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Do Multi-year Applications of Bacillus thuringiensis subsp. israelensis for Control of Mosquito Larvae Affect the Abundance of B. cereus Group Populations in Riparian Wetland Soils?

  • Soil Microbiology
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Abstract

Bacillus thuringiensis subsp. israelensis (Bti) is a soil-borne bacterium affiliated to the Bacillus cereus group (Bcg) and has been used in biocontrol products against nematoceran larvae for several decades. However, knowledge is limited on whether long-term Bti application can affect the structure of indigenous communities of Bcg and the overall abundance of Bti. Using species- and group-specific quantitative PCR assays, we measured the Bcg- and Bti-abundances in riparian wetlands in the River Dalälven floodplains of central Sweden. On five occasions during one vegetative season, soil samples were collected in alder swamps and wet meadows which had been treated with Bti for mosquito larvae control during the preceding 11 years, as well as in untreated control sites and well-drained forests in the same area. The average abundance of Bcg in alder swamps was around three times higher than in wet meadows. Across all sites and habitats, the Bti treatments had no effect on the Bcg-abundance, whereas the Bti-abundance was significantly higher in the treated than in the control sites. However, for individual sampling sites, abundances of Bti and Bcg were not correlated with the number of Bti applications, indicating that added Bti possibly influenced the total population of Bti in the short term but had only a limited effect in the longer term. The findings of this study increase the understanding of the ecology of Bti applications for mosquito control, which can facilitate environmental risk assessment in connection with approval of microbiological control agents.

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References

  1. Vilas-Bôas GT, Peruca APS, Arantes OMN (2007) Biology and taxonomy of Bacillus cereus, Bacillus anthracis, and Bacillus thuringiensis Can. J. Microbiol. 53:673–687. doi:10.1139/W07-029

    Article  PubMed  Google Scholar 

  2. Hendriksen NB (2016) The two lives of Bacillus thuringiensis: response to Ruan et al. and Loguercio and Argôlo-Filho Trends Microbiol. 24:1–2. doi:10.1016/j.tim.2015.10.010

    Article  CAS  PubMed  Google Scholar 

  3. Ceuppens S, Boon N, Uyttendaele M (2013) Diversity of Bacillus cereus group strains is reflected in their broad range of pathogenicity and diverse ecological lifestyles FEMS Microbiol. Ecol. 84:433–450. doi:10.1111/1574-6941.12110

    Article  CAS  PubMed  Google Scholar 

  4. Rasko D, Altherr M, Han C, Ravel J (2005) Genomics of the Bacillus cereus group of organisms FEMS Microbiol. Rev. 29:303–329. doi:10.1016/j.femsre.2004.12.005

    CAS  PubMed  Google Scholar 

  5. Lacey LA, Grzywacz D, Shapiro-Ilan DI, Frutos R, Brownbridge M, Goettel MS (2015) Insect pathogens as biological control agents: back to the future J. Invertebr. Pathol. 132:1–41. doi:10.1016/j.jip.2015.07.009

    Article  CAS  PubMed  Google Scholar 

  6. Lacey LA (2007) Bacillus thuringiensis serovariety israelensis and Bacillus sphaericus for mosquito control J. Am. Mosq. Control Assoc. 23:133–163. doi:10.2987/8756-971X(2007)23[133:BTSIAB]2.0.CO;2

    Article  CAS  PubMed  Google Scholar 

  7. Bravo A, Likitvivatanavong S, Gill SS, Soberón M (2011) Bacillus thuringiensis: a story of a successful bioinsecticide Insect Biochem. Mol. Biol. 41:423–431. doi:10.1016/j.ibmb.2011.02.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Guidi V, Patocchi N, Lüthy P, Tonolla M (2011) Distribution of Bacillus thuringiensis subsp. israelensis in soil of a Swiss wetland reserve after 22 years of mosquito control Appl. Environ. Microbiol. 77:3663–3668. doi:10.1128/aem.00132-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Becker N (1997) Microbial control of mosquitoes: management of the Upper Rhine mosquito population as a model programme Parasitol. Today 13:485–487. doi:10.1016/S0169-4758(97)01154-X

    Article  CAS  PubMed  Google Scholar 

  10. Boyer S, Tilquin M, Ravanel P (2007) Differential sensitivity to Bacillus thuringiensis var. israelensis and temephos in field mosquito populations of Ochlerotatus cataphylla (Diptera: Culicidae): toward resistance? Environ. Toxicol. Chem. 26:157–162. doi:10.1897/06-205R.1

