Impact of transgenerational host switch on gut bacterial assemblage in generalist pest, Spodoptera littoralis (Lepidoptera: Noctuidae)

. 2023 ; 14 () : 1172601. [epub] 20230713

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37520373

Diet composition is vital in shaping gut microbial assemblage in many insects. Minimal knowledge is available about the influence of transgenerational diet transition on gut microbial community structure and function in polyphagous pests. This study investigated transgenerational diet-induced changes in Spodoptera littoralis larval gut bacteriome using 16S ribosomal sequencing. Our data revealed that 88% of bacterial populations in the S. littoralis larval gut comprise Proteobacteria, Firmicutes, Actinobacteria, and Bacteroidetes. The first diet transition experiment from an artificial diet (F0) to a plant diet (F1), cabbage and cotton, caused an alteration of bacterial communities in the S. littoralis larval gut. The second transgenerational diet switch, where F1 larvae feed on the same plant in the F2 generation, displayed a significant variation suggesting further restructuring of the microbial communities in the Spodoptera larval gut. F1 larvae were also challenged with the plant diet transition at the F2 generation (cabbage to cotton or cotton to cabbage). After feeding on different plant diets, the microbial assemblage of F2 larvae pointed to considerable differences from other F2 larvae that continued on the same diet. Our results showed that S. littoralis larval gut bacteriome responds rapidly and inexplicably to different diet changes. Further experiments must be conducted to determine the developmental and ecological consequences of such changes. Nevertheless, this study improves our perception of the impact of transgenerational diet switches on the resident gut bacteriome in S. littoralis larvae and could facilitate future research to understand the importance of symbiosis in lepidopteran generalists better.

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Anderson M. J. (2014). “Permutational multivariate analysis of variance (PERMANOVA),” in Wiley Statsref: Statistics Reference Online 1–15.

Appel H. M. (2017). “The chewing herbivore gut lumen: physicochemical conditions and their impact on plant nutrients, allelochemicals, and insect pathogens,” in Insect-Plant Interactions (CRC Press: ) 209–224.

Arbuthnott D., Levin T. C., Promislow D. E. (2016). The impacts of Wolbachia and the microbiome on mate choice in Drosophila melanogaster. J. Evol. Biol. 29, 461–468. 10.1111/jeb.12788 PubMed DOI PMC

Atyame C. M., Labbé P., Lebon C., Weill M., Moretti R., Marini F., et al. (2016). Comparison of irradiation and wolbachia based approaches for sterile-male strategies targeting aedes albopictus. PLoS ONE 11, e0146834. 10.1371/journal.pone.0146834 PubMed DOI PMC

Baumann P., Moran N. A., Baumann L. (2006). “Bacteriocyte-Associated Endosymbionts of Insects,” in The Prokaryotes: Volume 1: Symbiotic associations, Biotechnology, Applied Microbiology, eds. M., Dworkin, S., Falkow, E., Rosenberg, K.-H., Schleifer, E., Stackebrandt. (New York, NY: Springer New York; ) 403–438. 10.1007/0-387-30741-9_16 DOI

Bras A., Roy A., Heckel D. G., Anderson P., Karlsson Green K. (2022). Pesticide resistance in arthropods: Ecology matters too. Ecol. Lett. 25, 1746–1759. 10.1111/ele.14030 PubMed DOI PMC

Caporaso J. G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F. D., Costello E. K., et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336. 10.1038/nmeth.f.303 PubMed DOI PMC

Caragata E. P., Walker T. (2012). Using bacteria to treat diseases. Expert. Opin. Biol. Ther. 12, 701–712. 10.1517/14712598.2012.677429 PubMed DOI

Cardé R. T., Minks A. K. (1995). Control of Moth Pests by Mating Disruption: Successes and Constraints. Ann. Rev. Entomol. 40, 559–585. 10.1146/annurev.en.40.010195.003015 DOI

