Molecular Rationale of Insect-Microbes Symbiosis-From Insect Behaviour to Mechanism

. 2021 Nov 24 ; 9 (12) : . [epub] 20211124

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

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid34946024
Odkazy

PubMed 34946024
PubMed Central PMC8707026
DOI 10.3390/microorganisms9122422
PII: microorganisms9122422
Knihovny.cz E-zdroje

Insects nurture a panoply of microbial populations that are often obligatory and exist mutually with their hosts. Symbionts not only impact their host fitness but also shape the trajectory of their phenotype. This co-constructed niche successfully evolved long in the past to mark advanced ecological specialization. The resident microbes regulate insect nutrition by controlling their host plant specialization and immunity. It enhances the host fitness and performance by detoxifying toxins secreted by the predators and abstains them. The profound effect of a microbial population on insect physiology and behaviour is exploited to understand the host-microbial system in diverse taxa. Emergent research of insect-associated microbes has revealed their potential to modulate insect brain functions and, ultimately, control their behaviours, including social interactions. The revelation of the gut microbiota-brain axis has now unravelled insects as a cost-effective potential model to study neurodegenerative disorders and behavioural dysfunctions in humans. This article reviewed our knowledge about the insect-microbial system, an exquisite network of interactions operating between insects and microbes, its mechanistic insight that holds intricate multi-organismal systems in harmony, and its future perspectives. The demystification of molecular networks governing insect-microbial symbiosis will reveal the perplexing behaviours of insects that could be utilized in managing insect pests.

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Eckburg P.B., Bik E.M., Bernstein C.N., Purdom E., Dethlefsen L., Sargent M., Gill S.R., Nelson K.E., Relman D.A. Microbiology: Diversity of the human intestinal microbial flora. Science. 2005;308:1635–1638. doi: 10.1126/science.1110591. PubMed DOI PMC

Metzker M.L. Sequencing technologies the next generation. Nat. Rev. Genet. 2010;11:31–46. doi: 10.1038/nrg2626. PubMed DOI

Shpigler H.Y., Saul M.C., Corona F., Block L., Ahmed A.C., Zhao S.D., Robinson G.E. Erratum: Deep evolutionary conservation of autism-related genes. Proc. Natl. Acad. Sci. USA. 2019;116:17600. doi: 10.1073/pnas.1913223116. PubMed DOI PMC

Feltzin V., Wan K., Celniker S., Bonini N. Role and impact of the gut microbiota in a Drosophila model for parkinsonism. bioRxiv. 2019:718825. doi: 10.1101/718825. DOI

De Cock M., Virgilio M., Vandamme P., Augustinos A., Bourtzis K., Willems A., De Meyer M. Impact of sample preservation and manipulation on insect gut microbiome profiling. A Test Case With Fruit Flies (Diptera, Tephritidae) Front. Microbiol. 2019;10:2833. doi: 10.3389/fmicb.2019.02833. PubMed DOI PMC

Liberti J., Engel P. The gut microbiota—Brain axis of insects. Curr. Opin. Insect Sci. 2020;39:6–13. doi: 10.1016/j.cois.2020.01.004. PubMed DOI

Round J.L., O’Connell R.M., Mazmanian S.K. Coordination of tolerogenic immune responses by the commensal microbiota. J. Autoimmun. 2010;34:J220–J225. doi: 10.1016/j.jaut.2009.11.007. PubMed DOI PMC

Levy M., Kolodziejczyk A.A., Thaiss C.A., Elinav E. Dysbiosis and the immune system. Nat. Rev. Immunol. 2017;17:219–232. doi: 10.1038/nri.2017.7. PubMed DOI

Frago E., Dicke M., Godfray H.C.J. Insect symbionts as hidden players in insect-plant interactions. Trends Ecol. Evol. 2012;27:705–711. doi: 10.1016/j.tree.2012.08.013. PubMed DOI

Engel P., Moran N.A. The gut microbiota of insects-diversity in structure and function. FEMS Microbiol. Rev. 2013;37:699–735. doi: 10.1111/1574-6976.12025. PubMed DOI

Oliver K.M., Martinez A.J. How resident microbes modulate ecologically-important traits of insects. Curr. Opin. Insect Sci. 2014;4:1–7. doi: 10.1016/j.cois.2014.08.001. PubMed DOI

Lewis Z., Lizé A. Insect behaviour and the microbiome. Curr. Opin. Insect Sci. 2015;9:86–90. doi: 10.1016/j.cois.2015.03.003. PubMed DOI

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

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

Weiss B., Aksoy S. Microbiome influences on insect host vector competence. Trends Parasitol. 2011;27:514–522. doi: 10.1016/j.pt.2011.05.001. PubMed DOI PMC

Hosokawa T., Kikuchi Y., Shimada M., Fukatsu T. Obligate symbiont involved in pest status of host insect. Proc. R. Soc. B Biol. Sci. 2007;274:1979–1984. doi: 10.1098/rspb.2007.0620. PubMed DOI PMC

