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Abstract

A neutrophilic iron-oxidizing bacterium, strain MIZ01, which was previously isolated from a wetland in Ibaraki, Japan, was taxonomically characterized in detail. Strain MIZ01 was a motile, curved-rod shaped, Gram-stain-negative bacterium. It was able to grow at 10–40 °C (optimally at 30–35 °C) and at pH 5.5–7.0 (optimally at pH 6.0). It grew microaerobically and chemolithoautotrophically using thiosulfate, in addition to ferrous iron, as the sole electron donor. Major cellular fatty acids of strain MIZ01 were C 7/C 6 and C. The complete genome sequence (2.74 Mbp) was determined, showing that its DNA G+C content was 60.0 mol%. Phylogenetic analyses indicated that strain MIZ01 belonged to the family , class , and was closely related to an isolate tentatively named ‘’ ES-1 (98.2 % of 16S rRNA gene sequence similarity). Based on its phenotypic and phylogenetic characteristics, we conclude that strain MIZ01 represents a new genus and species in the family for which we propose the name gen. nov., sp. nov. The type strain is strain MIZ01 (=JCM 39089=DSM 111897).

Funding
This study was supported by the:
  • Japan Society for the Promotion of Science (Award 19H03310)
    • Principle Award Recipient: ShingoKato
  • Japan Society for the Promotion of Science (Award 19H05689)
    • Principle Award Recipient: MoriyaOhkuma
  • Japan Society for the Promotion of Science (Award 19H05679)
    • Principle Award Recipient: MoriyaOhkuma
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/content/journal/ijsem/10.1099/ijsem.0.005347
2022-04-27
2024-05-06
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References

  1. Emerson D, Fleming EJ, McBeth JM. Iron-oxidizing bacteria: An environmental and genomic perspective. Annu Rev Microbiol 2010; 64:561–583 [View Article] [PubMed]
    [Google Scholar]
  2. Kappler A, Bryce C, Mansor M, Lueder U, Byrne JM et al. An evolving view on biogeochemical cycling of iron. Nat Rev Microbiol 2021; 19:360–374 [View Article] [PubMed]
    [Google Scholar]
  3. Ehrenberg CG. Vorläufige mittheilungen über das wirkliche vorkommen fossiler infusorien und ihre grosse verbreitung. Ann Phys Chem 1836; 114:213–227 [View Article]
    [Google Scholar]
  4. Ehrenberg CG. Die Infusionsthierchen Als Vollkommene Organismen: Ein Blick in Das Tiefere Organische Leben Der Natur Leipzig: Verlag von Leopold Voss; 1838
    [Google Scholar]
  5. Vatter AE, Wolfe RS. Electron microscopy of Gallionella ferruginea. J Bacteriol 1956; 72:248–252 [View Article] [PubMed]
    [Google Scholar]
  6. Hallbeck L, Ståhl F, Pedersen K. Phylogeny and phenotypic characterization of the stalk-forming and iron-oxidizing bacterium Gallionella ferruginea. J Gen Microbiol 1993; 139:1531–1535 [View Article] [PubMed]
    [Google Scholar]
  7. Ltters S, Hanert HH. The ultrastructure of chemolithoautotrophic Gallionella ferruginea and Thiobacillus ferrooxidans as revealed by chemical fixation and freeze-etching. Arch Microbiol 1989; 151:245–251 [View Article]
    [Google Scholar]
  8. Lütters-Czekalla S. Lithoautotrophic growth of the iron bacterium Gallionella ferruginea with thiosulfate or sulfide as energy source. Arch Microbiol 1990; 154:417–421 [View Article]
    [Google Scholar]
  9. Hallbeck L, Pedersen K. Culture parameters regulating stalk formation and growth-rate of Gallionella ferruginea. J Gen Microbiol 1990; 136:1675–1680 [View Article]
    [Google Scholar]
  10. Hallbeck L, Pedersen K. Autotrophic and mixotrophic growth of Gallionella ferruginea. J Gen Microbiol 1991; 137:2657–2661 [View Article]
    [Google Scholar]
  11. Sneath PHA, McGowan V, Skerman VBD. Approved lists of bacterial names. Int J Syst Bacteriol 1980; 30:225–420 [View Article]
    [Google Scholar]