Carter V., Underhill A., Baber I., Sylla L., Baby M., Larget-Thiery I., et al. (2013). Killer bee molecules: antimicrobial peptides as effector molecules to target sporogonic stages of Plasmodium. PLoS Pathog. 9, e1003790. 10.1371/journal.ppat.1003790 PubMed DOI PMC

Caspi-Fluger A., Inbar M., Mozes-Daube N., Katzir N., Portnoy V., Belausov E., et al. (2012). Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. Proc. R. Soc. B. 279, 1791–1796. 10.1098/rspb.2011.2095 PubMed DOI PMC

Chakraborty A., Ashraf M. Z., Modlinger R., Synek J., Schlyter F., Roy A. (2020). Unravelling the gut bacteriome of Ips (Coleoptera: Curculionidae: Scolytinae): identifying core bacterial assemblage and their ecological relevance. Scient. Rep. 10, 18572. 10.1038/s41598-020-75203-5 PubMed DOI PMC

Chakraborty A., Roy A. (2021). “Microbial influence on plant–insect interaction,” in Plant-pest interactions: from molecular mechanisms to chemical ecology (Springer: ) 337–363. 10.1007/978-981-15-2467-7_14 DOI

Chakraborty A., Zádrapová D., Dvorák J., Faltinová Z., Zacek P., Cajthaml T., et al. (2023). Impact of 30-year precipitation regime differences on forest soil physiology and microbial assemblages. Front. Forests Global Change 6, 1142979. 10.3389/ffgc.2023.1142979 DOI

Chen B., Mason C. J., Peiffer M., Zhang D., Shao Y., Felton G. W. (2022). Enterococcal symbionts of caterpillars facilitate the utilization of a suboptimal diet. J. Insect Physiol. 138, 104369. 10.1016/j.jinsphys.2022.104369 PubMed DOI

Chen B., Teh B.-S., Sun C., Hu S., Lu X., Boland W., et al. (2016). Biodiversity and activity of the gut microbiota across the life history of the insect herbivore PubMed DOI PMC

Chen B., Xie S., Zhang X., Zhang N., Feng H., Sun C., et al. (2020). Gut microbiota metabolic potential correlates with body size between mulberry-feeding lepidopteran pest species. Pest Manage. Sci. 76, 1313–1323. 10.1002/ps.5642 PubMed DOI

Chen S., Bagdasarian M., Walker E. D. (2015). Elizabethkingia anophelis: molecular manipulation and interactions with mosquito hosts. Appl. Envir. Microbiol. 81, 2233–2243. 10.1128/AEM.03733-14 PubMed DOI PMC

Chen Y., Zhou H., Lai Y., Chen Q., Yu X.-Q., Wang X. (2021). Gut microbiota dysbiosis influences metabolic homeostasis in PubMed DOI PMC

Chrostek E., Pelz-Stelinski K., Hurst G. D., Hughes G. L. (2017). Horizontal transmission of intracellular insect symbionts via plants. Front. Microbiol. 8, 2237. 10.3389/fmicb.2017.02237 PubMed DOI PMC

Coon K. L., Vogel K. J., Brown M. R., Strand M. R. (2014). Mosquitoes rely on their gut microbiota for development. Molec. Ecol. 23, 2727–2739. 10.1111/mec.12771 PubMed DOI PMC

Delacre M., Lakens D., Leys C. (2017). Why psychologists should by default use Welch's DOI

Douglas A. E. (2015). Multiorganismal insects: diversity and function of resident microorganisms. Annu. Rev. Entomol. 60, 17–34. 10.1146/annurev-ento-010814-020822 PubMed DOI PMC

Douglas G. M., Maffei V. J., Zaneveld J. R., Yurgel S. N., Brown J. R., Taylor C. M., et al. (2020). PICRUSt2 for prediction of metagenome functions. Nat. Biotechnol. 38, 685–688. 10.1038/s41587-020-0548-6 PubMed DOI PMC

Dow J. (1984). Extremely high pH in biological systems: a model for carbonate transport. Am. J. Physiol. Regul. Integr. Compar. Physiol. 246, R633–R636. 10.1152/ajpregu.1984.246.4.R633 PubMed DOI

