Host plant and population source drive diversity of microbial gut communities in two polyphagous insects (2024)

References

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

    Article CAS Google Scholar

  2. Pontes, M. H. & Dale, C. Culture and manipulation of insect facultative symbionts. Trends Microbiol. 14, 406–412 (2006).

    Article CAS Google Scholar

  3. Salem, H., Florez, L., Gerardo, N. & Kaltenpoth, M. An out-of-body experience: the extracellular dimension for the transmission of mutualistic bacteria in insects. Proc. R. Soc. B Biol. Sci. 282, 20142957 (2015).

    Article Google Scholar

  4. Mason, C. J., Jones, A. G. & Felton, G. W. Co-option of microbial associates by insects and their impact on plant–folivore interactions. Plant Cell Environ. 0 (2018).

  5. Kikuchi, Y., Hosokawa, T. & f*ckatsu, T. Insect-microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl. Environ. Microbiol. 73, 4308–4316 (2007).

    Article CAS Google Scholar

  6. Caspi-Fluger, A. et al. Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. Proc. R. Soc. B Biol. Sci. 279, 1791 (2012).

    Article CAS Google Scholar

  7. Gonella, E. et al. Horizontal transmission of the symbiotic bacterium Asaia sp. in the leafhopper Scaphoideus titanus Ball (Hemiptera: Cicadellidae). BMC Microbiol. 12, S4 (2012).

    Article Google Scholar

  8. Dillon, R. J. & Dillon, V. M. The gut bacteria of insects: nonpathogenic interactions. Annu. Rev. Entomol. 49, 71–92 (2004).

    Article CAS Google Scholar

  9. Kaufman, M. G. & Klug, M. J. The contribution of hindgut bacteria to dietary carbohydrate utilization by crickets (Orthoptera: Gryllidae). Comp. Biochem. Physiol. A Physiol. 98, 117–123 (1991).

    Article Google Scholar

  10. Salem, H. et al. Drastic genome reduction in an herbivore’s pectinolytic symbiont. Cell 171, 1520–1531.e13 (2017).

    Article CAS Google Scholar

  11. Salem, H. et al. Vitamin supplementation by gut symbionts ensures metabolic homeostasis in an insect host. Proc. R. Soc. B Biol. Sci. 281, 20141838 (2014).

    Article Google Scholar

  12. Scully, E. D. et al. Functional genomics and microbiome profiling of the Asian longhorned beetle (Anoplophora glabripennis) reveal insights into the digestive physiology and nutritional ecology of wood feeding beetles. BMC Genomics 15, 1096 (2014).

    Article Google Scholar

  13. Hu, Y. et al. Herbivorous turtle ants obtain essential nutrients from a conserved nitrogen-recycling gut microbiome. Nat. Commun. 9, 964 (2018).

    Article ADS Google Scholar

  14. Mason, C. J., Couture, J. J. & Raffa, K. F. Plant-associated bacteria degrade defense chemicals and reduce their adverse effects on an insect defoliator. Oecologia 175, 901–910 (2014).

    Article ADS Google Scholar

  15. Ceja-Navarro, J. A. et al. Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee. Nat. Commun. 6, 7618 (2015).

    Article CAS Google Scholar

  16. Welte, C. U. et al. Plasmids from the gut microbiome of cabbage root fly larvae encode SaxA that catalyses the conversion of the plant toxin 2-phenylethyl isothiocyanate. Environ. Microbiol. 18, 1379–1390 (2016).

    Article CAS Google Scholar

  17. Chung, S. H. et al. Herbivore exploits orally secreted bacteria to suppress plant defenses. Proc. Natl. Acad. Sci. 110, 15728–15733 (2013).

    Article ADS CAS Google Scholar

  18. Wang, J. et al. Herbivore oral secreted bacteria trigger distinct defense responses in preferred and non-preferred host plants. J. Chem. Ecol. 42, 463–474 (2016).