  12. Kato S, Krepski S, Chan C, Itoh T, Ohkuma M. Ferriphaselus amnicola gen. nov., sp. nov., a neutrophilic, stalk-forming, iron-oxidizing bacterium isolated from an iron-rich groundwater seep. Int J Syst Evol Microbiol 2014; 64:921–925 [View Article]
    [Google Scholar]
  13. Khalifa A, Nakasuji Y, Saka N, Honjo H, Asakawa S et al. Ferrigenium kumadai gen. nov., sp. nov., a microaerophilic iron-oxidizing bacterium isolated from a paddy field soil. Int J Syst Evol Microbiol 2018; 68:2587–2592 [View Article]
    [Google Scholar]
  14. Krepski ST, Hanson TE, Chan CS. Isolation and characterization of a novel biomineral stalk-forming iron-oxidizing bacterium from a circumneutral groundwater seep. Environ Microbiol 2012; 14:1671–1680 [View Article]
    [Google Scholar]
  15. Kato S, Ohkuma M, Powell DH, Krepski ST, Oshima K et al. Comparative genomic insights into ecophysiology of neutrophilic, microaerophilic iron oxidizing bacteria. Front Microbiol 2015; 6:1265 [View Article]
    [Google Scholar]
  16. Emerson D, Moyer C. Isolation and characterization of novel iron-oxidizing bacteria that grow at circumneutral pH. Appl Environ Microbiol 1997; 63:4784–4792 [View Article]
    [Google Scholar]
  17. Emerson D, Field EK, Chertkov O, Davenport KW, Goodwin L et al. Comparative genomics of freshwater Fe-oxidizing bacteria: Implications for physiology, ecology, and systematics. Front Microbiol 2013; 4:254 [View Article]
    [Google Scholar]
  18. Weiss JV, Rentz JA, Plaia T, Neubauer SC, Merrill-Floyd M et al. Characterization of neutrophilic Fe(II)-oxidizing bacteria isolated from the rhizosphere of wetland plants and description of Ferritrophicum radicicola gen. nov. sp. nov., and Sideroxydans paludicola sp. nov. Geomicrobiol J 2007; 24:559–570 [View Article]
    [Google Scholar]
  19. Lüdecke C, Reiche M, Eusterhues K, Nietzsche S, Küsel K. Acid-tolerant microaerophilic Fe(II)-oxidizing bacteria promote Fe(III)-accumulation in a fen. Environ Microbiol 2010; 12:2814–2825 [View Article]
    [Google Scholar]
  20. Kato S, Ohkuma M. A single bacterium capable of oxidation and reduction of iron at circumneutral pH. Microbiol Spectr 2021; 9:e0016121 [View Article]
    [Google Scholar]
  21. Kato S, Chan C, Itoh T, Ohkuma M. Functional gene analysis of freshwater iron-rich flocs at circumneutral pH and isolation of a stalk-forming microaerophilic iron-oxidizing bacterium. Appl Environ Microbiol 2013; 79:5283–5290 [View Article] [PubMed]
    [Google Scholar]
  22. Kato S, Yuki M, Itoh T, Ohkuma M. Complete genome sequence of Ferriphaselus amnicola strain OYT1, a neutrophilic, stalk-forming, iron-oxidizing bacterium. Microbiol Resour Announc 2018; 7:e00911-18 [View Article] [PubMed]
    [Google Scholar]
  23. Kato S, Itoh T, Ohkuma M. Complete genome sequence of Athalassotoga saccharophila strain NAS-01, a deep-branching thermophilic lineage in the phylum Thermotogae. Microbiol Resour Announc 2020; 9:e00322-20 [View Article] [PubMed]
    [Google Scholar]
  24. Uritskiy GV, DiRuggiero J, Taylor J. MetaWRAP-a flexible pipeline for genome-resolved metagenomic data analysis. Microbiome 2018; 6:158 [View Article] [PubMed]
    [Google Scholar]
  25. De Coster W, D’Hert S, Schultz DT, Cruts M, Van Broeckhoven C. Nanopack: Visualizing and processing long-read sequencing data. Bioinformatics 2018; 34:2666–2669 [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. 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]
  28. 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]
  29. Seemann T. Prokka: Rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  30. Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K. New perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res 2017; 45:D353–D361 [View Article] [PubMed]
