Skip to content
1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo International Journal of Systematic and Evolutionary Microbiology

Volume 73, Issue 4

subsp. subsp. nov. and subsp. subsp. nov., plant growth-promoting bacteria and biological control agents isolated from wheat ( subsp. ) in the Yaqui Valley, Mexico No Access

Abstract

Strain TSO2, a plant growth-promoting rhizobacteria and biological control agent, was isolated from wheat rhizosphere sampled from the Yaqui Valley in Mexico. The strain was identified using a polyphasic approach. Based on its analysis of the full-length 16S rRNA gene, strain TSO2 was assigned to the genus , which was supported by morphological and metabolic traits, such as Gram-positive staining, rod shape, spore formation, strictly aerobic metabolism, catalase-positive activity, starch, and casein hydrolysis, reduction of nitrate to nitrite, growth in presence of lysozyme and 2 % NaCl, citrate utilization, growth at pH 6.0, acid production from glucose and indole production from tryptophan. Additionally, strain TSO2 possesses swarming motility, presenting a featureless mat pattern that can cover the whole petri dish. The whole-genome phylogenetic relationship analysis elucidated that strain TSO2 is closely related to TE3. The maximum values for average nucleotide identity (ANI) and DNA–DNA hybridization from the genome-to-genome distance calculator (GGDC) were 97 and 73.4 %, respectively, related to TE3, where both ANI and GGDC values were barely above the species delimitation threshold, but below the subspecies limit. Also, strain TSO2 showed the ability to produce a fatty acid (C) that is not present in closely related species. These results provide evidence that strain TSO2 is a novel subspecies of the species , for which the name subsp. subsp. nov. is proposed. The type strain of subsp. subsp. nov. is TSO2 (CM-CNRG TB52=LBPCV TSO2). The description of this novel subspecies automatically creates the subspecies subsp. subsp. nov. for which the type strain is TE3 (CM-CNRG TB54=CCStamb A1).

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): average nucleotide identity , biological control agent , genome-to-genome distance calculator , plant growth-promoting bacteria and whole-genome phylogenetic
Funding
This study was supported by the:
  • PROFAPI-ITSON (Award 2022_001)
    • Principle Award Recipient: Sergiode los Santos Villalobos
  • CONACYT (Award 257246)
    • Principle Award Recipient: Sergiode los Santos Villalobos
  • CONACYT (Award 1774)
    • Principle Award Recipient: Sergiode los Santos Villalobos
© 2023 The Authors
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.005779
2023-04-26
2025-06-13
Loading full text...

Full text loading...

