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Abstract

Biological soil disinfestation (BSD) or reductive soil disinfestation (RSD) is a bioremediation method used to suppress or eliminate soil-borne plant pathogens by stimulating activities of indigenous anaerobic bacteria of the soil. An anaerobic bacterial strain (TW1) was isolated from an anoxic soil sample subjected to the BSD treatment and comprehensively characterized. Cells of the strain were Gram-stain-positive, slightly curved and motile rods producing terminal spores. The strain was aerotolerant. Strain TW1 was saccharolytic and produced acetate, butyrate, H and CO as fermentation end products. Strain TW1 decomposed β-1,3-glucan (curdlan and laminarin) and degraded mycelial cells of an ascomycete plant pathogen. Major cellular fatty acids of strain TW1 were C, C dimethylacetal (DMA), C aldehyde and C DMA. Strain TW1 made a group on the phylogenetic tree constructed based on 16S rRNA gene sequences with species such as (96.3 %) and (96.0 %). Whole genome analysis of strain TW1 showed that the total length of the genome was 5.28 Mb with the DNA G+C content of 31.3 mol%. The average nucleotide identity (ANIb) between strain TW1 and was 71.2 %. Presence of the genes encoding laminarinase or GH16 β-glucosidase was confirmed from the genome analysis of strain TW1. Based on the genomic, phylogenetic and phenotypic properties obtained, we propose strain TW1 should be assigned in the genus in the family as sp. nov. The type strain TW1 (=NBRC 112097=DSM 110791).

Funding
This study was supported by the:
  • Ministry of Agriculture, Forestry and Fisheries (Award 27016C)
    • Principle Award Recipient: AtsukoUeki
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2021-03-18
2024-04-19
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References