El Khoury S., Giovenazzo P., Derome N. (2022). Endogenous honeybee gut microbiota metabolize the pesticide clothianidin. Microorganisms 10, 493. 10.3390/microorganisms10030493 PubMed DOI PMC

Engl T., Kaltenpoth M. (2018). Influence of microbial symbionts on insect pheromones. Nat. Prod. Rep. 35, 386–397. 10.1039/C7NP00068E PubMed DOI

Flury P., Aellen N., Ruffner B., Péchy-Tarr M., Fataar S., Metla Z., et al. (2016). Insect pathogenicity in plant-beneficial pseudomonads: phylogenetic distribution and comparative genomics. ISME J. 10, 2527–2542. 10.1038/ismej.2016.5 PubMed DOI PMC

Gaden S., Robinson P. R. A., Ian J., Kitching G. W., Beccaloni L., Hernández M. (2010). HOSTS – A Database of the World's Lepidopteran Hostplants. London: Natural History Museum.

Gayatri Priya N., Ojha A., Kajla M. K., Raj A., Rajagopal R. (2012). Host plant induced variation in gut bacteria of Helicoverpa armigera. PLoS ONE 7, e30768. 10.1371/journal.pone.0030768 PubMed DOI PMC

Guannan L. (2020). The physiological and toxicological effects of antibiotics on an interspecies insect model. Chemosphere 248, 126019–126248. 10.1016/j.chemosphere.2020.126019 PubMed DOI

Gupta A., Nair S. (2020). Dynamics of insect–microbiome interaction influence host and microbial symbiont. Front. Microbiol. 11, 01357. 10.3389/fmicb.2020.01357 PubMed DOI PMC

Gurung K., Wertheim B., Falcao Salles J. (2019). The microbiome of pest insects: it is not just bacteria. Entomol. Exper. Applic. 167, 156–170. 10.1111/eea.12768 DOI

Hammer T. J., Janzen D. H., Hallwachs W., Jaffe S. P., Fierer N. (2017). Caterpillars lack a resident gut microbiome. Proc. Nat. Acad. Sci. 114, 9641–9646. 10.1073/pnas.1707186114 PubMed DOI PMC

Hansen T. E., Enders L. S. (2022). Host plant species influences the composition of milkweed and monarch microbiomes. Front. Microbiol. 13, 840078–840078. 10.3389/fmicb.2022.840078 PubMed DOI PMC

Harwood C. S., Parales R. E. (1996). The β-ketoadipate pathway and the biology of self-identity. Ann. Rev. Microbiol. 50, 553–590. 10.1146/annurev.micro.50.1.553 PubMed DOI

Hinks C. F., Byers J. R. (1976). Biosystematics of the genus Euxoa (Lepidoptera: Noctuidae). V. Rearing procedures, and life cycles of 36 species. Canad. Entomol. 108, 12. 10.4039/Ent1081345-12 DOI

Hu L., Sun Z., Xu C., Wang J., Mallik A. U., Gu C., et al. (2022). High nitrogen in maize enriches gut microbiota conferring insecticide tolerance in lepidopteran pest PubMed DOI PMC

Ibarra-Juarez L. A., Burton M., Biedermann P., Cruz L., Desgarennes D., Ibarra-Laclette E., et al. (2020). Evidence for succession and putative metabolic roles of fungi and bacteria in the farming mutualism of the ambrosia beetle Xyleborus affinis. Msystems 5, e00541–e00520. 10.1128/mSystems.00541-20 PubMed DOI PMC

Itoh H., Tago K., Hayatsu M., Kikuchi Y. (2018). Detoxifying symbiosis: microbe-mediated detoxification of phytotoxins and pesticides in insects. Natur. Product Rep. 35, 434–454. 10.1039/C7NP00051K PubMed DOI

Jing T. Z., Qi F. H., Wang Z. Y. (2020). Most dominant roles of insect gut bacteria: digestion, detoxification, or essential nutrient provision? Microbiome 8, 38. 10.1186/s40168-020-00823-y PubMed DOI PMC