    Article  CAS  PubMed  Google Scholar 

  11. Lévêque C, Hougard JM, Resh V, Statzner B, Yaméogo L (2003) Freshwater ecology and biodiversity in the tropics: what did we learn from 30 years of Onchocerciasis control and the associated biomonitoring of West African rivers? Hydrobiologia 500:23–49. doi:10.1023/A:1024660017077

    Article  Google Scholar 

  12. Hongyu Z, Changju Y, Jingye H, Lin L (2004) Susceptibility of field populations of Anopheles sinensis (Diptera: Culicidae) to Bacillus thuringiensis subsp. israelensis Biocontrol Sci. Tech. 14:321–325. doi:10.1080/09583150310001639187

    Article  Google Scholar 

  13. Lundström JO, Schäfer ML, Petersson E, Persson Vinnersten TZ, Landin J, Brodin Y (2010) Production of wetland Chironomidae (Diptera) and the effects of using Bacillus thuringiensis israelensis for mosquito control Bull. Entomol. Res. 100:117–125. doi:10.1017/S0007485309990137

    Article  PubMed  Google Scholar 

  14. Duchet C, Tetreau G, Marie A, Rey D, Besnard G, Perrin Y, Paris M, David J-P, Lagneau C, Després L (2014) Persistence and recycling of bioinsecticidal Bacillus thuringiensis subsp. israelensis spores in contrasting environments: evidence from field monitoring and laboratory experiments Microb. Ecol. 67:576–586. doi:10.1007/s00248-013-0360-7

    Article  CAS  PubMed  Google Scholar 

  15. Tetreau G, Alessi M, Veyrenc S, Périgon S, David J-P, Reynaud S, Després L (2012) Fate of Bacillus thuringiensis subsp. israelensis in the field: evidence for spore recycling and differential persistence of toxins in leaf litter Appl. Environ. Microbiol. 78:8362–8367. doi:10.1128/AEM.02088-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Schneider S, Hendriksen NB, Melin P, Lundström JO, Sundh I (2015) Chromosome-directed PCR-based detection and quantification of Bacillus cereus group members with focus on B. thuringiensis serovar israelensis active against nematoceran larvae Appl. Environ. Microbiol. 81:4894–4903. doi:10.1128/AEM.00671-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Schäfer ML, Lundström JO (2014) Efficiency of Bti-based floodwater mosquito control in Sweden—four examples J Eur Mosq Control Assoc 32:1–8

    Google Scholar 

  18. Travers RS, Martin PAW, Reichelderfer CF (1987) Selective process for efficient isolation of soil Bacillus spp Appl. Environ. Microbiol. 53:1263–1266

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Donnarumma F, Paffetti D, Stotzky G, Giannini R, Vettori C (2010) Potential gene exchange between Bacillus thuringiensis subsp. kurstaki and Bacillus spp. in soil in situ Soil Biol. Biochem. 42:1329–1337. doi:10.1016/j.soilbio.2010.03.014

    Article  CAS  Google Scholar 

  20. Guidi V, De Respinis S, Benagli C, Lüthy P, Tonolla M (2010) A real-time PCR method to quantify spores carrying the Bacillus thuringiensis var. israelensis cry4Aa and cry4Ba genes in soil J. Appl. Microbiol. 109:1209–1217. doi:10.1111/j.1365-2672.2010.04741.x

    Article  CAS  PubMed  Google Scholar 

  21. Fournier DA, Skaug HJ, Ancheta J, Ianelli J, Magnusson A, Maunder MN, Nielsen A, Sibert J (2012) AD model builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models Optim Methods Softw 27:233–249. doi:10.1080/10556788.2011.597854

    Article  Google Scholar 

  22. Development Core Team R (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, http://www.R-project.org

    Google Scholar 

  23. Venables WN, Ripley BD (2002) Modern applied statistics with S. R package version 7.2–45. In: Venables WN, Ripley BD. http://www.stats.ox.ac.uk/pub/MASS4/

  24. Fox J, Weisberg S (2011) An {R} Companion to applied regression, Second edition. http://socserv.socsci.mcmaster.ca/jfox/Books/Companion.

  25. Lander JP (2016) coefplot: plots coefficients from fitted models. R package version 1.2.4. https://CRAN.R-project.org/package=coefplot.