Nikoh N., Hosokawa T., Oshima K., Hattori M., Fukatsu T. Reductive evolution of bacterial genome in insect gut environment. Genome Biol. Evol. 2011;3:702–714. doi: 10.1093/gbe/evr064. PubMed DOI PMC

Tsuchida T., Koga R., Matsumoto S., Fukatsu T. Interspecific symbiont transfection confers a novel ecological trait to the recipient insect. Biol. Lett. 2011;7:245–248. doi: 10.1098/rsbl.2010.0699. PubMed DOI PMC

Barr K.L., Hearne L.B., Briesacher S., Clark T.L., Davis G.E. Microbial symbionts in insects influence down-regulation of defense genes in maize. PLoS ONE. 2010;5:e11339. doi: 10.1371/journal.pone.0011339. PubMed DOI PMC

Vorburger C., Gehrer L., Rodriguez P. A strain of the bacterial symbiont Regiella insecticola protects aphids against parasitoids. Biol. Lett. 2010;6:109–111. doi: 10.1098/rsbl.2009.0642. PubMed DOI PMC

Nikoh N., Hosokawa T., Moriyama M., Oshima K., Hattori M., Fukatsu T. Evolutionary origin of insect-Wolbachia nutritional mutualism. Proc. Natl. Acad. Sci. USA. 2014;111:10257–10262. doi: 10.1073/pnas.1409284111. PubMed DOI PMC

Hansen A.K., Trumble J.T., Stouthamer R., Paine T.D. A New Huanglongbing Species, “ Candidatus Liberibacter psyllaurous,” found to infect tomato and potato, is vectored by the Psyllid Bactericera cockerelli (Sulc) Appl. Environ. Microbiol. 2008;74:5862–5865. doi: 10.1128/AEM.01268-08. PubMed DOI PMC

Casteel C.L., Hansen A.K., Walling L.L., Paine T.D. Manipulation of plant defense responses by the tomato psyllid (Bactericerca cockerelli) and its associated endosymbiont Candidatus Liberibacter Psyllaurous. PLoS ONE. 2012;7:e35191. doi: 10.1371/annotation/9903158b-c45c-44b9-b152-7ffb5bec0c32. PubMed DOI PMC

Kaiser W., Huguet E., Casas J., Commin C., Giron D. Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts. Proc. R. Soc. B Biol. Sci. 2010;277:2311–2319. doi: 10.1098/rspb.2010.0214. PubMed DOI PMC

Morin S., Ghanim M., Zeidan M., Czosnek H., Verbeek M., van den Heuvel J.F.J.M. A GroEL homologue from endosymbiotic bacteria of the whitefly Bemisia tabaci Is implicated in the circulative transmission of tomato yellow leaf curl virus. Virology. 1999;256:75–84. doi: 10.1006/viro.1999.9631. PubMed DOI

Gottlieb Y., Zchori-Fein E., Mozes-Daube N., Kontsedalov S., Skaljac M., Brumin M., Sobol I., Czosnek H., Vavre F., Fleury F., et al. The transmission efficiency of tomato yellow leaf curl virus by the whitefly Bemisia tabaci Is Correlated with the Presence of a Specific Symbiotic Bacterium Species. J. Virol. 2010;84:9310–9317. doi: 10.1128/JVI.00423-10. PubMed DOI PMC

Klein A., Schrader L., Gil R., Manzano-Marín A., Flórez L., Wheeler D., Werren J.H., Latorre A., Heinze J., Kaltenpoth M., et al. A novel intracellular mutualistic bacterium in the invasive ant Cardiocondyla obscurior. ISME J. 2016;10:376–388. doi: 10.1038/ismej.2015.119. PubMed DOI PMC

Oliver K.M., Russell J.A., Moran N.A., Hunter M.S. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc. Natl. Acad. Sci. USA. 2003;100:1803–1807. doi: 10.1073/pnas.0335320100. PubMed DOI PMC

Scarborough C.L. Aphid Protected from pathogen by endosymbiont. Science. 2005;310:1781. doi: 10.1126/science.1120180. PubMed DOI

Kikuchi Y., Hayatsu M., Hosokawa T., Nagayama A., Tago K., Fukatsu T. Symbiont-mediated insecticide resistance. Proc. Natl. Acad. Sci. USA. 2012;109:8618–8622. doi: 10.1073/pnas.1200231109. PubMed DOI PMC

McCutcheon J.P., McDonald B.R., Moran N.A. Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc. Natl. Acad. Sci. USA. 2009;106:15394–15399. doi: 10.1073/pnas.0906424106. PubMed DOI PMC

Shigenobu S., Watanabe H., Hattori M., Sakaki Y., Ishikawa H. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature. 2000;407:81–86. doi: 10.1038/35024074. PubMed DOI

Weiss B.L., Wang J., Aksoy S. Tsetse immune system maturation requires the presence of obligate symbionts in larvae. PLoS Biol. 2011;9:e1000619. doi: 10.1371/journal.pbio.1000619. PubMed DOI PMC