    [Google Scholar]
  31. Garber AI, Nealson KH, Okamoto A, McAllister SM, Chan CS et al. FeGenie: A comprehensive tool for the identification of iron genes and iron gene neighborhoods in genome and metagenome assemblies. Front Microbiol 2020; 11:37 [View Article] [PubMed]
    [Google Scholar]
  32. Neukirchen S, Sousa FL. DiSCo: A sequence-based type-specific predictor of dsr-dependent dissimilatory sulphur metabolism in microbial data. Microb Genom 2021; 7: [View Article] [PubMed]
    [Google Scholar]
  33. Barco RA, Emerson D, Sylvan JB, Orcutt BN, Jacobson Meyers ME et al. New insight into microbial iron oxidation as revealed by the proteomic profile of an obligate iron-oxidizing chemolithoautotroph. Appl Environ Microbiol 2015; 81:5927–5937 [View Article] [PubMed]
    [Google Scholar]
  34. Castelle C, Guiral M, Malarte G, Ledgham F, Leroy G et al. A new ironoxidizing/O2-reducing supercomplex spanning both inner and outer membranes, isolated from the extreme acidophile Acidithiobacillus ferrooxidans. J Biol Chem 2008; 283:25803–25811 [View Article] [PubMed]
    [Google Scholar]
  35. Keffer JL, McAllister SM, Garber AI, Hallahan BJ, Sutherland MC et al. Iron oxidation by a fused cytochrome-porin common to diverse iron-oxidizing bacteria. mBio 2021; 12:e0107421 [View Article] [PubMed]
    [Google Scholar]
  36. Liu J, Wang Z, Belchik SM, Edwards MJ, Liu C et al. Identification and characterization of MtoA: A decaheme c-type cytochrome of the neutrophilic Fe(II)-oxidizing bacterium Sideroxydans lithotrophicus ES-1. Front Microbiol 2012; 3:37 [View Article] [PubMed]
    [Google Scholar]
  37. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res 2013; 41:D590–6 [View Article] [PubMed]
    [Google Scholar]
  38. Pruesse E, Peplies J, Glöckner FO. SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012; 28:1823–1829 [View Article] [PubMed]
    [Google Scholar]
  39. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009; 25:1972–1973 [View Article] [PubMed]
    [Google Scholar]
  40. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article] [PubMed]
    [Google Scholar]
  41. Parks DH, Chuvochina M, Rinke C, Mussig AJ, Chaumeil PA et al. GTDB: An ongoing census of bacterial and archaeal diversity through a phylogenetically consistent, rank normalized and complete genome-based taxonomy. Nucleic Acids Res 2022; 50:D785–D794 [View Article] [PubMed]
    [Google Scholar]
  42. 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]
  43. Rodriguez-R LM, Konstantinidis KT. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Preprints 2016; 4:e1900v1 [View Article]
    [Google Scholar]
  44. Qin Q-L, Xie B-B, Zhang X-Y, Chen X-L, Zhou B-C et al. A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 2014; 196:2210–2215 [View Article] [PubMed]
    [Google Scholar]
  45. 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]
  46. Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W et al. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 2014; 12:635–645 [View Article] [PubMed]
    [Google Scholar]
  47. Konstantinidis KT, Tiedje JM. Prokaryotic taxonomy and phylogeny in the genomic era: Advancements and challenges ahead. Curr Opin Microbiol 2007; 10:504–509 [View Article] [PubMed]
    [Google Scholar]
  48. Watanabe T, Khalifa A, Asakawa S. Complete genome sequence of Ferrigenium kumadai An22, a microaerophilic iron-oxidizing bacterium isolated from a paddy field soil. Microbiol Resour Announc 2021; 10:e0034621 [View Article] [PubMed]
    [Google Scholar]
  49. Hallbeck L, Pedersen K. Gallionella. In Brenner D, Krieg N, Staley J. eds Bergey’s Manual of Systematic Bacteriology, 2nd edion. New York: Springer; 2005 pp 880–886
    [Google Scholar]
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