  26. Eskils K, Lövgren A (1997) Release of Bacillus thuringiensis subsp. israelensis in Swedish soil FEMS Microbiol. Ecol. 23:229–237. doi:10.1111/j.1574-6941.1997.tb00405.x

    Article  CAS  Google Scholar 

  27. Hendriksen NB, Hansen BM (2002) Long-term survival and germination of Bacillus thuringiensis var. kurstaki in a field trial Can. J. Microbiol. 48:256–261. doi:10.1139/w02-009

    Article  CAS  PubMed  Google Scholar 

  28. Raymond B, Johnston PR, Nielsen-LeRoux C, Lereclus D, Crickmore N (2010) Bacillus thuringiensis: an impotent pathogen? Trends Microbiol. 18:189–194. doi:10.1016/j.tim.2010.02.006

    Article  CAS  PubMed  Google Scholar 

  29. Bizzarri MF, Bishop AH (2007) Recovery of Bacillus thuringiensis in vegetative form from the phylloplane of clover (Trifolium hybridum) during a growing season J. Invertebr. Pathol. 94:38–47. doi:10.1016/j.jip.2006.08.007

    Article  PubMed  Google Scholar 

  30. Wakisaka Y, Masaki E, Nishimoto Y (1982) Formation of crystalline delta-endotoxin or poly-beta-hydroxybutyric acid granules by asporogenous mutants of Bacillus thuringiensis Appl Env Microbiol 43:1473–1480

    CAS  Google Scholar 

  31. Blume H-P, Brümmer GW, Fleige H, Horn R, Kandeler E, Kögel-Knabner I, Kretzschmar R, Stahr K, Wilke B-M (2016) Soil organisms and their habitat. In: Scheffer F, Schachtchabel P (eds) Soil Science. Springer, Berlin Heidelberg, pp. 87–122

  32. De Respinis S, Demarta A, Patocchi N, Lüthy P, Peduzzi R, Tonolla M (2006) Molecular identification of Bacillus thuringiensis var. israelensis to trace its fate after application as a biological insecticide in wetland ecosystems Lett. Appl. Microbiol. 43:495–501. doi:10.1111/j.1472-765X.2006.01999.x

    Article  PubMed  Google Scholar 

  33. Schneider S, Rehner SA, Widmer F, Enkerli J (2011) A PCR-based tool for cultivation-independent detection and quantification of Metarhizium clade 1 J. Invertebr. Pathol. 108:106–114. doi:10.1016/j.jip.2011.07.005

    Article  CAS  PubMed  Google Scholar 

  34. Schneider S, Enkerli J, Widmer F (2009) A generally applicable assay for the quantification of inhibitory effects on PCR J. Microbiol. Methods 78:351–353. doi:10.1016/j.mimet.2009.06.010

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the anonymous reviewer for the valuable comments on the manuscript. The project was funded by the Carl Trygger Foundation (contract CTS 11: 452) and the Centre for Biological Control (CBC; http://www.slu.se/cbc) at the Swedish University of Agricultural Sciences (SLU).

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Authors and Affiliations

  1. Department of Microbiology, Swedish University of Agricultural Sciences (SLU), Uppsala, Sweden

    Salome Schneider, Tania Tajrin & Ingvar Sundh

  2. Biodiversity and Conservation Biology, Swiss Federal Research Institute WSL, Birmensdorf, Switzerland

    Salome Schneider

  3. Department of Medical Biochemistry and Microbiology (IMBIM), Uppsala University, Uppsala, Sweden

    Jan O. Lundström

  4. Swedish Biological Mosquito Control Project, Nedre Dalälvens Utvecklings AB, Gysinge, Sweden

    Jan O. Lundström

  5. Department of Environmental Science, Aarhus University, Roskilde, Denmark

    Niels B. Hendriksen

  6. Swedish Chemicals Agency, Sundbyberg, Sweden

    Petter Melin

  7. Department of Molecular Sciences, Swedish University of Agricultural Sciences (SLU), Uppsala, Sweden

    Ingvar Sundh

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  1. Salome Schneider
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Correspondence to Salome Schneider.

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Schneider, S., Tajrin, T., Lundström, J.O. et al. Do Multi-year Applications of Bacillus thuringiensis subsp. israelensis for Control of Mosquito Larvae Affect the Abundance of B. cereus Group Populations in Riparian Wetland Soils?. Microb Ecol 74, 901–909 (2017). https://doi.org/10.1007/s00248-017-1004-0

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