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Abstract

Reductive soil disinfestation (RSD), also known as biological soil disinfestation, is a bioremediation method used to suppress soil-borne plant pathogens by stimulating the activity of indigenous anaerobic bacteria in the soil. An anaerobic bacterial strain (E14) was isolated from an anoxic soil sample subjected to RSD treatment and then comprehensively characterized. Cells of the strain were Gram-stain-positive, curved to sigmoid, and spore-forming rods. Cells were motile with a polar flagellum. Strain E14 grew in peptone–yeast extract broth, indicating that it utilized proteinous compounds. Strain E14 was also saccharolytic and produced acetate, isobutyrate, butyrate, isovalerate and gases (H and CO) as fermentation products. The strain did not decompose any of examined polysaccharides except for starch. The major cellular fatty acids of strain E14 were iso-C and iso-C DMA. The closest relative to strain E14, based on 16S rRNA gene sequences, was SYSU GA15002 (96.2 %) in the . Whole-genome analysis of strain E14 showed that its genome was 4.66 Mb long with a genomic DNA G+C content of 32.5 mol%. The average nucleotide identity (ANIb) between strain E14 and SYSU GA15002 was 69.0 %. The presence of the genes encoding glycolysis and butyrate production via the acetyl–CoA pathway was confirmed through genome analysis. Based on the obtained phylogenetic, genomic and phenotypic data, we propose that strain E14 should be assigned to the genus in the family as sp. nov. The type strain is E14 (=NBRC 115133=DSM 114974).

Funding
This study was supported by the:
  • Ministry of Agriculture, Forestry and Fisheries (Award 27016C)
    • Principle Award Recipient: AtsukoUeki
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2024-06-11
2024-07-15
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References

  1. Ueki A, Tonouchi A, Kaku N, Honma S, Ueki K. Clostridium omnivorum sp. nov., isolated from anoxic soil under the treatment of reductive soil disinfestation Figshare 2024 https://doi.org/10.6084/m9.figshare.25633728.v1
    [Google Scholar]
  2. Strauss SL, Kluepfel DA. Anaerobic soil disinfestation: a chemical-independent approach to pre-plant control of plant pathogens. J Integ Agric 2015; 14:2309–2318 [View Article]
    [Google Scholar]
  3. Blok WJ, Lamers JG, Termorshuizen AJ, Bollen GJ. Control of soilborne plant pathogens by incorporating fresh organic amendments followed by tarping. Phytopathology 2000; 90:253–259 [View Article] [PubMed]
    [Google Scholar]
  4. Lopes EA, Canedo EJ, Gomes VA, Vieira BS, Parreira DF et al. Anaerobic soil disinfestation for the management of soilborne pathogens: a review. Appl Soil Ecol 2022; 174:1044 [View Article]
    [Google Scholar]
  5. Momma N, Kobara Y, Uematsu S, Kita N, Shinmura A. Development of biological soil disinfestations in Japan. Appl Microbiol Biotechnol 2013; 97:3801–3809 [View Article] [PubMed]
    [Google Scholar]
  6. Muramoto J, Shennan C, Baird G, Zavatta M, Koike ST et al. Optimizing anaerobic soil disinfestation for California strawberries. Acta Hortic 2014; 1044:215–220 [View Article]
    [Google Scholar]
  7. Ueki A, Kaku N, Ueki K. Role of anaerobic bacteria in biological soil disinfestation for elimination of soil-borne plant pathogens in agriculture. Appl Microbiol Biotechnol 2018; 102:6309–6318 [View Article] [PubMed]
    [Google Scholar]
  8. Mowlick S, Takehara T, Kaku N, Ueki K, Ueki A. Proliferation of diversified clostridial species during biological soil disinfestation incorporated with plant biomass under various conditions. Appl Microbiol Biotechnol 2013; 97:8365–8379 [View Article] [PubMed]
    [Google Scholar]
