Cereal leaf beetle-associated bacteria enhance the survival of their host upon insecticide treatments and respond differently to insecticides with different modes of action.

Beata Wielkopolan, Alicja Szabelska-Beręsewicz, Jan Gawor, Aleksandra Obrępalska-Stęplowska
Author Information
  1. Beata Wielkopolan: Department of Monitoring and Signaling of Agrophages, Institute of Plant Protection-National Research Institute, Poznan, Poland. ORCID
  2. Alicja Szabelska-Beręsewicz: Department of Mathematical and Statistical Methods, Poznań University of Life Sciences, Poznan, Poland. ORCID
  3. Jan Gawor: DNA Sequencing and Synthesis Facility, Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Warsaw, Poland. ORCID
  4. Aleksandra Obrępalska-Stęplowska: Department of Molecular Biology and Biotechnology, Institute of Plant Protection-National Research Institute, Poznan, Poland. ORCID

Abstract

The cereal leaf beetle (CLB, Oulema melanopus) is one of the major cereal pests. The effect of insecticides belonging to different chemical classes, with different mechanisms of action and the active substances' concentrations on the CLB bacterial microbiome, was investigated. Targeted metagenomic analysis of the V3-V4 regions of the 16S ribosomal gene was used to determine the composition of the CLB bacterial microbiome. Each of the insecticides caused a decrease in the abundance of bacteria of the genus Pantoea, and an increase in the abundance of bacteria of the genus Stenotrophomonas, Acinetobacter, compared to untreated insects. After cypermethrin application, a decrease in the relative abundance of bacteria of the genus Pseudomonas was noted. The dominant bacterial genera in cypermethrin-treated larvae were Lactococcus, Pantoea, while in insects exposed to chlorpyrifos or flonicamid it was Pseudomonas. Insecticide-treated larvae were characterized, on average, by higher biodiversity and richness of bacterial genera, compared to untreated insects. The depletion of CLB-associated bacteria resulted in a decrease in larval survival, especially after cypermethrin and chlorpyrifos treatments. The use of a metagenome-based functional prediction approach revealed a higher predicted function of bacterial acetyl-CoA C-acetyltransferase in flonicamid and chlorpyrifos-treated larvae and tRNA dimethyltransferase in cypermethrin-treated insects than in untreated insects.

