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Sex Biased Variance in the Structural and Functional Diversity of the Midgut Bacterial Community of Last Instar Larvae of Pectinophora gossypiella (Lepidoptera: Gelechiidae)

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Abstract

Elucidating the midgut bacterial diversity in an important cotton bollworm Pectinophora gossypiella can be a stepping stone in understanding the possible role of midgut bacteria in field evolved resistance against Bt cotton as well as to commonly used insecticides. Present study targeted metagenomics of 16S rRNA V3-V4 region to understand the influence of sex, if exists, in community diversity of gut microbes vis a vis their function in pink bollworm larvae. The results of the present study revealed that Proteobacteria, Firmicutes, and Actinobacteria were the predominant phyla in the midgut of pink bollworm. Distinctive differences were found in the Shannon and Simpson diversity indices, ChaoI and ACE richness estimates in male and female larvae. The alpha diversity analysis showed that the gut bacteria of male were diverse and rich as compared to that of female. Further, beta diversity analysis indicated that the gut bacterial communities of both larval groups were unique from each other. These findings are the maiden report on sex-based variation in gut bacteria in P. gossypiella larvae. Role of candidate phyla OD1 (Parcubacteria) and TM7 (Saccharibacteria) in the living organisms needs to be studied, and their fairly significant composition in male and negligible composition in female larva raises question on their obvious role. Taxonomic to phenotypic mapping revealed that these gut bacteria play vital role in many metabolic and physiological activities of pink bollworm. Difference in potential functions of gut bacteria also varied with the sex.

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References

  1. Villegas LM, Pimenta PFP (2014) Metagenomics, paratransgenesis and the Anopheles microbiome: A portrait of the geographical distribution of the anopheline microbiota based on a meta-analysis of reported taxa. Mem Inst Oswaldo Cruz 109:672–684

    Article  PubMed  PubMed Central  Google Scholar 

  2. Kikuchi Y, Hayatsu M, Hosokawa T et al (2012) Symbiont-mediated insecticide resistance. PNAS USA 109:8618–8622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Xia X, Gurr GM, Vasseur L et al (2017) Metagenomic sequencing of diamondback moth gut microbiome unveils key holobiont adaptations for herbivory. Front Microbiol 8:663. https://doi.org/10.3389/fmicb.2017.00663

    Article  PubMed  PubMed Central  Google Scholar 

  4. Dillon RJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49:71–92

    Article  CAS  PubMed  Google Scholar 

  5. Engel P, Moran NA (2013) The gut microbiota of insects–diversity in structure and function. FEMS Microbiol Rev 37:699–735

    Article  CAS  PubMed  Google Scholar 

  6. Näpflin K, Schmid-Hempel P (2016) Immune response and gut microbial community structure in bumblebees after microbiota transplants. Proc Royal Soc 283:20160312

    Google Scholar 

  7. Broderick NA, Raffa KF, Goodman RM et al (2004) Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Appl Environ Microbiol 70:293–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Voirol LRP, Frago E, Kaltenpoth M et al (2018) Bacterial symbionts in Lepidoptera: Their diversity, transmission, and impact on the host. Front Microbiol 9:556

    Article  Google Scholar 

  9. Jones AG, Mason CJ, Felton GW et al (2019) Host plant and population source drive diversity of microbial gut communities in two polyphagous insects. Sci Rep 9:2792

    Article  PubMed  PubMed Central  Google Scholar 

  10. Caccia S, Di Lelio I, La Storia A et al (2016) Midgut microbiota and host immunocompetence underlie Bacillus thuringiensis killing mechanism. PNAS USA 113:9486–9491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Broderick NA, Robinson CJ, McMahon MD et al (2009) Contributions of gut bacteria to Bacillus thuringiensis-induced mortality vary across a range of Lepidoptera. BMC Biol 7:11. https://doi.org/10.1186/1741-7007-7-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Hernández-Martínez P, Navarro-Cerrillo G, Caccia S et al (2010) Constitutive activation of the midgut response to Bacillus thuringiensis in Bt-resistant Spodoptera exigua. PLoS One 5:e12795

    Article  PubMed  PubMed Central  Google Scholar 

  13. Xia X, Zheng D, Zhong H et al (2013) DNA sequencing reveals the midgut microbiota of diamondback moth, Plutella xylostella (L.) and a possible relationship with insecticide resistance. PLoS One 8:e68852. https://doi.org/10.1371/journal.pone.0068852

  14. Anon (2020) https://www.statista.com/statistics/263055/cotton-production-worldwide-by-top-countries/ Accessed 5 December 2020

  15. Bambawale OM, Singh A, Sharma OP et al (2004) Performance of Bt cotton (MECH-162) under Integrated Pest Management in farmers’ participatory field trial in Nanded district, Central India. Curr Sci 86:1628–1633

