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Volume 2, Issue 12

Biofilm formation by is altered in the presence of pesticides Open Access

Abstract

uses swarming motility and biofilm formation to colonize plant roots and form a symbiotic relationship with the plant. Swarming motility and biofilm formation are group behaviours made possible through the use of chemical messengers. We investigated whether chemicals applied to plants would interfere with the swarming motility and biofilm-forming capabilities of . We hypothesized that pesticides could act as chemical signals that influence bacterial behaviour; this research investigates whether swarming motility and biofilm formation of is affected by the application of the commercial pesticides with the active ingredients of neem oil, pyrethrin, or malathion. The results indicate that all three pesticides inhibit biofilm formation. Swarming motility is not affected by the application of pyrethrin or malathion, but swarm expansion and pattern is altered in the presence of neem oil. Future studies to investigate the mechanism by which pesticides alter biofilm formation are warranted.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Bacillus subtilis , biofilm formation , neem , pesticide , plant growth-promoting bacteria and swarming
Funding
This study was supported by the:
  • Truman State University
    • Principle Award Recipient: Rachael Newton
© 2020 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2020-11-12
2024-04-25
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References

  1. Beneduzi A, Ambrosini A, Passaglia LMP. Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet Mol Biol 2012; 35:1044–1051 [View Article][PubMed]
     [Google Scholar]
  2. Souza Rde, Ambrosini A, Passaglia LMP. Plant growth-promoting bacteria as inoculants in agricultural soils. Genet Mol Biol 2015; 38:401–419 [View Article][PubMed]
     [Google Scholar]
  3. Rudrappa T, Biedrzycki ML, Bais HP. Causes and consequences of plant-associated biofilms. FEMS Microbiol Ecol 2008; 64:153–166 [View Article][PubMed]
     [Google Scholar]
  4. Lugtenberg B, Kamilova F. Plant-Growth-Promoting rhizobacteria. Annu Rev Microbiol 2009; 63:541–556 [View Article][PubMed]
     [Google Scholar]
  5. Lynch JM. The Rhizosphere Wiley: 1990
     [Google Scholar]
  6. Allard-Massicotte R, Tessier L, Lécuyer F, Lakshmanan V, Lucier J-F et al. Bacillus subtilis Early Colonization of Arabidopsis thaliana Roots Involves Multiple Chemotaxis Receptors. mBio 2016; 7:e01664–16 [View Article][PubMed]
     [Google Scholar]
  7. Gao S, Wu H, Yu X, Qian L, Gao X. Swarming motility plays the major role in migration during tomato root colonization by Bacillus subtilis SWR01. Biological Control 2016; 98:11–17 [View Article]
     [Google Scholar]
  8. Beauregard PB, Chai Y, Vlamakis H, Losick R, Kolter R. Bacillus subtilis biofilm induction by plant polysaccharides. Proc Natl Acad Sci U S A 2013; 110:E1621–E1630 [View Article][PubMed]
     [Google Scholar]
  9. Ikeda AC, Bassani LL, Adamoski D, Stringari D, Cordeiro VK et al. Morphological and genetic characterization of endophytic bacteria isolated from roots of different maize genotypes. Microb Ecol 2013; 65:154–160 [View Article][PubMed]
     [Google Scholar]
  10. Kearns DB. A field guide to bacterial swarming motility. Nat Rev Microbiol 2010; 8:634–644 [View Article][PubMed]
     [Google Scholar]
  11. Kearns DB, Losick R. Swarming motility in undomesticated Bacillus subtilis . Mol Microbiol 2004; 49:581–590 [View Article]
     [Google Scholar]
  12. Patrick JE, Kearns DB. Laboratory strains of Bacillus subtilis do not exhibit swarming motility. J Bacteriol 2009; 191:7129–7133 [View Article][PubMed]
     [Google Scholar]
  13. Kalamara M, Spacapan M, Mandic-Mulec I, Stanley-Wall NR. Social behaviours by Bacillus subtilis: quorum sensing, kin discrimination and beyond. Mol Microbiol 2018; 110:863–878 [View Article][PubMed]
     [Google Scholar]
  14. Guillen N, Weinrauch Y, Dubnau DA. Cloning and characterization of the regulatory Bacillus subtilis competence genes comA and comB. J Bacteriol 1989; 171:5354–5361 [View Article][PubMed]