Joga M. R., Mogilicherla K., Smagghe G., Roy A. (2021). RNA interference-based forest protection products (FPPs) against wood-boring coleopterans: Hope or hype? Front. Plant Sci. 12, 733608. 10.3389/fpls.2021.733608 PubMed DOI PMC

Jones A. G., Mason C. J., Felton G. W., Hoover K. (2019). Host plant and population source drive diversity of microbial gut communities in two polyphagous insects. Scient. Rep. 9, 1–11. 10.1038/s41598-019-39163-9 PubMed DOI PMC

Kaltenpoth M., Flórez L. V. (2020). Versatile and Dynamic Symbioses Between Insects and Burkholderia Bacteria. Ann. Rev. Entomol. 65, 145–170. 10.1146/annurev-ento-011019-025025 PubMed DOI

Kämpfer P., Chandel K., Prasad G., Shouche Y., Veer V. (2010). Chryseobacterium culicis sp. nov., isolated from the midgut of the mosquito Culex quinquefasciatus. Int. J. System. Evolut. Microbiol. 60, 2387–2391. 10.1099/ijs.0.019794-0 PubMed DOI

Kanehisa M., Furumichi M., Tanabe M., Sato Y., Morishima K. (2017). KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucl. Acids Res. 45, D353–D361. 10.1093/nar/gkw1092 PubMed DOI PMC

Koga R., Moriyama M., Onodera-Tanifuji N., Ishii Y., Takai H., Mizutani M., et al. (2022). Single mutation makes Escherichia coli an insect mutualist. bioRxiv. 10.1038/s41564-022-01179-9 PubMed DOI PMC

Lei X., Li Y., Chen Z., Zheng W., Lai Q., Zhang H., et al. (2014). Altererythrobacter xiamenensis sp. nov., an algicidal bacterium isolated from red tide seawater. Int. J. System. Evolut. Microbiol. 64, 631–637. 10.1099/ijs.0.057257-0 PubMed DOI

Lhomme P., Carrasco D., Larsson M., Hansson B., Anderson P. (2018). A context-dependent induction of natal habitat preference in a generalist herbivorous insect. Behav. Ecol. 29, 360–367. 10.1093/beheco/arx173 DOI

Li S.-J., Ahmed M. Z., Lv N., Shi P.-Q., Wang X.-M., Huang J.-L., et al. (2017). Plantmediated horizontal transmission of Wolbachia between whiteflies. ISME J. 11, 1019–1028. 10.1038/ismej.2016.164 PubMed DOI PMC

Liu F., Ye F., Cheng C., Kang Z., Kou H., Sun J. (2022). Symbiotic microbes aid host adaptation by metabolizing a deterrent host pine carbohydrate d-pinitol in a beetle-fungus invasive complex. Sci. Adv. 8, eadd5051. 10.1126/sciadv.add5051 PubMed DOI PMC

Lozupone C. A., Hamady M., Kelley S. T., Knight R. (2007). Quantitative and qualitative β diversity measures lead to different insights into factors that structure microbial communities. Appl. Environ. Microbiol. 73, 1576–1585. 10.1128/AEM.01996-06 PubMed DOI PMC

Lv D., Liu X., Dong Y., Yan Z., Zhang X., Wang P., et al. (2021). Comparison of gut bacterial communities of fall armyworm ( PubMed DOI PMC

Malacrinò A. (2022). Host species identity shapes the diversity and structure of insect microbiota. Molec. Ecol. 31, 723–735. 10.1111/mec.16285 PubMed DOI

Malhotra J., Dua A., Saxena A., Sangwan N., Mukherjee U., Pandey N., et al. (2012). Genome sequence of Acinetobacter sp. strain HA, isolated from the gut of the polyphagous insect pest Helicoverpa armigera. Am. Soc. Microbiol. 194, 12. 10.1128/JB.01194-12 PubMed DOI PMC