Dale C., Welburn S. The endosymbionts of tsetse flies: Manipulating host–parasite interactions. Int. J. Parasitol. 2001;31:628–631. doi: 10.1016/S0020-7519(01)00151-5. PubMed DOI

Pons I., Renoz F., Noël C., Hance T. Circulation of the cultivable symbiont Serratia symbiotica in Aphids Is Mediated by Plants. Front. Microbiol. 2019;10:764. doi: 10.3389/fmicb.2019.00764. PubMed DOI PMC

Bando H., Okado K., Guelbeogo W.M., Badolo A., Aonuma H., Nelson B., Fukumoto S., Xuan X., Sagnon N., Kanuka H. Intra-specific diversity of Serratia marcescens in Anopheles mosquito midgut defines Plasmodium transmission capacity. Sci. Rep. 2013;3:1641. doi: 10.1038/srep01641. PubMed DOI PMC

Colgan L.J., Erbilgin N. Tree-mediated interactions between the jack pine budworm and a mountain pine beetle fungal associate. Ecol. Entomol. 2011;36:425–434. doi: 10.1111/j.1365-2311.2011.01283.x. DOI

Adams A.S., Six D.L. Detection of host habitat by parasitoids using cues associated with mycangial fungi of the mountain pine beetle, Dendroctonus ponderosae. Can. Entomol. 2008;140:124–127. doi: 10.4039/n07-018. DOI

DiGuistini S., Wang Y., Liao N.Y., Taylor G., Tanguay P., Feau N., Henrissat B., Chan S.K., Hesse-Orce U., Alamouti S.M., et al. Genome and transcriptome analyses of the mountain pine beetle-fungal symbiont Grosmannia clavigera, a lodgepole pine pathogen. Proc. Natl. Acad. Sci. USA. 2011;108:2504–2509. doi: 10.1073/pnas.1011289108. PubMed DOI PMC

Hulcr J., Mann R., Stelinski L.L. The scent of a partner: Ambrosia beetles are attracted to volatiles from their fungal symbionts. J. Chem. Ecol. 2011;37:1374–1377. doi: 10.1007/s10886-011-0046-x. PubMed DOI

Kopac S.M., Klassen J.L. Can they make it on their own? Hosts, microbes, and the holobiont niche. Front. Microbiol. 2016;7:1647. doi: 10.3389/fmicb.2016.01647. PubMed DOI PMC

Borges R.M. Co-niche construction between hosts and symbionts: Ideas and evidence. J. Genet. 2017;96:483–489. doi: 10.1007/s12041-017-0792-9. PubMed DOI

Trumbo S., Klassen J. Editorial overview: Hidden players: Microbes reshape the insect niche. Curr. Opin. Insect Sci. 2020;39:vi–ix. doi: 10.1016/j.cois.2020.05.008. PubMed DOI

Currie C.R., Poulsen M., Mendenhall J., Boomsma J.J., Billen J. Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants. Science. 2006;311:81–83. doi: 10.1126/science.1119744. PubMed DOI

Hulcr J., Rountree N.R., Diamond S.E., Stelinski L.L., Fierer N., Dunn R.R. Mycangia of Ambrosia Beetles Host Communities of Bacteria. Microb. Ecol. 2012;64:784–793. doi: 10.1007/s00248-012-0055-5. PubMed DOI

Yek S.H., Mueller U.G. The metapleural gland of ants. Biol. Rev. 2011;86:774–791. doi: 10.1111/j.1469-185X.2010.00170.x. PubMed DOI

Mason C.J. Complex Relationships at the intersection of insect gut microbiomes and plant defenses. J. Chem. Ecol. 2020;46:793–807. doi: 10.1007/s10886-020-01187-1. PubMed DOI

Calusinska M., Marynowska M., Bertucci M., Untereiner B., Klimek D., Goux X., Sillam-Dussès D., Gawron P., Halder R., Wilmes P., et al. Integrative omics analysis of the termite gut system adaptation to Miscanthus diet identifies lignocellulose degradation enzymes. Commun. Biol. 2020;3:275. doi: 10.1038/s42003-020-1004-3. PubMed DOI PMC

Větrovský T., Soukup P., Stiblik P., Votýpková K., Chakraborty A., Larrañaga I.O., Sillam-Dussès D., Lo N., Bourguignon T., Baldrian P., et al. Termites host specific fungal communities that differ from those in their ambient environments. Fungal Ecol. 2020;48:100991. doi: 10.1016/j.funeco.2020.100991. DOI

Soukup P., Větrovský T., Stiblik P., Votýpková K., Chakraborty A., Sillam-Dussès D., Kolařík M., Odriozola I., Lo N., Baldrian P., et al. Termites are associated with external species-specific bacterial communities. Appl. Environ. Microbiol. 2021;87:e02042-20. doi: 10.1128/AEM.02042-20. PubMed DOI PMC

Edwards M.J., Jacobs-Lorena M. Permeability and disruption of the peritrophic matrix and caecal membrane from Aedes aegypti and Anopheles gambiae mosquito larvae. J. Insect Physiol. 2000;46:1313–1320. doi: 10.1016/S0022-1910(00)00053-6. PubMed DOI

