scholar]
  48. Fernández-Bravo A, Figueras MJ. An update on the genus aeromonas: taxonomy, epidemiology, and pathogenicity. Microorganisms 2020; 8:129 [View Article]
    [Google Scholar]
  49. Thompson CC, Chimetto L, Edwards RA, Swings J, Stackebrandt E et al. Microbial genomic taxonomy. BMC Genomics 2013; 14:913 [View Article] [PubMed]
    [Google Scholar]
  50. Bowmann JP. Shewanella. In Whitman WB. eds Bergey’s Manual of Systematics of Archaea and Bacteria John Wiley & Sons; 2015
    [Google Scholar]
  51. Schloter M, Lebuhn M, Heulin T, Hartmann A. Ecology and evolution of bacterial microdiversity. FEMS Microbiol Rev 2000; 24:647–660 [View Article] [PubMed]
    [Google Scholar]
  52. Satomi M, Vogel BF, Gram L, Venkateswaran K. Shewanella hafniensis sp. nov. and Shewanella morhuae sp. nov., isolated from marine fish of the Baltic Sea. Int J Syst Evol Microbiol 2006; 56:243–249 [View Article] [PubMed]
    [Google Scholar]
  53. Fraser C, Hanage WP, Spratt BG. Recombination and the nature of bacterial speciation. Science 2007; 315:476–480 [View Article] [PubMed]
    [Google Scholar]
  54. Wiedenbeck J, Cohan FM. Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. FEMS Microbiol Rev 2011; 35:957–976 [View Article] [PubMed]
    [Google Scholar]
  55. Caro-Quintero A, Deng J, Auchtung J, Brettar I, Höfle MG et al. Unprecedented levels of horizontal gene transfer among spatially co-occurring Shewanella bacteria from the Baltic Sea. ISME J 2011; 5:131–140 [View Article] [PubMed]
    [Google Scholar]
  56. Konstantinidis KT, Ramette A, Tiedje JM. The bacterial species definition in the genomic era. Philos Trans R Soc Lond B Biol Sci 2006; 361:1929–1940 [View Article] [PubMed]
    [Google Scholar]
  57. Crits-Christoph A, Olm MR, Diamond S, Bouma-Gregson K, Banfield JF. Soil bacterial populations are shaped by recombination and gene-specific selection across a grassland meadow. ISME J 2020; 14:1834–1846 [View Article] [PubMed]
    [Google Scholar]
  58. Dong X, Peng Y, Wang M, Woods L, Wu W et al. Evolutionary ecology of microbial populations inhabiting deep sea sediments associated with cold seeps. Nat Commun 2023; 14:1127 [View Article]
    [Google Scholar]
  59. Doolittle WF, Papke RT. Genomics and the bacterial species problem. Genome Biol 2006; 7:116 [View Article] [PubMed]
    [Google Scholar]
  60. Achtman M, Wagner M. Microbial diversity and the genetic nature of microbial species. Nat Rev Microbiol 2008; 6:431–440 [View Article] [PubMed]
    [Google Scholar]
  61. 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]
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