Martínez-Solís M., Collado M. C., Herrero S. (2020). Influence of diet, sex, and viral infections on the gut microbiota composition of spodoptera exigua caterpillars. Front. Microbiol. 11, 753. 10.3389/fmicb.2020.00753 PubMed DOI PMC

Mason C. J., Lowe-Power T. M., Rubert-Nason K. F., Lindroth R. L., Raffa K. F. (2016). Interactions between bacteria and aspen defense chemicals at the phyllosphere–herbivore interface. J. Chem. Ecol. 42, 193–201. 10.1007/s10886-016-0677-z PubMed DOI

Mason C. J., Peiffer M., Chen B., Hoover K., Felton G. W. (2022). Opposing growth responses of lepidopteran larvae to the establishment of gut microbiota. Microbiol. Spiectr. 10, e01941–01922. 10.1128/spectrum.01941-22 PubMed DOI PMC

Mason C. J., St. Clair A., Peiffer M., Gomez E., Jones A. G., Felton G. W., et al. (2020). Diet influences proliferation and stability of gut bacterial populations in herbivorous lepidopteran larvae. PLoS ONE 15, e0229848. 10.1371/journal.pone.0229848 PubMed DOI PMC

Mazumdar T., Teh B. S., Murali A., Schmidt-Heck W., Schlenker Y., Vogel H., et al. (2021). Transcriptomics reveal the survival strategies of Enterococcus mundtii in the gut of Spodoptera littoralis. J. Chem. Ecol. 47, 227–241. 10.1007/s10886-021-01246-1 PubMed DOI

McKight P. E., Najab J. (2010). “Kruskal-wallis test,” in The Corsini Encyclopedia of Psychology 1. 10.1002/9780470479216.corpsy0491 DOI

Moran N. A., Yun Y. (2015). Experimental replacement of an obligate insect symbiont. Proc. Natl. Acad. Sci. U S A. 112, 2093–2096. 10.1073/pnas.1420037112 PubMed DOI PMC

Mundt J. O. (1982). The ecology of the streptococci. Microbial. Ecol. 8, 355–369. 10.1007/BF02010675 PubMed DOI

Nardi J. B., Mackie R. I., Dawson J. O. (2002). Could microbial symbionts of arthropod guts contribute significantly to nitrogen fixation in terrestrial ecosystems? J. Insect. Physiol. 48, 751–763. 10.1016/S0022-1910(02)00105-1 PubMed DOI

Näsvall K., Wiklund C., Mrazek V., Künstner A., Talla V., Busch H., et al. (2021). Host plant diet affects growth and induces altered gene expression and microbiome composition in the wood white (Leptidea sinapis) butterfly. Molec. Ecol. 30, 499–516. 10.1111/mec.15745 PubMed DOI PMC

Oh S. N., Seo M. J., Youn Y. N., Yu Y. M. (2015). Antifungfal activity against plant pathogenic fungi on insect enterobacteriaceae. Korean J. Pesticide Sci. 19, 71–79. 10.7585/kjps.2015.19.1.71 DOI

Oliveira N. C., Rodrigues P. A., Cônsoli F. L. (2022). Host-adapted strains of spodoptera frugiperda hold and share a core microbial community across the western hemisphere. Microb. Ecol. 85, 1552–1563. 10.1007/s00248-022-02008-6 PubMed DOI

Otani S., Mikaelyan A., Nobre T., Hansen L. H., Kon,é N. G. A., Sørensen S. J., et al. (2014). Identifying the core microbial community in the gut of fungus-growing termites. Molec. Ecol. 23, 4631–4644. 10.1111/mec.12874 PubMed DOI

Paniagua Voirol L. R., Frago E., Kaltenpoth M., Hilker M., Fatouros N. E. (2018). Bacterial symbionts in Lepidoptera: their diversity, transmission, and impact on the host. Front. Microbiol. 9, 556. 10.3389/fmicb.2018.00556 PubMed DOI PMC

Parks D. H., Tyson G. W., Hugenholtz P., Beiko R. G. (2014). STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30, 3123–3124. 10.1093/bioinformatics/btu494 PubMed DOI PMC

