1887

Abstract

Forty-eight strains were isolated from soils and sediments in Japan. Among them, six representative strains, designated W79, W786, Red222, Red802, Red803, and Red804, were subjected to the taxonomic classification. These six strains are Gram-stain-negative, non-spore-forming, rod-shaped, and facultative anaerobic bacterium that can reduce ferric iron. Phylogenetic and phylogenomic trees based on 16S rRNA genes and multiple single-copy gene sequences showed that strains Red222, Red802, Red803, and Red804 formed a cluster with the type strains of species, but strains W79 and W786 created an independent cluster from any other type strains. The former four strains shared 97.95–99.08% similarities of 16S rRNA gene sequence with the type strains of the genus , whereas the latter two strains 94.86–95.49% similarities. The average amino acid identity of strains W79 and W786 were <63 % to any other type strains, which were below the genus delineation thresholds. Moreover, colonies of these two strains were white, while those of the other four isolated strains were reddish-yellow as well as the type strain H-5. Although the known type strains of species have been reported to be non-motile, five strains (W79, W786, Red222, Red803, and Red804) except for strain Red802 displayed motility. Furthermore, multiple genomic, phylogenetic, and phenotypic features supported the discrimination between these isolated strains. Based on the study evidence, we propose these six isolates as novel members within the ///, comprising two novel species of a novel genus, gen. nov., sp. nov., and sp. nov., and four novel species of the genus sp. nov., sp. nov., sp. nov., and sp. nov.

Funding
This study was supported by the:
  • Japan Society for the Promotion of Science (Award JP20K15423)
    • Principle Award Recipient: YokoMasuda
  • Japan Society for the Promotion of Science (Award JP20H05679)
    • Principle Award Recipient: HideomiItoh
  • Japan Society for the Promotion of Science (Award JP20H00409)
    • Principle Award Recipient: HideomiItoh
  • The Canon Foundation
    • Principle Award Recipient: HideomiItoh
  • Institute for Fermentation, Osaka (Award G-2021-1-028)
    • Principle Award Recipient: HideomiItoh
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/content/journal/ijsem/10.1099/ijsem.0.006073
2023-09-06
2024-04-27
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References

  1. Delgado-Baquerizo M, Oliverio AM, Brewer TE, Benavent-González A, Eldridge DJ et al. A global atlas of the dominant bacteria found in soil. Science 2018; 359:320–325 [View Article] [PubMed]
    [Google Scholar]
  2. Sunagawa S, Coelho LP, Chaffron S, Kultima JR, Labadie K et al. Structure and function of the global ocean microbiome. Science 2015; 348:1261359 [View Article] [PubMed]
    [Google Scholar]
  3. Kalam S, Basu A, Ahmad I, Sayyed RZ, El-Enshasy HA et al. Recent understanding of soil Acidobacteria and their ecological significance: a critical review. Front Microbiol 2020; 11:580024 [View Article] [PubMed]
    [Google Scholar]
  4. Dedysh SN, Yilmaz P. Refining the taxonomic structure of the phylum Acidobacteria. Int J Syst Evol Microbiol 2018; 68:3796–3806 [View Article] [PubMed]
    [Google Scholar]
  5. Liesack W, Bak F, Kreft JU, Stackebrandt E. Holophaga foetida gen. nov., sp. nov., a new, homoacetogenic bacterium degrading methoxylated aromatic compounds. Arch Microbiol 1994; 162:85–90 [View Article] [PubMed]
    [Google Scholar]
  6. Coates JD, Ellis DJ, Gaw CV, Lovley DR. Geothrix fermentans gen. nov., sp. nov., a novel Fe(III)-reducing bacterium from a hydrocarbon-contaminated aquifer. Int J Syst Evol Microbiol 1999; 49:1615–1622 [View Article]
    [Google Scholar]
  7. Klueglein N, Lösekann-Behrens T, Obst M, Behrens S, Appel E et al. Magnetite formation by the novel Fe(III)-reducing Geothrix fermentans strain HradG1 isolated from a hydrocarbon-contaminated sediment with increased magnetic susceptibility. Geomicrobiology J 2013; 30:863–873 [View Article]
    [Google Scholar]
  8. Han S, Tang R, Yang S, Xie C-J, Narsing Rao MP et al. Two ferric-reducing bacteria Geothrix terrae sp. nov. and Geothrix alkalitolerans sp. nov., isolated from paddy soil. Arch Microbiol 2022; 204:12 [View Article]
    [Google Scholar]