Pauchet Y., Muck A., Svatoš A., Heckel D.G., Preiss S. Mapping the larval midgut lumen proteome of Helicoverpa armigera, a generalist herbivorous insect. J. Proteome Res. 2008;7:1629–1639. doi: 10.1021/pr7006208. PubMed DOI

Smith T.E., Moran N.A. Coordination of host and symbiont gene expression reveals a metabolic tug-of-war between aphids and Buchnera. Proc. Natl. Acad. Sci. USA. 2020;117:2113–2121. doi: 10.1073/pnas.1916748117. PubMed DOI PMC

Chen B., Teh B.S., Sun C., Hu S., Lu X., Boland W., Shao Y. Biodiversity and activity of the gut microbiota across the life history of the insect herbivore Spodoptera littoralis. Sci. Rep. 2016;6:29505. doi: 10.1038/srep29505. PubMed DOI PMC

Ceja-Navarro J.A., Nguyen N.H., Karaoz U., Gross S.R., Herman D.J., Andersen G.L., Bruns T.D., Pett-Ridge J., Blackwell M., Brodie E.L. Compartmentalized microbial composition, oxygen gradients and nitrogen fixation in the gut of Odontotaenius disjunctus. ISME J. 2014;8:6–18. doi: 10.1038/ismej.2013.134. PubMed DOI PMC

Chung S.H., Scully E.D., Peiffer M., Geib S.M., Rosa C., Hoover K., Felton G.W. Host plant species determines symbiotic bacterial community mediating suppression of plant defenses. Sci. Rep. 2017;7:39690. doi: 10.1038/srep39690. PubMed DOI PMC

Ivens A.B.F., Gadau A., Kiers E.T., Kronauer D.J.C. Can social partnerships influence the microbiome? Insights from ant farmers and their trophobiont mutualists. Mol. Ecol. 2018;27:1898–1914. doi: 10.1111/mec.14506. PubMed DOI PMC

Lucas J.M., Madden A.A., Penick C.A., Epps M.J., Marting P.R., Stevens J.L., Fergus D.J., Dunn R.R., Meineke E.K. Azteca ants maintain unique microbiomes across functionally distinct nest chambers. Proc. R. Soc. B Biol. Sci. 2019;286:20191026. doi: 10.1098/rspb.2019.1026. PubMed DOI PMC

Bai S., Yao Z., Raza M.F., Cai Z., Zhang H. Regulatory mechanisms of microbial homeostasis in insect gut. Insect Sci. 2021;28:286–301. doi: 10.1111/1744-7917.12868. PubMed DOI

Chakraborty A., Roy A. Plant-Pest Interactions: From Molecular Mechanisms to Chemical Ecology. Springer; Singapore: 2021. Microbial influence on plant–insect interaction; pp. 337–363.

Hammer T.J., Bowers M.D. Gut microbes may facilitate insect herbivory of chemically defended plants. Oecologia. 2015;179:1–14. doi: 10.1007/s00442-015-3327-1. PubMed DOI

Jones A.G., Mason C.J., Felton G.W., Hoover K. Host plant and population source drive diversity of microbial gut communities in two polyphagous insects. Sci. Rep. 2019;9:2792. doi: 10.1038/s41598-019-39163-9. PubMed DOI PMC

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. 2015;41:75–84. doi: 10.1007/s10886-014-0530-1. PubMed DOI

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

Mason C.J., Hoover K., Felton G.W. Effects of maize (Zea mays) genotypes and microbial sources in shaping fall armyworm (Spodoptera frugiperda) gut bacterial communities. Sci. Rep. 2021;11:4429. doi: 10.1038/s41598-021-83497-2. PubMed DOI PMC

Casteel C.L., Hansen A.K. Evaluating insect-microbiomes at the plant-insect interface. J. Chem. Ecol. 2014;40:836–847. doi: 10.1007/s10886-014-0475-4. PubMed DOI

Ceja-Navarro J.A., Vega F.E., Karaoz U., Hao Z., Jenkins S., Lim H.C., Kosina P., Infante F., Northen T.R., Brodie E.L. Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee. Nat. Commun. 2015;6:7618. doi: 10.1038/ncomms8618. PubMed DOI PMC

Mason C.J., Ray S., Shikano I., Peiffer M., Jones A.G., Luthe D.S., Hoover K., Felton G.W. Plant defenses interact with insect enteric bacteria by initiating a leaky gut syndrome. Proc. Natl. Acad. Sci. USA. 2019;116:15991–15996. doi: 10.1073/pnas.1908748116. PubMed DOI PMC

Van den Bosch T.J.M., Welte C.U. Detoxifying symbionts in agriculturally important pest insects. Microb. Biotechnol. 2017;10:531–540. doi: 10.1111/1751-7915.12483. PubMed DOI PMC

Berasategui A., Salem H., Paetz C., Santoro M., Gershenzon J., Kaltenpoth M., Schmidt A. Gut microbiota of the pine weevil degrades conifer diterpenes and increases insect fitness. Mol. Ecol. 2017;26:4099–4110. doi: 10.1111/mec.14186. PubMed DOI