Paulson J. N., Stine O. C., Bravo H. C., Pop M. (2013). Differential abundance analysis for microbial marker-gene surveys. Nat. Methods 10, 1200–1202. 10.1038/nmeth.2658 PubMed DOI PMC

Prem Anand A. A., Vennison S. J., Sankar S. G., Gilwax Prabhu D. I., Vasan P. T., Raghuraman T., et al. (2010). Isolation and characterization of bacteria from the gut of Bombyx mori that degrade cellulose, xylan, pectin and starch and their impact on digestion. J. Insect Sci. 10, 107. 10.1673/031.010.10701 PubMed DOI PMC

Proffit M., Khallaf M. A., Carrasco D., Larsson M. C., Anderson P. (2015). ‘Do you remember the first time?'Host plant preference in a moth is modulated by experiences during larval feeding and adult mating. Ecol. Lett. 18, 365–374. 10.1111/ele.12419 PubMed DOI

Qadri M., Short S., Gast K., Hernandez J., Wong A. C.-N. (2020). Microbiome innovation in agriculture: development of microbial based tools for insect pest management. Front. Sustain. Food Syst. 4, 547751. 10.3389/fsufs.2020.547751 DOI

R CoreTeam (2017). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available online at: https://www.R-project.org (accessed September 28, 2022).

Rösvik A., Lhomme P., Khallaf M. A., Anderson P. (2020). Plant-induced transgenerational plasticity affecting performance but not preference in a polyphagous moth. Front. Ecol. Evol. 8, 254. 10.3389/fevo.2020.00254 DOI

Roy A., Walker W. B., III., Vogel H., Chattington S., Larsson M. C., Anderson P., et al. (2016). Diet dependent metabolic responses in three generalist insect herbivores PubMed DOI

Russell C. W., Poliakov A., Haribal M., Jander G., van Wijk K. J., Douglas A. E. (2014). Matching the supply of bacterial nutrients to the nutritional demand of the animal host. Proc. Biol. Sci. 281, 20141163. 10.1098/rspb.2014.1163 PubMed DOI PMC

Salem H., Kaltenpoth M. (2022). Beetle–bacterial symbioses: endless forms most functional. Annu. Rev. Entomol. 67, 201–219. 10.1146/annurev-ento-061421-063433 PubMed DOI

Samuel G., Reeves P. (2003). Biosynthesis of O-antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly. Carbohydrate Res. 338, 2503–2519. 10.1016/j.carres.2003.07.009 PubMed DOI

Sandal S., Singh S., Bansal G., Kaur R., Mogilicherla K., Pandher S., et al. (2023). Nanoparticle-shielded dsRNA delivery for enhancing RNAi efficiency in cotton spotted bollworm PubMed DOI PMC

Schloss P. D., Westcott S. L., Ryabin T., Hall J. R., Hartmann M., Hollister E. B., et al. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537–7541. 10.1128/AEM.01541-09 PubMed DOI PMC

Scolari F., Casiraghi M., Bonizzoni M. (2019). Aedes spp. and their microbiota: a review. Front. Microbiol. 10, 2036. 10.3389/fmicb.2019.02036 PubMed DOI PMC

Segers F. H., Kešnerov,á L., Kosoy M., Engel P. (2017). Genomic changes associated with the evolutionary transition of an insect gut symbiont into a blood-borne pathogen. The ISME J. 11, 1232–1244. 10.1038/ismej.2016.201 PubMed DOI PMC

Selvakumar G., Sushil S. N., Stanley J., Mohan M., Deol A., Rai D., et al. (2011). Brevibacterium frigoritolerans a novel entomopathogen of Anomala dimidiata and Holotrichia longipennis (Scarabaeidae: Coleoptera). Biocontrol Sci. Technol. 21, 821–827. 10.1080/09583157.2011.586021 DOI

Shade A., Handelsman J. (2012). Beyond the Venn diagram: the hunt for a core microbiome. Environ. Microbiol. 14, 4–12. 10.1111/j.1462-2920.2011.02585.x PubMed DOI

