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Does Host Plant Drive Variation in Microbial Gut Communities in a Recently Shifted Pest?

  • Invertebrate Microbiology
  • Published:
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Abstract

Biotic interactions can modulate the responses of organisms to environmental stresses, including diet changes. Gut microbes have substantial effects on diverse ecological and evolutionary traits of their hosts, and microbial communities can be highly dynamic within and between individuals in space and time. Modulations of the gut microbiome composition and their potential role in the success of a species to maintain itself in a new environment have been poorly studied to date. Here we examine this question in a large wood-boring beetle Cacosceles newmannii (Cerambycidae), that was recently found thriving on a newly colonized host plant. Using 16S metabarcoding, we assessed the gut bacterial community composition of larvae collected in an infested field and in “common garden” conditions, fed under laboratory-controlled conditions on four either suspected or known hosts (sugarcane, tea tree, wattle, and eucalyptus). We analysed microbiome variation (i.e. diversity and differentiation), measured fitness-related larval growth, and studied host plant lignin and cellulose contents, since their degradation is especially challenging for wood-boring insects. We show that sugarcane seems to be a much more favourable host for larval growth. Bacterial diversity level was the highest in field-collected larvae, whereas lab-reared larvae fed on sugarcane showed a relatively low level of diversity but very specific bacterial variants. Bacterial communities were mainly dominated by Proteobacteria, but were significantly different between sugarcane-fed lab-reared larvae and any other hosts or field-collected larvae. We identified changes in the gut microbiome associated with different hosts over a short time frame, which support the hypothesis of a role of the microbiome in host switches.

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Data Availability

Raw data from MiSeq Illumina sequencing of the 426 PCR products were deposited in the Zenodo repository and are available from this link: https://doi.org/10.5281/zenodo.6341252. The literature database on known functions of bacterial genera identified in insects, the growth experimental data on insects, the abundance table of the 100 analysed samples (along with its metadata, taxonomy, and sequences) and the R script for data analysis were deposited in the Cirad data repository (https://dataverse.cirad.fr/) and available from this link: https://doi.org/10.18167/DVN1/4KYM3B.

References 

  1. Frago E, Zytynska S, Fatouros N (2020) Microbial symbionts of herbivorous species across the insect tree. In: Mechanisms underlying microbial symbiosis, K. O. Ed. JA Russell, Éd., Academic Press

  2. Yun J-H, Roh SW, Whon TW, Jung M-J, Kim M-S, Park D-S, Yoon C, Nam Y-D, Kim Y-J, Choi J-H, Kim J-Y, Shin N-R, Kim S-H, Lee W-J, Bae J-W (2014) Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage and phylogeny of host. Appl Environ Habitat Microbiol 80:5254–5264

    Article  Google Scholar 

  3. Kim JM, Choi M, Kim J, Lee SA, Ahn J, Song J, Kim SH, Weon H (2017) Effects of diet type, developmental stage, and gut compartment in the gut bacterial communities of two Cerambycidae species (Coleoptera). Microbial Ecol Environ Microbiol 55:21–30

    CAS  Google Scholar 

  4. 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 

  5. Douglas A (2015) Multiorganismal insects: diversity and function of resident microorganisms. Annu Rev Entomol 60:17–34

    Article  CAS  PubMed  Google Scholar 

  6. Biedermann P, Vega F (2020) Ecology and evolution of insect-fungus mutualisms. Annu Rev Entomol 65:431–455

    Article  CAS  PubMed  Google Scholar 

  7. Duffey SS, Stout MJ (1996) Antinutritive and toxic components of plant defense against insects. Arch Insect Biochem Physiol 32:3–37

    Article  CAS  Google Scholar 

  8. Geib S, Filley T, Hoover K, Hatcher P, Carlson J, del Mar Jimenez-Gasco M, Nakagawa-Izumi A, Sleighter R, Tien M (2008) Lignin degradation in wood-feeding insects. Proc Natl Acad Sci USA 105:12932–12937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Watanabe H, Tokuda G (2010) Cellulolytic systems in insects. Annu Rev Entomol 55:609–632

    Article  CAS  PubMed  Google Scholar 

  10. Hammer TJ, Bowers MD (2015) Gut microbes may facilitate insect herbivory of chemically defended plants. Oecologia 179:1–14

    Article  PubMed  Google Scholar 

  11. Hanks L (1999) Influence of the larval host plant on reproductive strategies of cerambycid beetles. Annu Rev Entomol 44:483–505

  12. Lawrence J (1982) Coleoptera, chez Synopsis and Classification of Living Organisms, 2, S. Parker, Éd, New-York 482–553

  13. Ferreira G (1980) The Parandrinae and the Prioninae of Southern Africa (Cerambycidae, Coleoptera), Bloemfontein, 9300: Memoirs van die Nasionale Museum. Posbus 266:334

    Google Scholar 

  14. Mohammed WS, Ziganshina EE, Shagimardanova EI, Gogoleva NE, Ziganshin AM (2018) Comparison of intestinal bacterial and fungal communities across various xylophagous beetle larvae (Coleoptera: Cerambycidae). Scientific Reports 8:10073