References

  1. PLoS One. 2013 Apr 22;8(4):e61217 [PMID: 23630581]
  2. Nucleic Acids Res. 2023 Jul 5;51(W1):W310-W318 [PMID: 37166960]
  3. Pestic Biochem Physiol. 2020 Nov;170:104666 [PMID: 32980073]
  4. Curr Opin Microbiol. 2018 Jun;43:69-76 [PMID: 29309997]
  5. Planta. 2016 Aug;244(2):313-32 [PMID: 27170360]
  6. Sci Rep. 2018 Feb 1;8(1):2084 [PMID: 29391526]
  7. NPJ Biofilms Microbiomes. 2023 Jan 12;9(1):2 [PMID: 36635299]
  8. J Pest Sci (2004). 2017;90(2):759-771 [PMID: 28275327]
  9. J Econ Entomol. 2001 Jun;94(3):634-9 [PMID: 11425017]
  10. Sci Rep. 2019 Apr 23;9(1):6435 [PMID: 31015559]
  11. Insect Mol Biol. 2014 Oct;23(5):682-93 [PMID: 24974912]
  12. Pest Manag Sci. 2022 Nov;78(11):4802-4808 [PMID: 35904889]
  13. Sci Rep. 2020 Jun 11;10(1):9489 [PMID: 32528116]
  14. Environ Int. 2020 Oct;143:105886 [PMID: 32623217]
  15. Sci Rep. 2021 Oct 14;11(1):20496 [PMID: 34650106]
  16. Acta Trop. 2021 Jan;213:105747 [PMID: 33188748]
  17. Pest Manag Sci. 2023 Dec;79(12):4921-4930 [PMID: 37532920]
  18. J Basic Microbiol. 2016 Feb;56(2):105-19 [PMID: 26837064]
  19. Nat Methods. 2016 Jul;13(7):581-3 [PMID: 27214047]
  20. Genome Biol. 2014;15(12):550 [PMID: 25516281]
  21. Bioinformatics. 2014 Nov 1;30(21):3123-4 [PMID: 25061070]
  22. Sci Rep. 2018 Aug 24;8(1):12755 [PMID: 30143738]
  23. Insects. 2022 Jun 26;13(7): [PMID: 35886759]
  24. AMB Express. 2020 Jun 3;10(1):106 [PMID: 32495133]
  25. Nat Biotechnol. 2020 Jun;38(6):685-688 [PMID: 32483366]
  26. Med Vet Entomol. 1998 Jan;12(1):1-12 [PMID: 9513933]
  27. Sci Rep. 2022 Mar 22;12(1):4919 [PMID: 35318403]
  28. Microbiome. 2021 Mar 28;9(1):76 [PMID: 33775256]
  29. Nucleic Acids Res. 2013 Jan;41(Database issue):D590-6 [PMID: 23193283]
  30. Environ Microbiol Rep. 2024 Apr;16(2):e13247 [PMID: 38644048]
  31. Microb Ecol. 2019 Nov;78(4):995-1013 [PMID: 30915518]
  32. Biom J. 2008 Jun;50(3):346-63 [PMID: 18481363]
  33. Sci Rep. 2021 Jul 13;11(1):14406 [PMID: 34257327]
  34. Curr Opin Insect Sci. 2019 Jun;33:84-90 [PMID: 31358201]
  35. Malar J. 2018 Feb 15;17(1):80 [PMID: 29448925]
  36. Malar J. 2015 Aug 22;14:327 [PMID: 26296644]
  37. Front Microbiol. 2020 Sep 30;11:547108 [PMID: 33101225]
  38. Sci Total Environ. 2020 Nov 25;745:140873 [PMID: 32758760]
  39. PLoS One. 2018 Dec 12;13(12):e0207985 [PMID: 30540788]
  40. PLoS Negl Trop Dis. 2022 Mar 4;16(3):e0010208 [PMID: 35245311]
  41. Arch Microbiol. 2022 Feb 3;204(3):159 [PMID: 35113233]
  42. Saudi J Biol Sci. 2021 Jun;28(6):3214-3224 [PMID: 34121858]
  43. Pest Manag Sci. 2016 Jan;72(1):162-71 [PMID: 25652001]
  44. J Econ Entomol. 2004 Apr;97(2):374-82 [PMID: 15154458]
  45. J Econ Entomol. 2020 Aug 13;113(4):1823-1830 [PMID: 32372086]
  46. Ecotoxicol Environ Saf. 2021 Sep 1;220:112384 [PMID: 34091185]
  47. Front Microbiol. 2022 Sep 14;13:979383 [PMID: 36187965]
  48. Nat Biotechnol. 2019 Aug;37(8):852-857 [PMID: 31341288]

Grants

  1. UMO-2020/37/N/NZ9/02577/Polish National Science Centre

MeSH Term

Animals
Insecticides
Bacteria
Larva
Coleoptera
RNA, Ribosomal, 16S
Microbiota
Metagenomics
Pyrethrins
Chlorpyrifos
Pantoea

Chemicals

Insecticides
RNA, Ribosomal, 16S
Pyrethrins
Chlorpyrifos
cypermethrin

Word Cloud

Created with Highcharts 10.0.0bacterialbacteriainsectsCLBinsecticidesdifferentdecreaseabundancegenusuntreatedlarvaecerealleafactionmicrobiomePantoeacomparedcypermethrinPseudomonasgeneracypermethrin-treatedchlorpyrifosflonicamidhighersurvivaltreatmentsbeetleOulemamelanopusonemajorpestseffectbelongingchemicalclassesmechanismsactivesubstances'concentrationsinvestigatedTargetedmetagenomicanalysisV3-V4regions16SribosomalgeneuseddeterminecompositioncausedincreaseStenotrophomonasAcinetobacterapplicationrelativenoteddominantLactococcusexposedInsecticide-treatedcharacterizedaveragebiodiversityrichnessdepletionCLB-associatedresultedlarvalespeciallyusemetagenome-basedfunctionalpredictionapproachrevealedpredictedfunctionacetyl-CoAC-acetyltransferasechlorpyrifos-treatedtRNAdimethyltransferaseCerealbeetle-associatedenhancehostuponinsecticideresponddifferentlymodes

Similar Articles

Cited By