  1. 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]
  2. Goud JKC, Termorshuizen AJ, Blok WJ, van Bruggen AHC. Long-term effect of biological soil disinfestation on Verticillium wilt. Plant Dis 2004; 88:688–694 [View Article][PubMed]
    [Google Scholar]
  3. 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]
  4. 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]
  5. Strauss SL, Kluepfel DA. Anaerobic soil disinfestation: a chemical-independent approach to pre-plant control of plant pathogens. J Integr Agric 2015; 14:2309–2318 [View Article]
    [Google Scholar]
  6. 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]
  7. Browne G, Ott N, Poret-Peterson A, Gouran H, Lampinen B. Efficacy of anaerobic soil disinfestation for control of prunus replant disease. Plant Dis 2018; 102:209–219 [View Article][PubMed]
    [Google Scholar]
  8. Mazzola M, Muramoto J, Shennan C. Anaerobic disinfestation induced changes to the soil microbiome, disease incidence and strawberry fruit yields in California field trials. Appl Soil Ecol 2018; 127:74–86 [View Article]
    [Google Scholar]
  9. 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]
  10. 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]
  11. 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]
  12. Mowlick S, Hirota K, Takehara T, Kaku N, Ueki K et al. Development of anaerobic bacterial community consisted of diverse clostridial species during biological soil disinfestation amended with plant biomass. Soil Sci Plant Nutr 2012; 58:273–287 [View Article]
    [Google Scholar]
  13. Mowlick S, Inoue T, Takehara T, Kaku N, Ueki K et al. Changes and recovery of soil bacterial communities influenced by biological soil disinfestation as compared with chloropicrin-treatment. AMB Express 2013; 3:46 [View Article][PubMed]
    [Google Scholar]
  14. 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]
  15. 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 Expr 2019; 9:114 [View Article]
    [Google Scholar]
  16. 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]
  17. Rainey FA, Hollen BJ, Small A. Genus I. Clostridium Prazmowski 1880, 23AL. In De Vos P, Garrity G, Jones D, Krieg NR, Ludwig W. (editors) Bergey’s Manual of Systematic Bacteriology (The Firmicutes) 3, 2nd edn. NewYork: Springer; 2009 pp 736–864
    [Google Scholar]
  18. Holdeman LV, Cato EP, Moore WEC. Anaerobe Laboratory Manual, 4th edn. Blacksburg, VA: Virginia Polytechnic Institute and State University; 1977
    [Google Scholar]
  19. 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]
  20. 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]
  21. 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]
  22. Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010; 27:221–224 [View Article][PubMed]
    [Google Scholar]
  23. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007; 23:2947–2948 [View Article][PubMed]
    [Google Scholar]
  24. 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]
  25. 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]
  26. Duda VI, Lebedinsky AV, Mushegian MS, Mitjushina LL. A new anaerobic bacterium, forming up to five endospores per cell – Anaerobacter polyendosporus gen. et spec. nov. Arch Microbiol 1987; 148:121–127 [View Article]
    [Google Scholar]
  27. Siunov AV, Nikitin DV, Suzina NE, Dmitriev VV, Kuzmint NP et al. Phylogenetic status of Anaerobacter polyendosporus, an anaerobic, polysporogenic bacterium. Int J Syst Bacteriol 1999; 49 Pt 3:1119–1124 [View Article][PubMed]
    [Google Scholar]
  28. Lawson PA, Rainey FA. Proposal to restrict the genus Clostridium Prazmowski to Clostridium butyricum and related species. Int J Syst Evol Microbiol 2016; 66:1009–1016 [View Article][PubMed]
    [Google Scholar]
  29. 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]
  30. 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]
  31. Shaw LP, Hubbard A, George S. Comparison of long-read sequencing technologies in the hybrid assembly of complex bacterial genomes. Microb Genom 2017; 3:e000118
    [Google Scholar]
  32. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article][PubMed]
    [Google Scholar]
  33. Yoon SH, 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]
  34. 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]
  35. 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]
  36. 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]
  37. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 2013; 14:60 [View Article][PubMed]
    [Google Scholar]
  38. Blenden DC, Goldberg HS. Silver impregnation stain for Leptospira and flagella. J Bacteriol 1965; 89:899–900 [View Article][PubMed]
    [Google Scholar]
  39. Watanabe M, Kaku N, Ueki K, Ueki A. Falcatimonas natans gen. nov., sp. nov., a strictly anaerobic, amino-acid-decomposing bacterium isolated from a methanogenic reactor of cattle waste. Int J Syst Evol Microbiol 2016; 66:4639–4644 [View Article][PubMed]
    [Google Scholar]
  40. Miller LT. Single derivatization method for routine analysis of bacterial whole-cell fatty acid methyl esters, including hydroxy acids. J Clin Microbiol 1982; 16:584–586 [View Article][PubMed]
    [Google Scholar]
  41. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V et al. The carbohydrate-active enzymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 2009; 37:D233–D238 [View Article][PubMed]
    [Google Scholar]
  42. Ueki A, Takehara T, Ishioka G, Kaku N, Ueki K. Degradation of the fungal cell wall by clostridial strains isolated from soil subjected to biological soil disinfestation and biocontrol of Fusarium wilt disease of spinach. Appl Microbiol Biotechnol 2017; 101:8267–8277 [View Article][PubMed]
    [Google Scholar]
  43. Itoh T, Hibi T, Fujii Y, Sugimoto I, Fujiwara A et al. Cooperative degradation of chitin by extracellular and cell surface-expressed chitinases from Paenibacillus sp. strain FPU-7. Appl Environ Microbiol 2013; 79:7482–7490 [View Article][PubMed]
    [Google Scholar]
  44. Lupa B, Wiegel J. Genus IV. Desulfitbacterium Utkin, Woese and Wiegel 1994, 615vp. In De Vos P, Garrity G, Jones D, Krieg NR, Ludwig W. (editors) In Bergey’s Manual of Systematic Bacteriology (The Firmicutes) 3, 2nd edn. NewYork: Springer; 2009 pp 975–982
    [Google Scholar]
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