  9. Han S, Tang R, Yang S, Xie C-J, Narsing Rao MP et al. Geothrix oryzisoli sp. nov., a ferric iron-reducing bacterium isolated from paddy soil. Antonie van Leeuwenhoek 2023; 116:477–486 [View Article] [PubMed]
    [Google Scholar]
  10. Han S, Yang S, Tang R, Xie C-J, Liu G-H et al. Geothrix fuzhouensis sp. nov. and Geothrix paludis sp. nov., two novel Fe(III)-reducing bacteria isolated from paddy soil. Int J Syst Evol Microbiol 2023; 73: [View Article]
    [Google Scholar]
  11. Berg JS, Jézéquel D, Duverger A, Lamy D, Laberty-Robert C et al. Microbial diversity involved in iron and cryptic sulfur cycling in the ferruginous, low-sulfate waters of Lake Pavin. PLoS One 2019; 14:e0212787 [View Article] [PubMed]
    [Google Scholar]
  12. Ding L-J, Su J-Q, Xu H-J, Jia Z-J, Zhu Y-G. Long-term nitrogen fertilization of paddy soil shifts iron-reducing microbial community revealed by RNA-(13)C-acetate probing coupled with pyrosequencing. ISME J 2015; 9:721–734 [View Article] [PubMed]
    [Google Scholar]
  13. Chen D, Feng Q, Li W, Song Y, Zhao C. Effects of acid drainage from abandoned coal mines on the microbial community of Shandi river sediment, Shanxi province. Int J Coal Sci Technol 2021; 8:756–766 [View Article]
    [Google Scholar]
  14. Yang L, Jiang M, Zou Y, Qin L, Chen Y. Geographical distribution of iron redox cycling bacterial community in peatlands: distinct assemble mechanism across environmental gradient. Front Microbiol 2021; 12:674411 [View Article] [PubMed]
    [Google Scholar]
  15. Xu Z, Masuda Y, Itoh H, Ushijima N, Shiratori Y et al. Geomonas oryzae gen. nov., sp. nov., Geomonas edaphica sp. nov., Geomonas ferrireducens sp. nov., Geomonas terrae sp. nov., four ferric-reducing bacteria isolated from paddy doil, and reclassification of three species of the genus Geobacter as members of the genus Geomonas gen. nov. Front Microbiol 2019; 10:2201 [View Article]
    [Google Scholar]
  16. Xu Z, Masuda Y, Hayakawa C, Ushijima N, Kawano K et al. Description of three novel members in the family Geobacteraceae, Oryzomonas japonicum gen. nov., sp. nov., Oryzomonas sagensis sp. nov., and Oryzomonas ruber sp. nov. Microorganisms 2020; 8:634 [View Article]
    [Google Scholar]
  17. Xu Z, Masuda Y, Wang X, Ushijima N, Shiratori Y et al. Genome-based taxonomic rearrangement of the order Geobacterales including the description of Geomonas azotofigens sp. nov. and Geomonas diazotrophica sp. nov. Front Microbiol 2021; 12:2715 [View Article]
    [Google Scholar]
  18. Zhang Z, Xu Z, Masuda Y, Wang X, Ushijima N et al. Geomesophilobacter sediminis gen. nov., sp. nov., Geomonas propionica sp. nov. and Geomonas anaerohicana sp. nov., three novel members in the family Geobacterecace isolated from river sediment and paddy soil. Syst Appl Microbiol 2021; 44:126233 [View Article] [PubMed]
    [Google Scholar]
  19. Itoh H, Xu Z, Masuda Y, Ushijima N, Hayakawa C et al. Geomonas silvestris sp. nov., Geomonas paludis sp. nov. and Geomonas limicola sp. nov., isolated from terrestrial environments, and emended description of the genus Geomonas. Int J Syst Evol Microbiol 2021; 71: [View Article] [PubMed]
    [Google Scholar]
  20. Itoh H, Xu Z, Mise K, Masuda Y, Ushijima N et al. Anaeromyxobacter oryzae sp. nov., Anaeromyxobacter diazotrophicus sp. nov. and Anaeromyxobacter paludicola sp. nov., isolated from paddy soils. Int J Syst Evol Microbiol 2022; 72:10 [View Article] [PubMed]
    [Google Scholar]
  21. Masuda Y, Yamanaka H, Xu Z-X, Shiratori Y, Aono T et al. Diazotrophic Anaeromyxobacter isolates from soils. Appl Environ Microbiol 2020; 86:e00956–00920 [View Article]
    [Google Scholar]
  22. Itoh H, Navarro R, Takeshita K, Tago K, Hayatsu M et al. Bacterial population succession and adaptation affected by insecticide application and soil spraying history. Front Microbiol 2014; 5:457 [View Article] [PubMed]
    [Google Scholar]
  23. Fukatsu T, Nikoh N. Two intracellular symbiotic bacteria from the mulberry psyllid Anomoneura mori (Insecta, Homoptera). Appl Environ Microbiol 1998; 64:3599–3606 [View Article] [PubMed]
    [Google Scholar]
  24. Kawano K, Ushijima N, Kihara M, Itoh H. Patiriisocius marinistellae gen. nov., sp. nov., isolated from the starfish Patiria pectinifera, and reclassification of Ulvibacter marinus as a member of the genus Patiriisocius comb. nov. Int J Syst Evol Microbiol 2020; 70:4119–4129 [View Article]
    [Google Scholar]