Itoh H., Tago K., Hayatsu M., Kikuchi Y. Detoxifying symbiosis: Microbe-mediated detoxification of phytotoxins and pesticides in insects. Nat. Prod. Rep. 2018;35:434–454. doi: 10.1039/C7NP00051K. PubMed DOI

De Fine Licht H.H., Schitøt M., Rogowska-Wrzesinska A., Nygaard S., Roepstorff P., Boomsma J.J. Laccase detoxification mediates the nutritional alliance between leaf-cutting ants and fungus-garden symbionts. Proc. Natl. Acad. Sci. USA. 2013;110:583–587. doi: 10.1073/pnas.1212709110. PubMed DOI PMC

Welte C.U., de Graaf R.M., van den Bosch T.J.M., Op den Camp H.J.M., van Dam N.M., Jetten M.S.M. 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. 2016;18:1379–1390. doi: 10.1111/1462-2920.12997. PubMed DOI

Xia X., Gurr G.M., Vasseur L., Zheng D., Zhong H., Qin B., Lin J., Wang Y., Song F., Li Y., et al. Metagenomic sequencing of diamondback moth gut microbiome unveils key holobiont adaptations for herbivory. Front. Microbiol. 2017;8:663. doi: 10.3389/fmicb.2017.00663. PubMed DOI PMC

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

Chakraborty A., Modlinger R., Ashraf M.Z., Synek J., Schlyter F., Roy A. Core Mycobiome and Their Ecological Relevance in the Gut of Five Ips Bark Beetles (Coleoptera: Curculionidae: Scolytinae) Front. Microbiol. 2020;11:568853. doi: 10.3389/fmicb.2020.568853. PubMed DOI PMC

Hammerbacher A., Schmidt A., Wadke N., Wright L.P., Schneider B., Bohlmann J., Brand W.A., Fenning T.M., Gershenzon J., Paetz C. A common fungal associate of the spruce bark beetle metabolizes the stilbene defenses of Norway spruce. Plant Physiol. 2013;162:1324–1336. doi: 10.1104/pp.113.218610. PubMed DOI PMC

Guo Z., Lu Y., Yang F., Zeng L., Liang G., Xu Y. Transmission modes of a pesticide-degrading symbiont of the oriental fruit fly Bactrocera dorsalis (Hendel) Appl. Microbiol. Biotechnol. 2017;101:8543–8556. doi: 10.1007/s00253-017-8551-7. PubMed DOI

Cheng D., Guo Z., Riegler M., Xi Z., Liang G., Xu Y. Gut symbiont enhances insecticide resistance in a significant pest, the oriental fruit fly Bactrocera dorsalis (Hendel) Microbiome. 2017;5:13. doi: 10.1186/s40168-017-0236-z. PubMed DOI PMC

Ramya S.L., Venkatesan T., Murthy K.S., Jalali S.K., Varghese A. Degradation of acephate by Enterobacter asburiae, Bacillus cereus and Pantoea agglomerans isolated from diamondback moth Plutella xylostella (L), a pest of cruciferous crops. J. Environ. Biol. 2016;37:611–618. PubMed

De Almeida L.G., De Moraes L.A.B., Trigo J.R., Omoto C., Cônsoli F.L. The gut microbiota of insecticide-resistant insects houses insecticide-degrading bacteria: A potential source for biotechnological exploitation. PLoS ONE. 2017;12:e0174754. doi: 10.1371/journal.pone.0174754. PubMed DOI PMC

Abe H., Tomitaka Y., Shimoda T., Seo S., Sakurai T., Kugimiya S., Tsuda S., Kobayashi M. Antagonistic plant defense system regulated by phytohormones assists interactions among vector insect, thrips and a tospovirus. Plant Cell Physiol. 2012;53:204–212. doi: 10.1093/pcp/pcr173. PubMed DOI

Chung S.H., Rosa C., Scully E.D., Peiffer M., Tooker J.F., Hoover K., Luthe D.S., Felton G.W. Herbivore exploits orally secreted bacteria to suppress plant defenses. Proc. Natl. Acad. Sci. USA. 2013;110:15728–15733. doi: 10.1073/pnas.1308867110. PubMed DOI PMC

Wang J., Chung S.H., Peiffer M., Rosa C., Hoover K., Zeng R., Felton G.W. Herbivore oral secreted bacteria trigger distinct defense responses in preferred and non-preferred host plants. J. Chem. Ecol. 2016;42:463–474. doi: 10.1007/s10886-016-0712-0. PubMed DOI

Yamasaki Y., Sumioka H., Takiguchi M., Uemura T., Kihara Y., Shinya T., Galis I., Arimura G. Phytohormone-dependent plant defense signaling orchestrated by oral bacteria of the herbivore Spodoptera litura. New Phytol. 2021;231:2029–2038. doi: 10.1111/nph.17444. PubMed DOI