    Article  PubMed  PubMed Central  Google Scholar 

  15. Way M, Conlong D, Rutherford R, Sweby D, Gillespie D, Stranack R, Lagerwall G, Grobbelaar E, Perissinotto et R (2017) Cacosceles (Zelogenes) newmannii (Thomson) (Cerambycidae:Prioninae), a new pest in the South African sugarcane industry, chez Proceedings of the 90th Annual Congress of the South African Sugar Technologists Association, Durban, South Africa

  16. Javal M, Terblanche J, Conlong D, Malan A (2019) First screening of entomopathogenic nematodes and fungus as biocontrol agents against an emerging pest of sugarcane, Cacosceles newmannii (Coleoptera: Cerambycidae). Insects 10:117

    Article  PubMed  PubMed Central  Google Scholar 

  17. Javal M, Thomas S, Lehmann M Barton, Conlong D, Plessis A, Terblanche JS (2019) The effect of oxygen limitation on a xylophagous insect’s heat tolerance is influenced by life-stage through variation in aerobic scope and respiratory anatomy. Front Physiol 10:1426

    Article  PubMed  PubMed Central  Google Scholar 

  18. Smit C, Javal M, Conlong D, Hall G, Terblanche J (2021) Host range determination in a novel outbreak pest of sugarcane, Cacosceles newmannii (Coleoptera: Cerambycidae, Prioninae), inferred from stable isotopes. Agric Forest Entomol 23:378–387

    Article  Google Scholar 

  19. Smit C, Javal M, Lehmann P, Terblanche J (2021) Metabolic responses to starvation and feeding contribute to the invasiveness of an emerging pest insect. J Insect Physiol 128:104162

    Article  CAS  PubMed  Google Scholar 

  20. Javal M, Lehmann P, du Plessis A, Terblanche J (2021) Using µCT in live larvae of a large wood-boring beetle to study tracheal oxygen supply during development. J Insect Physiol 130:104199

    Article  PubMed  Google Scholar 

  21. Dubb A (2016) The rise and decline of small-scale sugarcane production in South Africa: a historical perspective. J Agrar Chang 16

  22. Masarin F, Gurpilhares DB, Baffa DC, Barbosa MH, Carvalho W, Ferraz A, Milagres A (2011) Chemical composition and enzymatic digestability of sugarcane clones selected for varied lignin content. Biotechnol Biofuels 55

  23. Lingle S, Thomson J (2012) Sugarcane internode composition during crop development. Bioenerg Res 5:168–178

    Article  CAS  Google Scholar 

  24. Chaunbi G (1997) Black wattle plantations in South Africa: introduction, silviculture and management, chez Black wattle and its utilisation., Rural Industries Research and Development Corporation Publication No 97/72

  25. Bennett B (2010) The El Dorado of forestry: the Eucalyptus in India, South Africa and Thailand. Inte Rev Soc Hist 55:27–50

    Article  Google Scholar 

  26. Jacobs LEO, Richardson D, Lepschi BJ, Wilson JRU (2017) Quantifying errors and omissions in alien species lists: the introduction status of Melaleuca species in South Africa as a case study. NeoBiota 32:89–105

  27. R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. Retrieved from https://www.r-project.org

  28. McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8:e61217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Oksanen J, Blanchet F, Friendly M, Kindt R, Legendre D McGlinn, Minchin R O’Hara, Simpson G, Solymos M Stevens, Szoecs E, Wagner H (2020) Vegan: community ecology package. R package version 2:5–7

    Google Scholar 

  30. Schliep K (2011) Phangorn: phylogenetic analysis in R. Bioinformatics 27:592–593

    Article  CAS  PubMed  Google Scholar 

  31. Wickham H, Averick M, Bryan J, Chang W, D’Agostino McGowan L, François R, Grolemund G, Hayes A, Henry L, Hester J, Kuhn M, Lin Perdersen T, Miller E, Milton Bache S, Müller K, Ooms J, Robinson D, Paige Seidel D, Spinu V, Takahashi K, Vaughan D, Wilke C, Woo K, Yutani H (2019) Welcome to the tidyverse. J Open Source Softw 4:1686

    Article  Google Scholar 

  32. Kim B, Shin J, Guevarra R, Lee J, Kim D, Seol K, Lee J, Kim H, Isaacson R (2017) Deciphering diversity indices for a better understanding of microbial communities. J Microbiol Biotechnol 27:2089–2093

    Article  PubMed  Google Scholar 

  33. Anderson M (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol :32–46

  34. Legendre P, Legendre L (2012) Numerical Ecology. 3rd English ed. Elsevier

  35. Ramette A (2007) Multivariate analyses in microbial ecology: Multivariate analyses in microbial ecology. FEMS MicrobiologyEcology 62:142–160. https://doi.org/10.1111/j.1574-6941.2007.00375.x

    Article  CAS  Google Scholar 

  36. Astudillo-Garcia C, Bell JJ, Webster N, Glasl B, Jompa J, Montoya J, Taylor M (2017) Evaluating the core microbiota in complex communities: a systematic investigation. Environ Microbiol 19:1450–1462