    Google Scholar 

  16. Dhurua S, Gujar GT (2011) Field-evolved resistance to Bt toxin Cry1Ac in the pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), from India. Pest Manag Sci 67:898–903

    Article  CAS  PubMed  Google Scholar 

  17. Naik VC, Kumbhare S, Kranthi S et al (2018) Field-evolved resistance of pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), to transgenic Bacillus thuringiensis (Bt) cotton expressing crystal 1Ac (Cry1Ac) and Cry2Ab in India. Pest Manag Sci 74:2544–2554

    Article  CAS  PubMed  Google Scholar 

  18. Koch H, Schmid-Hempel P (2011) Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. PNAS USA 108:19288–19292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Carriére Y, Ellers-Kirk C, Liu YB et al (2001) Fitness costs and maternal effects associated with resistance to transgenic cotton in the pink bollworm (Lepidoptera: Gelechiidae). J Econ Entomol 94:1571–1576

    Article  PubMed  Google Scholar 

  20. Takahashi S, Tomita J, Nishioka K et al (2014) Development of a prokaryotic universal primer for simultaneous analysis of bacteria and archaea using next-generation sequencing. PLoS ONE 9:e105592. https://doi.org/10.1371/journal.pone.0105592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Bolyen E, Rideout JR, Dillon MR et al (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857. https://doi.org/10.1038/s41587-019-0209-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Dhariwal A, Chong J, Habib S et al (2017) MicrobiomeAnalyst: a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Res 45:W180–W188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Arndt D, Xia J, Li Y et al (2012) METAGENassist: a comprehensive web server for comparative metagenomics. Nucleic Acids Res 40:W88–W95

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Meyer F, Paarmann D, D’Souza M et al (2008) The metagenomics RAST server–a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9:1–8. https://doi.org/10.1186/1471-2105-9-386

    Article  CAS  Google Scholar 

  25. Chen B, Teh BS, Sun C et al (2016) Biodiversity and activity of the gut microbiota across the life history of the insect herbivore Spodoptera littoralis. Sci Rep 6:1–14. https://doi.org/10.1038/srep29505

    Article  CAS  Google Scholar 

  26. Nelson WC, Stegen JC (2015) The reduced genomes of Parcubacteria (OD1) contain signatures of a symbiotic lifestyle. Front Microbiol 6:1415. https://doi.org/10.3389/fmicb.2015.00713

    Article  PubMed  Google Scholar 

  27. Castelle CJ, Brown CT, Thomas BC et al (2017) Unusual respiratory capacity and nitrogen metabolism in a Parcubacterium (OD1) of the Candidate Phyla Radiation. Sci Rep 7:1–12

    Article  Google Scholar 

  28. Yun JH, Roh SW, Whon TW et al (2014) Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Appl Environ Microbiol 80:5254–5264. https://doi.org/10.1128/AEM.01226-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. MsangoSoko K, Gandotra S, Chandel R et al (2020) Composition and diversity of gut bacteria associated with the Eri silk moth, Samia ricini, (Lepidoptera: Saturniidae) as revealed by culture-dependent and metagenomics analysis. J Microbiol Biotechn 30:1367–1378. https://doi.org/10.4014/jmb.2002.02055

    Article  CAS  Google Scholar 

  30. Robinson CJ, Schloss P, Ramos Y et al (2010) Robustness of the bacterial community in the cabbage white butterfly larval midgut. Microb Ecol 59:199–211. https://doi.org/10.1007/s00248-009-9595-8

    Article  PubMed  Google Scholar 

  31. Frankenhuyzen K, van Liu Y, Tonon A (2010) Interactions between Bacillus thuringiensis subsp. kurstaki HD-1 and midgut bacteria in larvae of gypsy moth and spruce budworm. J Invertebr Pathol 103:124–131. https://doi.org/10.1016/j.jip.2009.12.008

    Article  PubMed  Google Scholar 

  32. Lin XL, Pan QJ, Tian HG et al (2015) Bacteria abundance and diversity of different life stages of Plutella xylostella (Lepidoptera: Plutellidae), revealed by bacteria culture-dependent and PCR-DGGE methods. Insect Sci 22:375–385. https://doi.org/10.1111/1744-7917.12079

    Article  CAS  PubMed  Google Scholar 

  33. Tang X, Freitak D, Vogel H et al (2012) Complexity and variability of gut commensal microbiota in polyphagous lepidopteran larvae. PLoS ONE 7:e36978. https://doi.org/10.1371/journal.pone.0036978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Shan Y, Shu C, Crickmore N et al (2014) Cultivable gut bacteria of scarabs (Coleoptera: Scarabaeidae) inhibit Bacillus thuringiensis multiplication. Environ Entomol 43:612–616. https://doi.org/10.1603/EN14028

    Article  CAS  PubMed  Google Scholar 

  35. Gandotra S, Kumar A, Naga K et al (2018) Bacterial community structure and diversity in the gut of the muga silkworm, Antheraea assamensis (Lepidoptera: Saturniidae), from India. Insect Mol Biol 27:603–619. https://doi.org/10.1111/imb.12495