Spiteller D., Dettner K., Boland W. Gut bacteria may be involved in interactions between plants, herbivores and their predators: Microbial biosynthesis of N-acylglutamine surfactants as elicitors of plant volatiles. Biol. Chem. 2000;381:755–762. doi: 10.1515/BC.2000.096. PubMed DOI

Hill C.A., Kafatos F.C., Stansfield S.K., Collins F.H. Arthropod-borne diseases: Vector control in the genomics era. Nat. Rev. Microbiol. 2005;3:262–268. doi: 10.1038/nrmicro1101. PubMed DOI

Cirimotich C.M., Dong Y., Garver L.S., Sim S., Dimopoulos G. Mosquito immune defenses against Plasmodium infection. Dev. Comp. Immunol. 2010;34:387–395. doi: 10.1016/j.dci.2009.12.005. PubMed DOI PMC

Xi Z., Ramirez J.L., Dimopoulos G. The Aedes aegypti toll pathway controls dengue virus infection. PLoS Pathog. 2008;4:e1000098. doi: 10.1371/journal.ppat.1000098. PubMed DOI PMC

Minard G., Mavingui P., Moro C.V. Diversity and function of bacterial microbiota in the mosquito holobiont. Parasites Vectors. 2013;6:146. doi: 10.1186/1756-3305-6-146. PubMed DOI PMC

Mereghetti V., Chouaia B., Montagna M. New insights into the microbiota of moth pests. Int. J. Mol. Sci. 2017;18:2450. doi: 10.3390/ijms18112450. PubMed DOI PMC

Guégan M., Zouache K., Démichel C., Minard G., Tran Van V., Potier P., Mavingui P., Valiente Moro C. The mosquito holobiont: Fresh insight into mosquito-microbiota interactions. Microbiome. 2018;6:49. doi: 10.1186/s40168-018-0435-2. PubMed DOI PMC

Strand M.R. Composition and functional roles of the gut microbiota in mosquitoes. Curr. Opin. Insect Sci. 2018;28:59–65. doi: 10.1016/j.cois.2018.05.008. PubMed DOI PMC

Degnan P.H., Lazarus A.B., Wernegreen J.J. Genome sequence of Blochmannia pennsylvanicus indicates parallel evolutionary trends among bacterial mutualists of insects. Genome Res. 2005;15:1023–1033. doi: 10.1101/gr.3771305. PubMed DOI PMC

Akman L., Yamashita A., Watanabe H., Oshima K., Shiba T., Hattori M., Aksoy S. Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat. Genet. 2002;32:402–407. doi: 10.1038/ng986. PubMed DOI

Degnan P.H., Yu Y., Sisneros N., Wing R.A., Moran N.A. Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proc. Natl. Acad. Sci. USA. 2009;106:9063–9068. doi: 10.1073/pnas.0900194106. PubMed DOI PMC

Akman L., Rio R.V.M., Beard C.B., Aksoy S. Genome size determination and coding capacity of Sodalis glossinidius, an enteric symbiont of tsetse flies, as revealed by hybridization to Escherichia coli gene arrays. J. Bacteriol. 2001;183:4517–4525. doi: 10.1128/JB.183.15.4517-4525.2001. PubMed DOI PMC

Hoffmann A.A., Clancy D., Duncan J. Naturally-occurring Wolbachia infection in Drosophila simulans that does not cause cytoplasmic incompatibility. Heredity. 1996;76:1–8. doi: 10.1038/hdy.1996.1. PubMed DOI

Reynolds K.T., Hoffmann A.A. Male age, host effects and the weak expression or non-expression of cytoplasmic incompatibility in Drosophila strains infected by maternally transmitted Wolbachia. Genet. Res. 2002;80:79–87. doi: 10.1017/S0016672302005827. PubMed DOI

Fry A.J., Palmer M.R., Rand D.M. Variable fitness effects of Wolbachia infection in Drosophila melanogaster. Heredity. 2004;93:379–389. doi: 10.1038/sj.hdy.6800514. PubMed DOI

Brownlie J.C., Cass B.N., Riegler M., Witsenburg J.J., Iturbe-Ormaetxe I., McGraw E.A., O’Neill S.L. Evidence for metabolic provisioning by a common invertebrate endosymbiont, Wolbachia pipientis, during periods of nutritional stress. PLoS Pathog. 2009;5:e1000368. doi: 10.1371/journal.ppat.1000368. PubMed DOI PMC

Kremer N., Voronin D., Charif D., Mavingui P., Mollereau B., Vavre F. Wolbachia interferes with ferritin expression and iron metabolism in insects. PLoS Pathog. 2009;5:e1000630. doi: 10.1371/journal.ppat.1000630. PubMed DOI PMC

Ikeya T., Broughton S., Alic N., Grandison R., Partridge L. The endosymbiont Wolbachia increases insulin/IGF-like signalling in Drosophila. Proc. R. Soc. B Biol. Sci. 2009;276:3799–3807. doi: 10.1098/rspb.2009.0778. PubMed DOI PMC