    Article CAS Google Scholar

  19. Dow, J. A. Insect midgut function. in Advances in Insect Physiology (eds Evans, P. D. & Wigglesworth, V. B.) 19, 187–328 (Academic Press, 1987).

  20. Harrison, J. F. Insect acid-base physiology. Annu. Rev. Entomol. 46, 221–250 (2001).

    Article CAS Google Scholar

  21. Appel, H. M. & Martin, M. M. Gut redox conditions in herbivorous lepidopteran larvae. J. Chem. Ecol. 16, 3277–3290 (1990).

    Article CAS Google Scholar

  22. Johnson, K. S. & Felton, G. W. Physiological and dietary influences on midgut redox conditions in generalist lepidopteran larvae. J. Insect Physiol. 42, 191–198 (1996).

    Article CAS Google Scholar

  23. Broderick, N. A., Raffa, K. F., Goodman, R. M. & Handelsman, J. Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Appl. Environ. Microbiol. 70, 293–300 (2004).

    Article CAS Google Scholar

  24. Tang, X. et al. Complexity and variability of gut commensal microbiota in polyphagous lepidopteran larvae. Plos One 7, e36978 (2012).

    Article ADS CAS Google Scholar

  25. Chen, B. et al. Biodiversity and activity of the gut microbiota across the life history of the insect herbivore Spodoptera littoralis. Sci. Rep. 6, 29505 (2016).

    Article ADS CAS Google Scholar

  26. Xiang, H. et al. Microbial communities in the larval midgut of laboratory and field populations of cotton bollworm (Helicoverpa armigera). Can. J. Microbiol. 52, 1085–1092 (2006).

    Article CAS Google Scholar

  27. Chaturvedi, S., Rego, A., Lucas, L. K. & Gompert, Z. Sources of variation in the gut microbial community of Lycaeides melissa caterpillars. Sci. Rep. 7, 11335 (2017).

    Article ADS Google Scholar

  28. Mason, C. J. & Raffa, K. F. Acquisition and structuring of midgut bacterial communities in gypsy moth (Lepidoptera: Erebidae) larvae. Environ. Entomol. 43, 595–604 (2014).

    Article Google Scholar

  29. Staudacher, H. et al. Variability of bacterial communities in the moth Heliothis virescens indicates transient association with the host. Plos One 11, e0154514 (2016).

    Article Google Scholar

  30. Acevedo, F. E. et al. Fall armyworm-associated gut bacteria modulate plant defense responses. Mol. Plant. Microbe Interact (2017).

  31. Stokstad, E. New crop pest takes Africa at lightning speed. Science 356, 473 (2017).

    Article ADS CAS Google Scholar

  32. Goergen, G., Kumar, P. L., Sankung, S. B., Togola, A. & Tamò, M. First report of outbreaks of the fall armyworm Spodoptera frugiperda (J. E. Smith) (Lepidoptera, Noctuidae), a new alien invasive pest in west and central Africa. Plos One 11, e0165632 (2016).

    Article Google Scholar

  33. Nagoshi, R. N., Meagher, R. L. & Hay-Roe, M. Inferring the annual migration patterns of fall armyworm (Lepidoptera: Noctuidae) in the United States from mitochondrial haplotypes. Ecol. Evol. 2, 1458–1467 (2012).

    Article Google Scholar

  34. Silva, D. M. da et al. Biology and nutrition of Spodoptera frugiperda (Lepidoptera: Noctuidae) fed on different food sources. Sci. Agric. 74, 18–31 (2017).

    Article Google Scholar

  35. Bentivenha, J. P. F. et al. Battle in the New World: Helicoverpa armigera versus Helicoverpa zea (Lepidoptera: Noctuidae). Plos One 11, e0167182 (2016).

    Article Google Scholar

  36. Reisig, D., Suits, R., Burrack, H., Bacheler, J. & Dunphy, J. E. Does florivory by Helicoverpa zea (Lepidoptera: Noctuidae) cause yield loss in soybeans? J. Econ. Entomol. 110, 464–470 (2017).