     [Google Scholar]
  15. Nakano MM, Zuber P. Cloning and characterization of srfB, a regulatory gene involved in surfactin production and competence in Bacillus subtilis . J Bacteriol 1989; 171:5347–5353 [View Article][PubMed]
     [Google Scholar]
  16. Nakano MM, Marahiel MA, Zuber P. Identification of a genetic locus required for biosynthesis of the lipopeptide antibiotic surfactin in Bacillus subtilis . J Bacteriol 1988; 170:5662–5668 [View Article][PubMed]
     [Google Scholar]
  17. Rudrappa T, Czymmek KJ, Paré PW, Bais HP. Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 2008; 148:1547–1556 [View Article][PubMed]
     [Google Scholar]
  18. Vlamakis H, Chai Y, Beauregard P, Losick R, Kolter R. Sticking together: building a biofilm the Bacillus subtilis way. Nat Rev Microbiol 2013; 11:157–168 [View Article][PubMed]
     [Google Scholar]
  19. Cairns LS, Hobley L, Stanley-Wall NR. Biofilm formation by Bacillus subtilis: new insights into regulatory strategies and assembly mechanisms. Mol Microbiol 2014; 93:587–598 [View Article][PubMed]
     [Google Scholar]
  20. Branda SS, González-Pastor JE, Ben-Yehuda S, Losick R, Kolter R. Fruiting body formation by Bacillus subtilis . Proc Natl Acad Sci USA 2001; 98:11621–11626 [View Article][PubMed]
     [Google Scholar]
  21. Earl AM, Losick R, Kolter R. Ecology and genomics of Bacillus subtilis . Trends Microbiol 2008; 16:269–275 [View Article][PubMed]
     [Google Scholar]
  22. Rudrappa T, Bais HP. Arabidopsis thaliana root surface chemistry regulates in planta biofilm formation of Bacillus subtilis . Plant Signal Behav 2007; 2:349–350 [View Article][PubMed]
     [Google Scholar]
  23. Choudhary DK, Johri BN. Interactions of Bacillus spp. and plants--with special reference to induced systemic resistance (ISR). Microbiol Res 2009; 164:493–513 [View Article][PubMed]
     [Google Scholar]
  24. Ongena M, Jourdan E, Adam A, Paquot M, Brans A et al. Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ Microbiol 2007; 9:1084–1090 [View Article][PubMed]
     [Google Scholar]
  25. Hirooka K. Transcriptional response machineries of Bacillus subtilis conducive to plant growth promotion. Biosci Biotechnol Biochem 2014; 78:1471–1484 [View Article][PubMed]
     [Google Scholar]
  26. Gopal M, Gupta A, Arunachalam V, Magu SP. Impact of azadirachtin, an insecticidal allelochemical from neem on soil microflora, enzyme and respiratory activities. Bioresour Technol 2007; 98:3154–3158 [View Article][PubMed]
     [Google Scholar]
  27. Spyrou IM, Karpouzas DG, Menkissoglu-Spiroudi U. Do botanical pesticides alter the structure of the soil microbial community?. Microb Ecol 2009; 58:715–727 [View Article][PubMed]
     [Google Scholar]
  28. C-C L. Effect of pesticides on soil microbial community. J Environ Sci Heal B 2010; 45:348–359
     [Google Scholar]
  29. Duke SO. Interaction of chemical pesticides and their formulation ingredients with microbes associated with plants and plant pests. J Agric Food Chem 2018; 66:7553–7561 [View Article][PubMed]
     [Google Scholar]
  30. Kumar V, Singh S, Upadhyay N. Effects of organophosphate pesticides on siderophore producing soils microorganisms. Biocatal Agric Biotechnol 2019; 21:101359 [View Article]
     [Google Scholar]
  31. Kalia A, Gosal SK. Effect of pesticide application on soil microorganisms. Arch Agron Soil Sci 2011; 57:569–596 [View Article]
     [Google Scholar]
  32. Eisenhauer N, Klier M, Partsch S, Sabais ACW, Scherber C et al. No interactive effects of pesticides and plant diversity on soil microbial biomass and respiration. Applied Soil Ecology 2009; 42:31–36 [View Article]
     [Google Scholar]
  33. O'Toole GA, Kolter R. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 1998; 28:449–461 [View Article][PubMed]
     [Google Scholar]
  34. Atwood D. Paisley-Jones, Claire Pesticides Industry Sales and Usage: 2008-2012 Market Estimates Washington, DC: U.S. Environmental Protection Agency; n.d; 2008
     [Google Scholar]
  35. The list of organic pesticides Approved by the USDA | AGDAILY n.d https://www.agdaily.com/technology/the-list-of-pesticides-approved-for-organic-production/ (accessed May 18, 2020).