    Article  PubMed  Google Scholar 

  37. Lu M, Hulcr J, Sun J (2016) The role of symbiotic microbes in insect invasions. An Rev Ecol Evol Syst 47:487–505

    Article  Google Scholar 

  38. Davidowitz G, D’Amico LJ, Nijhout HF (2003) Critical weight in the development of insect body size. Evol Dev 5:188–197

    Article  PubMed  Google Scholar 

  39. Philippot L, Raaijmakers J, Lemanceau P, van der Putten W (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799

    Article  CAS  PubMed  Google Scholar 

  40. Kaltenpoth M (2009) Actinobacteria as mutualists: general healthcare for insects? Trends Microbiol 17:529–535

    Article  CAS  PubMed  Google Scholar 

  41. Erlacher A, Cernava T, Cardinale M, Soh J, Sensen C, Grube M, Berg G (2015) Rhizobiales as functional and endosymbiontic members in the lichen symbiosis of Lobaria pulmonaria L. Front Microbiol 6:53

    Article  PubMed  PubMed Central  Google Scholar 

  42. Wiegand S, Jogler M, Jogler C (2018) On the maverick Planctomycetes. FEMS Microbiol Rev 42:739–760

    Article  CAS  PubMed  Google Scholar 

  43. Yamada Y, Yukphan P (2008) Genera and species in acetic acid bacteria. Int J Food Microbiol 125:15–24

    Article  CAS  PubMed  Google Scholar 

  44. Staudacher H, Kaltenpoth M, Breeuwer J, Menken S, Heckel D, Groot A (2016) Variability of bacterial communities in the Moth Heliothis virescens indicates transient association with the host. PLoS One 11:e0154514

    Article  PubMed  PubMed Central  Google Scholar 

  45. Angzzas S, Ashuvila M, Dayang N (2016) Potential lignin degraders isolated from the gut of Rhynchophorus Ferrugineus., Proceedings of the 2016 International Conference on Mechanics, Materials and Structural Engineering, 66–72

  46. Kamutando C, Vikram S, Kamgan-Nkuekam G, Makhalanyane T, Greve M, Roux J, Richardson D, Cowan D, Valverde A (2017) Soil nutritional status and biogeography influence rhizosphere microbial communities associated with the invasive tree Acacia dealbata. Sci Rep 7:6472

    Article  PubMed  PubMed Central  Google Scholar 

  47. Andreote F, Rossetto R Mendes, Avila L, Labate C, Pizzirani-Kleiner A, JL A, Araújo W (2009) Bacterial community in the rhizosphere and rhizoplane of wild type and transgenic eucalyptus. World J Microbiol Biotechnol 25:1065–1073

    Article  Google Scholar 

  48. Muñoz-Benavent M, Pérez-Cobas A, García-Ferris C, Moya A, Latorre A (2021) Insects’ potential: understanding the functional role of their gut microbiome. J Pharm Biomed Anal 5:113787

    Article  Google Scholar 

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Acknowledgements

The authors thank Denise Gillespie and Nelson Muthusamy for ensuring the survival of the C. newmannii and assisting with larval maintenance. The Entumeni Biosecurity team of SASRI is thanked for collecting the larvae from infested sugarcane fields. The authors thank Bruno Michel for his help and explanations to successfully perform dissection of the larvae. They also thank Enric Frago for his constructive comments on the manuscript.

Funding

This research was supported by funding from the Centre for Invasion Biology and the South African Sugarcane Research Institute. MPC and LB were supported by the Insect Microbiome Project, funded by a CRESI from the French Agricultural Research Centre for International Development (CIRAD).

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Authors and Affiliations

  1. Department of Conservation Ecology & Entomology, Faculty of AgriSciences, Stellenbosch University, Stellenbosch, South Africa

    Marion Javal, John S. Terblanche, Desmond E. Conlong & Chantelle Smit

  2. Current Address: CEFE, Univ Montpellier, CNRS, EPHE, Montpellier, IRD, France

    Marion Javal

  3. CBGP, Cirad, Montpellier SupAgro, INRA, IRD, Univ. Montpellier, Montpellier, France

    Laure Benoit & Marie-Pierre Chapuis

  4. South African Sugarcane Research Institute, Mount Edgecombe, South Africa

    Desmond E. Conlong

  5. Institute for Plant Biotechnology, Department of Genetics, Stellenbosch University, Stellenbosch, South Africa

    James R. Lloyd

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  1. Marion Javal
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  7. Marie-Pierre Chapuis
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Contributions

MJ, JST, and DEC designed the research; JST and DEC secured the funding; MJ and CS conducted the insect sampling and collected insect data; JL collected plant data; LB and MJ produced the molecular work and performed the bioinformatics analyses; MJ carried out the literature survey; MJ and MPC performed the statistical analyses; MJ and MPC drafted the manuscript. All authors read and approved the final version.

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Correspondence to Marion Javal.

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Javal, M., Terblanche, J.S., Benoit, L. et al. Does Host Plant Drive Variation in Microbial Gut Communities in a Recently Shifted Pest?. Microb Ecol 86, 636–646 (2023). https://doi.org/10.1007/s00248-022-02100-x

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