References

  1. Valenzuela Ruiz V, de los Santos-Villalobos S, Montoya-Martínez AC, Parra-Cota FI, Santoyo G et al. Bacillus cabrialesii subsp. cabrialesii subsp. nov. and Bacillus cabrialesii subsp. tritici subsp. nov., plant growth-promoting bacteria and biological control agents isolated from wheat (Triticum turgidum subsp. durum) in the yaqui Valley, Mexico. Figshare 2023 https://doi.org/10.6084/m9.figshare.21664136.v1
     [Google Scholar]
  2. Turnbull P. Bacillus. In Baron S. eds Medical Microbiology Galveston: University of Texas Medical Branch at Galveston; 1996 p Chapter 15
     [Google Scholar]
  3. De Vos P, Garrity GM, Jones D, Krieg NR, Ludwig W. Bergey’s manual of Systematic Bacteriology. Volume 3: The Firmicutes, 2 edition. New York, NY: Springer-Verlag New York; 2009 [View Article]
     [Google Scholar]
  4. Radhakrishnan R, Hashem A, Abd Allah EF. Bacillus: a biological tool for crop improvement through bio-molecular changes in adverse environments. Front Physiol 2017; 8:667 [View Article]
     [Google Scholar]
  5. Valenzuela-Ruiz V, Gálvez-Gamboa GT, Villla-Rodriguez ED, Parra-Cota FI, Santoyo G. Lipopeptides produced by biological control agents of the genus Bacillus: a review of analytical tools used for their study. Rev Mex Ciencias Agrícolas 2020; 11:419–432
     [Google Scholar]
  6. Shafi J, Tian H, Ji M. Bacillus species as versatile weapons for plant pathogens: a review. Biotechnol Biotechnol Equip 2017; 31:446–459 [View Article]
     [Google Scholar]
  7. Valenzuela-Aragon B, Parra-Cota FI, Santoyo G, Arellano-Wattenbarger GL, de los Santos-Villalobos S. Plant-assisted selection: a promising alternative for in vivo identification of wheat (Triticum turgidum L. subsp. durum) growth promoting bacteria. Plant Soil 2018; 435:367–384
     [Google Scholar]
  8. Villarreal-Delgado MF, Villa-Rodríguez ED, Cira-Chávez LA, Estrada-Alvarado MI, Parra-Cota FI et al. The genus Bacillus as a biological control agent and its implications in the agricultural biosecurity. Mex J Phytopathol 2018; 36:95–130 [View Article]
     [Google Scholar]
  9. Gupta RS, Patel S, Saini N, Chen S. Robust demarcation of 17 distinct Bacillus species clades, proposed as novel Bacillaceae genera, by phylogenomics and comparative genomic analyses: description of Robertmurraya kyonggiensis sp. nov. and proposal for an emended genus Bacillus limiting it only to the members of the Subtilis and Cereus clades of species. Int J Syst Evol Microbiol 2020; 70:5753–5798 [View Article] [PubMed]
     [Google Scholar]
  10. de los Santos Villalobos S, Robles RI, Parra Cota FI, Larsen J, Lozano P et al. Bacillus cabrialesii sp. nov., an endophytic plant growth promoting bacterium isolated from wheat (Triticum turgidum subsp. durum) in the Yaqui Valley, Mexico. Int J Syst Evol Microbiol 2019; 69:3939–3945 [View Article]
     [Google Scholar]
  11. Villa-Rodríguez E, Parra-Cota F, Castro-Longoria E, López-Cervantes J, de los Santos-Villalobos S. Bacillus subtilis TE3: a promising biological control agent against Bipolaris sorokiniana, the causal agent of spot blotch in wheat (Triticum turgidum L. subsp. durum). Biological Control 2019; 132:135–143 [View Article]
     [Google Scholar]
  12. Rojas Padilla J, Chaparro Encinas LA, Robles Montoya RI, De los Santos Villalobos S. Promoción de crecimiento en trigo (Triticum turgidum L. subsp. durum) por la co-inoculación de cepas nativas de Bacillus aisladas del Valle del Yaqui, México. NS 2020; 12:1–27 [View Article]
     [Google Scholar]
  13. Villa-Rodriguez E, Moreno-Ulloa A, Castro-Longoria E, Parra-Cota FI, de Los Santos-Villalobos S. Integrated omics approaches for deciphering antifungal metabolites produced by a novel Bacillus species, B. cabrialesii TE3T, against the spot blotch disease of wheat (Triticum turgidum L. subsp. durum). Microbiol Res 2021; 251:126826 [View Article]
     [Google Scholar]
  14. Moore WEC, Stackebrandt E, Kandler O, Colwell RR, Krichevsky MI et al. Report of the AD hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Evol Microbiol 1987; 37:463–464 [View Article]
     [Google Scholar]
  15. Borriss R, Chen X-H, Rueckert C, Blom J, Becker A et al. Relationship of Bacillus amyloliquefaciens clades associated with strains DSM 7T and FZB42T: a proposal for Bacillus amyloliquefaciens subsp. amyloliquefaciens subsp. nov. and Bacillus amyloliquefaciens subsp. plantarum subsp. nov. based on complete genome sequence comparisons. Int J Syst Evol Microbiol 2011; 61:1786–1801 [View Article] [PubMed]
     [Google Scholar]
  16. de los Santos-Villalobos S, Díaz-Rodríguez AM, Ávila-Mascareño MF, Martínez-Vidales AD, Parra-Cota FI. Colmena: a culture collection of native microorganisms for harnessing theagro-biotechnological potential in soils and contributing to food security. Diversity 2021; 13:337 [View Article]
     [Google Scholar]