    Article Google Scholar

  37. Priya, N. G., Ojha, A., Kajla, M. K., Raj, A. & Rajagopal, R. Host plant induced variation in gut bacteria of Helicoverpa armigera. PLoS One 7, e30768 (2012).

    Article Google Scholar

  38. Hammer, T. J., Janzen, D. H., Hallwachs, W., Jaffe, S. L. & Fierer, N. Caterpillars lack a resident gut microbiome. Proc. Natl. Acad. Sci. USA 114, 9641–9646 (2017).

    Article CAS Google Scholar

  39. Appel, H. M. The chewing herbivore gut lumen: physicochemical conditions and their impact on plant nutrients, allelochemicals and insect pathogens. In Insect-Plant Interactions (ed. Bernays, E. A.) 5, 209–221 (CRC Press, 1994).

  40. Visôtto, L. E., Oliveira, M. G. A., Guedes, R. N. C., Ribon, A. O. B. & Good-God, P. I. V. Contribution of gut bacteria to digestion and development of the velvetbean caterpillar, Anticarsia gemmatalis. J. Insect Physiol. 55, 185–191 (2009).

    Article Google Scholar

  41. Douglas, A. E. Microbial brokers of insect-plant interactions. in Proceedings of the 8th International Symposium on Insect-Plant Relationships (eds. Menken, S. B. J., Visser, J. H. & Harrewijn, P.) 329–336 (Springer Netherlands, 1992).

  42. Caccia, S. et al. Midgut microbiota and host immunocompetence underlie Bacillus thuringiensis killing mechanism. Proc. Natl. Acad. Sci. 113, 9486 (2016).

    Article CAS Google Scholar

  43. Broderick, N. A., Raffa, K. F. & Handelsman, J. Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proc. Natl. Acad. Sci. 103, 15196 (2006).

    Article ADS CAS Google Scholar

  44. Jakubowska, A. K., Vogel, H. & Herrero, S. Increase in gut microbiota after immune suppression in baculovirus-infected larvae. Plos Pathog. 9, e1003379 (2013).

    Article CAS Google Scholar

  45. Mikaelyan, A., Thompson, C. L., Hofer, M. J. & Brune, A. Deterministic assembly of complex bacterial communities in guts of germ-free co*ckroaches. Appl. Environ. Microbiol. 82, 1256–1263 (2016).

    Article CAS Google Scholar

  46. Byeon, J. H. et al. A specific cathepsin-L-like protease purified from an insect midgut shows antibacterial activity against gut symbiotic bacteria. Dev. Comp. Immunol. 53, 79–84 (2015).

    Article CAS Google Scholar

  47. Futahashi, R. et al. Gene expression in gut symbiotic organ of stinkbug affected by extracellular bacterial symbiont. Plos One 8, e64557 (2013).

    Article ADS CAS Google Scholar

  48. Ohbayashi, T. et al. Insect’s intestinal organ for symbiont sorting. Proc. Natl. Acad. Sci. USA 112, E5179–E5188 (2015).

    Article CAS Google Scholar

  49. Näpflin, K. & Schmid-Hempel, P. Host effects on microbiota community assembly. J. Anim. Ecol. 87, 331–340 (2017).

    Article Google Scholar

  50. Chung, S. H. et al. Host plant species determines symbiotic bacterial community mediating suppression of plant defenses. Sci. Rep. 7, 39690 (2017).

    Article ADS CAS Google Scholar

  51. Lindow, S. E. & Brandl, M. T. Microbiology of the phyllosphere. Appl. Environ. Microbiol. 69, 1875–1883 (2003).

    Article CAS Google Scholar

  52. Mason, C. J., Rubert-Nason, K. F., Lindroth, R. L. & Raffa, K. F. Aspen defense chemicals influence midgut bacterial community composition of gypsy moth. J. Chem. Ecol. 41, 75–84 (2015).