Moreira L.A., Iturbe-Ormaetxe I., Jeffery J.A., Lu G., Pyke A.T., Hedges L.M., Rocha B.C., Hall-Mendelin S., Day A., Riegler M., et al. A Wolbachia Symbiont in Aedes aegypti Limits Infection with Dengue, Chikungunya, and Plasmodium. Cell. 2009;139:1268–1278. doi: 10.1016/j.cell.2009.11.042. PubMed DOI

Bian G., Xu Y., Lu P., Xie Y., Xi Z. The Endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti. PLoS Pathog. 2010;6:e1000833. doi: 10.1371/journal.ppat.1000833. PubMed DOI PMC

Glaser R.L., Meola M.A. The native Wolbachia Endosymbionts of Drosophila melanogaster and Culex quinquefasciatus increase host resistance to west nile virus infection. PLoS ONE. 2010;5:e11977. doi: 10.1371/journal.pone.0011977. PubMed DOI PMC

Nazni W.A., Hoffmann A.A., NoorAfizah A., Cheong Y.L., Mancini M.V., Golding N., Kamarul G.M.R., Arif M.A.K., Thohir H., NurSyamimi H., et al. Establishment of Wolbachia strain wAlbB in malaysian populations of aedes aegypti for dengue control. Curr. Biol. 2019;29:4241–4248.e5. doi: 10.1016/j.cub.2019.11.007. PubMed DOI PMC

Pinto S.B., Riback T.I.S., Sylvestre G., Costa G., Peixoto J., Dias F.B.S., Tanamas S.K., Simmons C.P., Dufault S.M., Ryan P.A., et al. Effectiveness of wolbachia-infected mosquito deployments in reducing the incidence of dengue and other aedes-borne diseases in niterói, brazil: A quasi-experimental study. PLoS Negl. Trop. Dis. 2021;15:e0009556. doi: 10.1371/journal.pntd.0009556. PubMed DOI PMC

Ant T.H., Herd C.S., Geoghegan V., Hoffmann A.A., Sinkins S.P. The Wolbachia strain wAu provides highly efficient virus transmission blocking in Aedes aegypti. PLoS Pathog. 2018;14:e1006815. doi: 10.1371/journal.ppat.1006815. PubMed DOI PMC

Utarini A., Indriani C., Ahmad R.A., Tantowijoyo W., Arguni E., Ansari M.R., Supriyati E., Wardana D.S., Meitika Y., Ernesia I., et al. Efficacy of Wolbachia-infected mosquito deployments for the control of dengue. N. Engl. J. Med. 2021;384:2177–2186. doi: 10.1056/NEJMoa2030243. PubMed DOI PMC

Fraser J.E., De Bruyne J.T., Iturbe-Ormaetxe I., Stepnell J., Burns R.L., Flores H.A., O’Neill S.L. Novel Wolbachia-transinfected Aedes aegypti mosquitoes possess diverse fitness and vector competence phenotypes. PLoS Pathog. 2017;13:e1006751. doi: 10.1371/journal.ppat.1006751. PubMed DOI PMC

Zhang R., Zhu Y., Pang X., Xiao X., Zhang R., Cheng G. Regulation of antimicrobial peptides in Aedes aegypti Aag2 Cells. Front. Cell. Infect. Microbiol. 2017;7:22. doi: 10.3389/fcimb.2017.00022. PubMed DOI PMC

Royet J., Dziarski R. Peptidoglycan recognition proteins: Pleiotropic sensors and effectors of antimicrobial defences. Nat. Rev. Microbiol. 2007;5:264–277. doi: 10.1038/nrmicro1620. PubMed DOI

Pang X., Xiao X., Liu Y., Zhang R., Liu J., Liu Q., Wang P., Cheng G. Mosquito C-type lectins maintain gut microbiome homeostasis. Nat. Microbiol. 2016;1:16023. doi: 10.1038/nmicrobiol.2016.23. PubMed DOI

Xiao X., Yang L., Pang X., Zhang R., Zhu Y., Wang P., Gao G., Cheng G. A Mesh-Duox pathway regulates homeostasis in the insect gut. Nat. Microbiol. 2017;2:17020. doi: 10.1038/nmicrobiol.2017.20. PubMed DOI PMC

Oliveira J.H.M., Gonçalves R.L.S., Lara F.A., Dias F.A., Gandara A.C.P., Menna-Barreto R.F.S., Edwards M.C., Laurindo F.R.M., Silva-Neto M.A.C., Sorgine M.H.F., et al. Blood meal-derived heme decreases ROS levels in the midgut of Aedes aegypti and allows proliferation of intestinal microbiota. PLoS Pathog. 2011;7:e1001320. doi: 10.1371/journal.ppat.1001320. PubMed DOI PMC

Diaz-Albiter H., Sant’Anna M.R.V., Genta F.A., Dillon R.J. Reactive oxygen species-mediated immunity against Leishmania mexicana and Serratia marcescens in the phlebotomine sand fly Lutzomyia longipalpis. J. Biol. Chem. 2012;287:23995–24003. doi: 10.1074/jbc.M112.376095. PubMed DOI PMC