    Article  CAS  PubMed  Google Scholar 

  36. Hadapad AB, Shettigar SK, Hire RS (2019) Bacterial communities in the gut of wild and mass-reared Zeugodacus cucurbitae and Bactrocera dorsalis revealed by metagenomic sequencing. BMC Microbiol 19:1–11. https://doi.org/10.1186/s12866-019-1647-8

    Article  CAS  Google Scholar 

  37. Chen B, Yu T, Xie S et al (2018) Comparative shotgun metagenomic data of the silkworm Bombyx mori gut microbiome. Sci Data 5:1–10

    Article  Google Scholar 

  38. Malhotra J, Dua A, Saxena A et al (2012) Genome sequence of Acinetobacter sp. strain HA, isolated from the gut of the polyphagous insect pest Helicoverpa armigera. J Bacteriol Res 194:5156. https://doi.org/10.1128/JB.01194-12

  39. Ngugi DK, Tsanuo MK, Boga HI (2005) Rhodococcus opacus strain RW, a resorcinol-degrading bacterium from the gut of Macrotermes michaelseni. Afr J Biotechnol 4:839–845

    Google Scholar 

  40. van der Vlugt-Bergmans CJB, van der Werf MJ (2001) Genetic and biochemical characterization of a novel monoterpene eta-lactone hydrolase from Rhodococcus erythropolis DCL14. Appl Environ Microbiol 67:733–741. https://doi.org/10.1128/AEM.67.2.733-741.2001

    Article  PubMed  PubMed Central  Google Scholar 

  41. Opitz S, Kunert G, Gershenzon J (2008) Increased terpenoid accumulation in cotton (Gossypium hirsutum) foliage is a general wound response. J Chem Ecol 34:508–522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Goodfellow M, Williams E (1986) New strategies for the selective isolation of industrially important bacteria. Biotechnol Genet Eng Rev 4:213–262

    Article  CAS  Google Scholar 

  43. Warhurst AM, Fewson CA (1994) Biotransformations catalyzed by the genus Rhodococcus. Crit Rev Biotechnol 14:29–73. https://doi.org/10.3109/07388559409079833

    Article  CAS  PubMed  Google Scholar 

  44. Bell KS, Philp JC, Aw DWJ et al (1998) The genus Rhodococcus. J Appl Microbiol 85:195–210

    Article  CAS  PubMed  Google Scholar 

  45. Chen B, Du K, Sun C et al (2018) Gut bacterial and fungal communities of the domesticated silkworm (Bombyx mori) and wild mulberry-feeding relatives. ISME J 12:2252–2262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Xia X, Sun B, Gurr GM et al (2018) Gut microbiota mediate insecticide resistance in the diamondback moth, Plutella xylostella (L.). Front Microbiol 9:25. https://doi.org/10.3389/fmicb.2018.00025

  47. Vilanova C, Baixeras J, Latorre A et al (2016) The generalist inside the specialist: Gut bacterial communities of two insect species feeding on toxic plants are dominated by Enterococcus sp. Front Microbiol 7:1005

    Article  PubMed  PubMed Central  Google Scholar 

  48. Thakur A, Dhammi P, Saini HS et al (2015) Pathogenicity of bacteria isolated from gut of Spodoptera litura (Lepidoptera: Noctuidae) and fitness costs of insect associated with consumption of bacteria. J Invertebr Pathol 127:38–46

    Article  PubMed  Google Scholar 

  49. Johnston PR, Crickmore N (2009) Gut bacteria are not required for the insecticidal activity of Bacillus thuringiensis toward the tobacco hornworm, Manduca sexta. Appl Environ Microbiol 75:5094–5099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Broderick NA, Raffa KF, Handelsman J (2006) Midgut bacteria required for Bacillus thuringiensis insecticidal activity. PNAS USA 103:15196–15199. https://doi.org/10.1073/pnas.0604865103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

CHS is grateful to the Post Graduate School and Director, Indian Agricultural Research Institute (New Delhi), for providing fellowship to carry out the Ph.D. programme. The authors are grateful to the Director, Indian Agricultural Research Institute, New Delhi, for providing the necessary infrastructure and facilities.

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CHS and VKK designed the project, CHS performed the experiment, PK and AS analyzed the data and interpreted the results. CHS and VKK wrote the manuscript with contributions from PK and AS. All the authors critically read and approved the manuscript.

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Correspondence to Vinay K. Kalia.

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Chaitra, H.S., Singh, A., Pandiyan, K. et al. Sex Biased Variance in the Structural and Functional Diversity of the Midgut Bacterial Community of Last Instar Larvae of Pectinophora gossypiella (Lepidoptera: Gelechiidae). Microb Ecol 83, 1112–1122 (2022). https://doi.org/10.1007/s00248-021-01829-1

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