  36. LaForge FB, Barthel WF. Constituents of pyrethrum flowers; the partial synthesis of pyrethrins and cinerins and their relative toxicities. J Org Chem 1947; 12:199–202 [View Article][PubMed]
     [Google Scholar]
  37. Jensen IM, Whatling P. Chapter 71 - Malathion: A Review of Toxicology. In Krieger R. editor Hayes’ Handbook of Pesticide Toxicology, 3rd ed. New York: Academic Press; 2010 pp 1527–1542
     [Google Scholar]
  38. Kobayashi K. Bacillus subtilis pellicle formation proceeds through genetically defined morphological changes. J Bacteriol 2007; 189:4920–4931 [View Article][PubMed]
     [Google Scholar]
  39. Lee LM, Rosenberg G, Rubinstein SM. A sequence of developmental events occurs underneath growing Bacillus subtilis pellicles. Front Microbiol 2019; 10:842 [View Article][PubMed]
     [Google Scholar]
  40. Trejo M, Douarche C, Bailleux V, Poulard C, Mariot S et al. Elasticity and wrinkled morphology of Bacillus subtilis pellicles. Proc Natl Acad Sci USA 2013; 110:2011–2016 [View Article][PubMed]
     [Google Scholar]
  41. Asally M, Kittisopikul M, Rué P, Du Y, Hu Z et al. Localized cell death focuses mechanical forces during 3D patterning in a biofilm. Proc Natl Acad Sci U S A 2012; 109:18891–18896 [View Article][PubMed]
     [Google Scholar]
  42. Stanlake GJ, Clark JB. Effects of a commercial malathion preparation on selected soil bacteria. Appl Microbiol 1975; 30:335–336 [View Article][PubMed]
     [Google Scholar]
  43. Butterworth JH, Morgan ED. Isolation of a substance that suppresses feeding in locusts. Chem Commun. 196823–24 [View Article]
     [Google Scholar]
  44. Djibril D, Mamadou F, Gérard V, Geuye M-DC, Oumar S et al. Physical characteristics, chemical composition and distribution of constituents of the neem seeds (Azadirachta indica A. Juss) collected in Senegal. Res J Chem Sci 2015; 5:7
     [Google Scholar]
  45. Swapna Sonale R, Ramalakshmi K, Udaya Sankar K. Characterization of neem (Azadirachta indica A. Juss) seed volatile compounds obtained by supercritical carbon dioxide process. J Food Sci Technol 2018; 55:1444–1454 [View Article][PubMed]
     [Google Scholar]
  46. Gossé B, Amissa AA, Anoh Adjé F, Bobélé Niamké F, Ollivier D et al. Analysis of components of neem (Azadirachta indica) oil by diverse chromatographic techniques. J Liq Chromatogr Relat Technol 2005; 28:2225–2233 [View Article]
     [Google Scholar]
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Biofilm formation by Bacillus subtilis is altered in the presence of pesticides
Access Microbiology 2, e000175 (2020); https://doi.org/10.1099/acmi.0.000175
/content/journal/acmi/10.1099/acmi.0.000175
/content/journal/acmi/10.1099/acmi.0.000175
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