  17. de los Santos-Villalobos S, Parra-Cota FI, Herrera-Sepúlveda A, Valenzuela-Aragon B, Estrada-Mora JC. Collection of edaphic microorganisms and native endophytes to contribute to national food security. Rev Mex ciencias agrícolas 2018; 9:191–202 [View Article]
     [Google Scholar]
  18. Ibarra-Villarreal AL, Gándara-Ledezma A, Godoy-Flores AD, Herrera-Sepúlveda A, Díaz-Rodríguez AM et al. Salt-tolerant Bacillus species as a promising strategy to mitigate the salinity stress in wheat (Triticum turgidum subsp. durum). Journal of Arid Environments 2021; 186:104399 [View Article]
     [Google Scholar]
  19. Andrews S. FastQC: a quality control tool for high throughput sequence data; 2010 http://www.bioinformatics.babraham.ac.uk/projects/fastqc
  20. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article]
     [Google Scholar]
  21. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article]
     [Google Scholar]
  22. Darling ACE, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 2004; 14:1394–1403 [View Article]
     [Google Scholar]
  23. Carattoli A, Zankari E, García-Fernández A, Voldby Larsen M, Lund O et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 2014; 58:3895–3903 [View Article] [PubMed]
     [Google Scholar]
  24. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ et al. The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res 2014; 42:D206–14 [View Article]
     [Google Scholar]
  25. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
     [Google Scholar]
  26. Lee I, Chalita M, Ha S-M, Na S-I, Yoon S-H et al. ContEst16S: an algorithm that identifies contaminated prokaryotic genomes using 16S RNA gene sequences. Int J Syst Evol Microbiol 2017; 67:2053–2057 [View Article] [PubMed]
     [Google Scholar]
  27. 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]
     [Google Scholar]
  28. 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]
     [Google Scholar]
  29. Liu Y, Du J, Lai Q, Zeng R, Ye D et al. Proposal of nine novel species of the Bacillus cereus group. Int J Syst Evol Microbiol 2017; 67:2499–2508 [View Article]
     [Google Scholar]
  30. Wang L-T, Lee F-L, Tai C-J, Kasai H. Comparison of gyrB gene sequences, 16S rRNA gene sequences and DNA-DNA hybridization in the Bacillus subtilis group. Int J Syst Evol Microbiol 2007; 57:1846–1850 [View Article]
     [Google Scholar]
  31. 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]
  32. 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]
     [Google Scholar]
  33. Yoon S-H, Ha S-M, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017; 110:1281–1286 [View Article]
     [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]
     [Google Scholar]
  35. Meier-Kolthoff JP, Hahnke RL, Petersen J, Scheuner C, Michael V et al. Completegenome sequence of DSM 30083T, the type strain (U5/41T)of Escherichia coli, and a proposal for delineating subspecies inmicrobial taxonomy. Stand Genomic Sci 2014; 9:2 [View Article]
     [Google Scholar]
  36. Varghese NJ, Mukherjee S, Ivanova N, Konstantinidis KT, Mavrommatis K et al. Microbial species delineation using whole genome sequences. Nucleic Acids Res 2015; 43:6761–6771 [View Article] [PubMed]
     [Google Scholar]
  37. Auch AF, von Jan M, Klenk H-P, Göker M. Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci 2010; 2:117–134 [View Article] [PubMed]
     [Google Scholar]
  38. 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]
  39. Arkin AP, Cottingham RW, Henry CS, Harris NL, Stevens RL et al. KBase: the United States department of energy systems biology knowledgebase. Nat Biotechnol 2018; 36:566–569 [View Article]
     [Google Scholar]
  40. Kearns DB, Losick R. Swarming motility in undomesticated Bacillus subtilis. Mol Microbiol 2003; 49:581–590 [View Article] [PubMed]
     [Google Scholar]
  41. Logan NA, Berge O, Bishop AH, Busse H-J, De Vos P et al. Proposed minimal standards for describing new taxa of aerobic, endospore-forming bacteria. Int J Syst Evol Microbiol 2009; 59:2114–2121 [View Article] [PubMed]
     [Google Scholar]
  42. Tindall BJ. Proposed modifications to rule 40d of the international code of nomenclature of prokaryotes. Int J Syst Evol Microbiol 2019; 69:1519–1520 [View Article]
     [Google Scholar]
  43. Parker CT, Tindall BJ, Garrity GM. International Code of Nomenclature of Prokaryotes. Int J Syst Evol Microbiol 2019; 69:S1–S111 [View Article]
     [Google Scholar]
/content/journal/ijsem/10.1099/ijsem.0.005779
Loading
Bacillus cabrialesii subsp. cabrialesii subsp. nov. and Bacillus cabrialesii subsp. tritici subsp. nov., plant growth-promoting bacteria and biological control agents isolated from wheat (Triticum turgidum subsp. durum) in the Yaqui Valley, Mexico
Int J Syst Evol Microbiol 73, 005779 (2023); https://doi.org/10.1099/ijsem.0.005779
/content/journal/ijsem/10.1099/ijsem.0.005779
/content/journal/ijsem/10.1099/ijsem.0.005779
Loading

Data & Media loading...

Supplements

Loading data from figshare Loading data from figshare

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error