  9. Swilling KJ, Shrestha U, Ownley BH, Gwinn KD, Butler DM. Volatile fatty acid concentration, soil pH and soil texture during anaerobic soil conditions affect viability of Athelia (Sclerotium) rolfsii sclerotia. Eur J Plant Pathol 2022; 162:149–161 [View Article]
    [Google Scholar]
  10. Ueki A, Takehara T, Ishioka G, Kaku N, Ueki K. Production of β-1,3-glucanase and chitosanase from clostridial strains isolated from the soil subjected to biological disinfestation. AMB Express 2019; 9:114 [View Article] [PubMed]
    [Google Scholar]
  11. Ueki A, Takehara T, Ishioka G, Kaku N, Ueki K. β-1,3-Glucanase production as an anti-fungal enzyme by phylogenetically different strains of the genus Clostridium isolated from anoxic soil that underwent biological disinfestation. Appl Microbiol Biotechnol 2020; 104:5563–5578 [View Article] [PubMed]
    [Google Scholar]
  12. Ueki A, Tonouchi A, Kaku N, Ueki K. Clostridium fungisolvens sp. nov., a new β-1,3-glucan-decomposing bacterium isolated from anoxic soil subjected to biological soil disinfestation. Int J Syst Evol Microbiol 2021; 71:004761 [View Article]
    [Google Scholar]
  13. Shirane S, Momma N, Usami T, Suzuki C, Hori T et al. Fungicidal activity of caproate produced by Clostridium sp. strain E801, a bacterium isolated from cocopeat medium subjected to anaerobic soil disinfestation.. Agronomy 2023; 13:747 [View Article]
    [Google Scholar]
  14. Lee CG, Kunitomo E, Iida T, Nakaho K, Ohkuma M. Soil prokaryotes are associated with decreasing Fusarium oxysporum density during anaerobic soil disinfestation in the tomato field. Appl Soil Ecol 2020; 155:103632 [View Article]
    [Google Scholar]
  15. Serrano-Pérez P, Rosskopf E, De Santiago A, Rodríguez-Molina MC. Anaerobic soil disinfestation reduces survival and infectivity of Phytophthora nicotianae chlamydospores in pepper. Sci Hort 2017; 215:38–48 [View Article]
    [Google Scholar]
  16. Butler DM, Kokalis-Burelle N, Albano JP, McCollum TG, Muramoto J et al. Anaerobic soil disinfestation (ASD) combined with soil solarization as a methyl bromide alternative: vegetable crop performance and soil nutrient dynamics. Plant Soil 2014; 378:365–381 [View Article]
    [Google Scholar]
  17. Messiha NAS, van Diepeningen AD, Wenneker M, van Beuningen AR, Janse JD et al. Biological Soil Disinfestation (BSD), a new control method for potato brown rot, caused by Ralstonia solanacearum race 3 biovar 2. Eur J Plant Pathol 2007; 117:403–415 [View Article]
    [Google Scholar]
  18. Shrestha U, Dee ME, Ownley BH, Butler DM. Anaerobic soil disinfestation reduces germination and affects colonization of Sclerotium rolfsii sclerotia. Phytopathology 2018; 108:342–351 [View Article] [PubMed]
    [Google Scholar]
  19. 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]
  20. Oren A, Garrity GM. Valid publication of the names of forty-two phyla of prokaryotes. Int J Syst Evol Microbiol 2021; 71:005056 [View Article]
    [Google Scholar]
  21. Holdeman LV, Cato EP, Moore WEC. Anaerobe Laboratory Manual, 4th edn Blacksburg, VA: Virginia Polytechnic Institute and State University; 1977
    [Google Scholar]
  22. Satoh A, Watanabe M, Ueki A, Ueki K. Physiological properties and phylogenetic affiliations of anaerobic bacteria isolated from roots of rice plants cultivated on a paddy field. Anaerobe 2002; 8:233–246 [View Article]
    [Google Scholar]
  23. Akasaka H, Ueki A, Hanada S, Kamagata Y, Ueki K. Propionicimonas paludicola gen. nov., sp. nov., a novel facultatively anaerobic, gram-positive, propionate-producing bacterium isolated from plant residue in irrigated rice-field soil. Int J Syst Evol Microbiol 2003; 53:1991–1998 [View Article] [PubMed]
    [Google Scholar]
  24. Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 1991; 173:697–703 [View Article] [PubMed]
    [Google Scholar]
  25. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25:3389–3402 [View Article] [PubMed]