Shao Y., Arias-Cordero E., Guo H., Bartram S., Boland W. (2014). PubMed DOI PMC

Siddiqui J. A., Khan M. M., Bamisile B. S., Hafeez M., Qasim M., Rasheed M. T., et al. (2022). Role of insect gut microbiota in pesticide degradation: a review. Front. Microbiol. 13, 870462. 10.3389/fmicb.2022.870462 PubMed DOI PMC

Singh S., Singh A., Baweja V., Roy A., Chakraborty A., Singh I. K. (2021). Molecular rationale of insect-microbes symbiosis—from insect behaviour to Mechanism. Microorganisms 9, 2422. 10.3390/microorganisms9122422 PubMed DOI PMC

Staudacher H., Kaltenpoth M., Breeuwer J. A., Menken S. B., Heckel D. G., Groot A. T. (2016). Variability of bacterial communities in the moth Heliothis virescens indicates transient association with the host. PLoS ONE 11, e0154514. 10.1371/journal.pone.0154514 PubMed DOI PMC

Teh B.-S., Apel J., Shao Y., Boland W. (2016). Colonization of the intestinal tract of the polyphagous pest PubMed DOI PMC

Thöming G., Larsson M. C., Hansson B. S., Anderson P. (2013). Comparison of plant preference hierarchies of male and female moths and the impact of larval rearing hosts. Ecology 94, 1744–1752. 10.1890/12-0907.1 PubMed DOI

Ugwu J. A., Liu M., Sun H., Asiegbu F. O. (2020). Microbiome of the larvae of Spodoptera frugiperda (J.E. DOI

Ugwu J. A., Wenzi R., Asiegbu F. O. (2022). Monocot diet sources drive diversity of gut bacterial communities in Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae. J. Appl. Entomol. 146, 942–956. 10.1111/jen.13022 DOI

Vijayakumar M. M., More R. P., Rangasamy A., Gandhi G. R., Muthugounder M., Thiruvengadam V., et al. (2018). Gut bacterial diversity of insecticide-susceptible and -resistant nymphs of the brown planthopper nilaparvata lugens Stål (Hemiptera: Delphacidae) and elucidation of their putative functional roles. J. Microbiol. Biotechnol. 28, 976–986. 10.4014/jmb.1711.11039 PubMed DOI

Vilanova C., Marín M., Baixeras J., Latorre A., Porcar M. (2014). Selecting microbial strains from pine tree resin: biotechnological applications from a terpene world. PLoS ONE 9, e100740. 10.1371/journal.pone.0100740 PubMed DOI PMC

Vogels G. V. D., Van der Drift C. (1976). Degradation of purines and pyrimidines by microorganisms. Bacteriol. Rev. 40, 403–468. 10.1128/br.40.2.403-468.1976 PubMed DOI PMC

Wadleigh R. W., Yu S. J. (1988). Detoxification of isothiocyanate allelochemicals by glutathione transferase in three lepidopterous species. J. Chem. Ecol. 14, 1279–1288. 10.1007/BF01019352 PubMed DOI

Wielkopolan B., Obrepalska-Steplowska A. (2016). Three-way interaction among plants, bacteria, and coleopteran insects. Planta 244, 313–332. 10.1007/s00425-016-2543-1 PubMed DOI PMC

Xia X., Lan B., Tao X., Lin J., You M. (2020). Characterization of PubMed DOI PMC

Xia X., Sun B., Gurr G. M., Vasseur L., Xue M., You M. (2018). Gut microbiota mediate insecticide resistance in the diamondback moth, PubMed DOI PMC

Zhang X., Zhang F., Lu X. (2022). Diversity and functional roles of the gut microbiota in lepidopteran insects. Microorganisms 10, 1234. 10.3390/microorganisms10061234 PubMed DOI PMC

Zhao M., Lin X., Guo X. (2022). The role of insect symbiotic bacteria in metabolizing phytochemicals and agrochemicals. Insects 13, 583. 10.3390/insects13070583 PubMed DOI PMC

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