    Article CAS Google Scholar

  53. Knief, C., Ramette, A., Frances, L., Alonso-Blanco, C. & Vorholt, J. A. Site and plant species are important determinants of the Methylobacterium community composition in the plant phyllosphere. Isme J. 4, 719 (2010).

    Article CAS Google Scholar

  54. Rastogi, G. et al. Leaf microbiota in an agroecosystem: spatiotemporal variation in bacterial community composition on field-grown lettuce. ISME J. 6, 1812–1822 (2012).

    Article CAS Google Scholar

  55. Appel, H. M. & Maines, L. W. The influence of host plant on gut conditions of gypsy moth (Lymantria dispar) caterpillars. J. Insect Physiol. 41, 241–246 (1995).

    Article ADS CAS Google Scholar

  56. Dow, J. A. pH gradients in the lepidopteran midgut. J. Exp. Biol. 172, 355 (1992).

    CAS PubMed Google Scholar

  57. Teh, B.-S., Apel, J., Shao, Y. & Boland, W. Colonization of the intestinal tract of the polyphagous pest Spodoptera littoralis with the GFP-tagged indigenous gut bacterium Enterococcus mundtii. Front. Microbiol. 7, 928 (2016).

    Article Google Scholar

  58. Gedling, C. R., Smith, C. M., LeMoine, C. M. R. & Cassone, B. J. The Mexican bean beetle (Epilachna varivestis) regurgitome and insights into beetle-borne virus specificity. Plos One 13, e0192003 (2018).

    Article Google Scholar

  59. Engel, P. & Moran, N. A. The gut microbiota of insects – diversity in structure and function. FEMS Microbiol. Rev. 37, 699–735 (2013).

    Article CAS Google Scholar

  60. Větrovský, T. & Baldrian, P. The variability of the 16S rRNA gene in bacterial genomes and its consequences for bacterial community analyses. Plos One 8, e57923 (2013).

    Article ADS Google Scholar

  61. Chakravorty, S., Helb, D., Burday, M., Connell, N. & Alland, D. A detailed analysis of 16S ribosomal RNA gene segments for the diagnosis of pathogenic bacteria. J. Microbiol. Methods 69, 330–339 (2007).

    Article CAS Google Scholar

  62. Jovel, J. et al. Characterization of the gut microbiome using 16S or shotgun metagenomics. Front. Microbiol. 7, 459 (2016).

    Article Google Scholar

  63. Chen, W. P. & Kuo, T. T. A simple and rapid method for the preparation of gram-negative bacterial genomic DNA. Nucleic Acids Res. 21, 2260 (1993).

    Article ADS CAS Google Scholar

  64. Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261–5267 (2007).

    Article CAS Google Scholar

  65. Cole, R. J. et al. Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. D633–D642, https://doi.org/10.1093/nar/gkt1244 (2014).

  66. Kumar, S., Stecher, G. & Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874 (2016).

    Article CAS Google Scholar

  67. Jukes, T. H. & Cantor, C. R. Evolution of protein molecules. In Mammalian Protein Metabolism 21–132 (Academic Press, 1969).

  68. Caporaso, J. G. et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6, 1621–1624 (2012).

    Article CAS Google Scholar

  69. Schloss, P. D. et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537–41 (2009).

    Article CAS Google Scholar

Download references

Host plant and population source drive diversity of microbial gut communities in two polyphagous insects (2024)
Top Articles
Latest Posts
Article information

Author: Dr. Pierre Goyette

Last Updated:

Views: 5964

Rating: 5 / 5 (50 voted)

Reviews: 89% of readers found this page helpful

Author information

Name: Dr. Pierre Goyette

Birthday: 1998-01-29

Address: Apt. 611 3357 Yong Plain, West Audra, IL 70053

Phone: +5819954278378

Job: Construction Director

Hobby: Embroidery, Creative writing, Shopping, Driving, Stand-up comedy, Coffee roasting, Scrapbooking

Introduction: My name is Dr. Pierre Goyette, I am a enchanting, powerful, jolly, rich, graceful, colorful, zany person who loves writing and wants to share my knowledge and understanding with you.