    [Google Scholar]
  26. 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]
  27. Liu L, Jiao J-Y, Fang B-Z, Lv A-P, Ming Y-Z et al. Isolation of Clostridium from Yunnan-Tibet hot springs and description of Clostridium thermarum sp. nov. with lignocellulosic ethanol production. Syst Appl Microbiol 2020; 43:126104 [View Article] [PubMed]
    [Google Scholar]
  28. Liu C, Huang D, Liu L, Zhang J, Deng Y et al. Clostridium swellfunianum sp. nov., a novel anaerobic bacterium isolated from the pit mud of Chinese Luzhou-flavor liquor production. Antonie van Leeuwenhoek 2014; 106:817–825 [View Article] [PubMed]
    [Google Scholar]
  29. Song L, Dong X. Clostridium amylolyticum sp. nov., isolated from H2-producing UASB granules. Int J Syst Evol Microbiol 2008; 58:2132–2135 [View Article] [PubMed]
    [Google Scholar]
  30. Rainey FA, Hollen BJ, Small A. Bergey’s Manual of Systematic Bacteriology, 2nd edn NewYork: Springer; 2009 pp 738–864
    [Google Scholar]
  31. Honma S, Ueki A, Tonouchi A, Kaku N, Ueki K. Clostridium gelidum sp. nov., a psychrotrophic anaerobic bacterium isolated from rice field soil. Int J Syst Evol Microbiol 2022; 72:005478 [View Article] [PubMed]
    [Google Scholar]
  32. Maio ND, Shaw LP, Hubbard A, George S et al. Comparison of long-read sequencing technologies in the hybrid assembly of complex bacterial genomes. Microb Genom 2017; 3:e000118
    [Google Scholar]
  33. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  34. 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]
  35. Yoon SH, Ha SM, 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]
  36. 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]
  37. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M et al. Versatile and open software for comparing large genomes. Genome Biol 2004; 5:R12 [View Article] [PubMed]
    [Google Scholar]
  38. 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]
  39. 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]
  40. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article] [PubMed]
    [Google Scholar]
  41. 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] [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. Na SI, Kim YO, Yoon SH, Ha SM, Baek I et al. UBCG: Up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J Microbiol 2018; 56:280–285 [View Article] [PubMed]
    [Google Scholar]
  44. 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]
  45. Blenden DC, Goldberg HS. Silver impregnation stain for Leptospira and flagella. J Bacteriol 1965; 89:899–900 [View Article] [PubMed]
    [Google Scholar]
  46. Miller LT. Single derivatization method for routine analysis of bacterial whole-cell fatty acid methyl esters, including hydroxyl acids. J Clin Microbiol 1982; 16:584–586 [View Article] [PubMed]
    [Google Scholar]
  47. Komagata K, Suzuki K. Lipid and cell-wall analysis in bacterial systematics. Methods Microbiol 1987; 19:161–207
    [Google Scholar]
  48. Vital M, Howe AC, Tiedje JM. Revealing the bacterial butyrate synthesis pathways by analyzing (meta)genomic data. mBio 2014; 5:e00889–14 [View Article] [PubMed]
    [Google Scholar]
  49. Hiron A, Borezée-Durant E, Piard J-C, Juillard V. Only one of four oligopeptide transport systems mediates nitrogen nutrition in Staphylococcus aureus. J Bacteriol 2007; 189:5119–5129 [View Article] [PubMed]
    [Google Scholar]
  50. Slamti L, Lereclus D. The oligopeptide ABC-importers are essential communication channels in Gram-positive bacteria. Res Microbiol 2019; 170:338–344 [View Article] [PubMed]
    [Google Scholar]
  51. Hutson S. Structure and function of branched chain aminotransferases. Prog Nucleic Acid Res Mol Biol 2001; 70:175–206 [View Article] [PubMed]
    [Google Scholar]
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