  25. Madeira F, Pearce M, Tivey ARN, Basutkar P, Lee J et al. Search and sequence analysis tools services from EMBL-EBI in 2022. Nucleic Acids Res 2022; 50:W276–W279 [View Article] [PubMed]
    [Google Scholar]
  26. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 1993; 10:512–526 [View Article] [PubMed]
    [Google Scholar]
  27. Tamura K, Stecher G, Kumar S. MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 2021; 38:3022–3027 [View Article] [PubMed]
    [Google Scholar]
  28. Kim M, Oh H-S, Park S-C, 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] [PubMed]
    [Google Scholar]
  29. Itoh H, Kawano K, Kihara M. Draft genome sequence of Agarivorans sp. strain Toyoura001, isolated from an Abalone Gut. Microbiol Resour Announc 2019; 8:e00169-19 [View Article] [PubMed]
    [Google Scholar]
  30. 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]
  31. 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]
  32. Tanizawa Y, Fujisawa T, Nakamura Y. DFAST: a flexible prokaryotic genome annotation pipeline for faster genome publication. Bioinformatics 2018; 34:1037–1039 [View Article] [PubMed]
    [Google Scholar]
  33. Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 2016; 428:726–731 [View Article] [PubMed]
    [Google Scholar]
  34. 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]
  35. 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]
  36. Rodriguez-R LM, Konstantinidis KT. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ 2016 [View Article]
    [Google Scholar]
  37. Hug LA, Baker BJ, Anantharaman K, Brown CT, Probst AJ et al. A new view of the tree of life. Nat Microbiol 2016; 1:16048 [View Article]
    [Google Scholar]
  38. Parks DH, Chuvochina M, Chaumeil P-A, Rinke C, Mussig AJ et al. A complete domain-to-species taxonomy for Bacteria and Archaea. Nat Biotechnol 2020; 38:1079–1086 [View Article]
    [Google Scholar]
  39. Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 2019; 35:4453–4455 [View Article] [PubMed]
    [Google Scholar]
  40. Dalcin Martins P, Frank J, Mitchell H, Markillie LM, Wilkins MJ. Wetland sediments host diverse microbial taxa capable of cycling alcohols. Appl Environ Microbiol 2019; 85:e00189-19 [View Article] [PubMed]
    [Google Scholar]
  41. Preisig O, Zufferey R, Thöny-Meyer L, Appleby CA, Hennecke H. A high-affinity cbb3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum. J Bacteriol 1996; 178:1532–1538 [View Article] [PubMed]
    [Google Scholar]
  42. Kim S-J, Park S-J, Cha I-T, Min D, Kim J-S et al. Metabolic versatility of toluene-degrading, iron-reducing bacteria in tidal flat sediment, characterized by stable isotope probing-based metagenomic analysis. Environ Microbiol 2014; 16:189–204 [View Article] [PubMed]
    [Google Scholar]
  43. Kielak AM, Barreto CC, Kowalchuk GA, van Veen JA, Kuramae EE. The ecology of Acidobacteria: moving beyond genes and genomes. Front Microbiol 2016; 7:744 [View Article] [PubMed]
    [Google Scholar]
  44. Skennerton CT, Ward LM, Michel A, Metcalfe K, Valiente C et al. Genomic reconstruction of an uncultured hydrothermal vent gammaproteobacterial methanotroph (family Methylothermaceae) indicates multiple adaptations to oxygen limitation. Front Microbiol 2015; 6:1425 [View Article] [PubMed]
    [Google Scholar]
  45. Orata FD, Meier-Kolthoff JP, Sauvageau D, Stein LY. Phylogenomic analysis of the gammaproteobacterial methanotrophs (Order Methylococcales) calls for the reclassification of members at the genus and species levels. Front Microbiol 2018; 9:3162 [View Article] [PubMed]
    [Google Scholar]
  46. Nicholson AC, Gulvik CA, Whitney AM, Humrighouse BW, Bell ME et al. Division of the genus Chryseobacterium: observation of discontinuities in amino acid identity values, a possible consequence of major extinction events, guides transfer of nine species to the genus Epilithonimonas, eleven species to the genus Kaistella, and three species to the genus Halpernia gen. nov., with description of Kaistella daneshvariae sp. nov. and Epilithonimonas vandammei sp. nov. derived from clinical specimens. Int J Syst Evol Microbiol 2020; 70:4432–4450 [View Article]
    [Google Scholar]
  47. Sasser M. Identification of bacteria by gas chromatography of cellular fatty acids. In MIDI Technical Note vol 101 Newark, DE: MIDI inc; 1990
    [Google Scholar]
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