Pan X., Zhou G., Wu J., Bian G., Lu P., Raikhel A.S., Xi Z. Wolbachia induces reactive oxygen species (ROS)-dependent activation of the Toll pathway to control dengue virus in the mosquito Aedes aegypti. Proc. Natl. Acad. Sci. USA. 2012;109:E23–E31. doi: 10.1073/pnas.1116932108. PubMed DOI PMC

Hurst G.D.D., Anbutsu H., Kutsukake M., Fukatsu T. Hidden from the host: Spiroplasma bacteria infecting Drosophila do not cause an immune response, but are suppressed by ectopic immune activation. Insect Mol. Biol. 2003;12:93–97. doi: 10.1046/j.1365-2583.2003.00380.x. PubMed DOI

Hutchence K.J., Fischer B., Paterson S., Hurst G.D.D. How do insects react to novel inherited symbionts? A microarray analysis of Drosophila melanogaster response to the presence of natural and introduced Spiroplasma. Mol. Ecol. 2011;20:950–958. doi: 10.1111/j.1365-294X.2010.04974.x. PubMed DOI

Zug R., Hammerstein P. Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts. Biol. Rev. 2015;90:89–111. doi: 10.1111/brv.12098. PubMed DOI

Kumar S., Molina-Cruz A., Gupta L., Rodrigues J., Barillas-Mury C. A Peroxidase/Dual oxidase system modulates midgut epithelial immunity in Anopheles gambiae. Science. 2010;327:1644–1648. doi: 10.1126/science.1184008. PubMed DOI PMC

Louis C., Nigro L. Ultrastructural evidence of Wolbachia rickettsiales in Drosophila simulans and their relationships with unidirectional cross-incompatibility. J. Invertebr. Pathol. 1989;54:39–44. doi: 10.1016/0022-2011(89)90137-7. DOI

Zug R., Hammerstein P. Wolbachia and the insect immune system: What reactive oxygen species can tell us about the mechanisms of Wolbachia-host interactions. Front. Microbiol. 2015;6:1201. doi: 10.3389/fmicb.2015.01201. PubMed DOI PMC

Cleton N., Koopmans M., Reimerink J., Godeke G.J., Reusken C. Come fly with me: Review of clinically important arboviruses for global travelers. J. Clin. Virol. 2012;55:191–203. doi: 10.1016/j.jcv.2012.07.004. PubMed DOI

Moyes C.L., Vontas J., Martins A.J., Ng L.C., Koou S.Y., Dusfour I., Raghavendra K., Pinto J., Corbel V., David J.-P., et al. Contemporary status of insecticide resistance in the major Aedes vectors of arboviruses infecting humans. PLoS Negl. Trop. Dis. 2017;11:e0005625. doi: 10.1371/journal.pntd.0005625. PubMed DOI PMC

Shaw W.R., Catteruccia F. Vector biology meets disease control: Using basic research to fight vector-borne diseases. Nat. Microbiol. 2019;4:20–34. doi: 10.1038/s41564-018-0214-7. PubMed DOI PMC

Gonzales-Ceron L., Santillan F., Rodriguez M.H., Mendez D., Hernandez-Avila J.E. Bacteria in midguts of field-collected Anopheles albimanus Block Plasmodium vivax Sporogonic Development. J. Med. Entomol. 2003;40:371–374. doi: 10.1603/0022-2585-40.3.371. PubMed DOI

Dong Y., Aguilar R., Xi Z., Warr E., Mongin E., Dimopoulos G. Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathog. 2006;2:0513–0525. doi: 10.1371/journal.ppat.0020052. PubMed DOI PMC

Dong Y., Manfredini F., Dimopoulos G. Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog. 2009;5:e1000423. doi: 10.1371/journal.ppat.1000423. PubMed DOI PMC

Pais R., Lohs C., Wu Y., Wang J., Aksoy S. The obligate mutualist Wigglesworthia glossinidia influences reproduction, digestion, and immunity processes of its host, the tsetse fly. Appl. Environ. Microbiol. 2008;74:5965–5974. doi: 10.1128/AEM.00741-08. PubMed DOI PMC

Saraiva R.G., Fang J., Kang S., Angleró-Rodríguez Y.I., Dong Y., Dimopoulos G. Aminopeptidase secreted by Chromobacterium sp. Panama inhibits dengue virus infection by degrading the E protein. PLoS Negl. Trop. Dis. 2018;12:e0006443. doi: 10.1371/journal.pntd.0006443. PubMed DOI PMC

Apte-Deshpande A., Paingankar M., Gokhale M.D., Deobagkar D.N. Serratia odorifera a midgut inhabitant of aedes aegypti mosquito enhances its susceptibility to dengue-2 virus. PLoS ONE. 2012;7:e40401. doi: 10.1371/journal.pone.0040401. PubMed DOI PMC

Cirimotich C.M., Dong Y., Clayton A.M., Sandiford S.L., Souza-Neto J.A., Mulenga M., Dimopoulos G. Natural microbe-mediated refractoriness to Plasmodium infection in Anopheles gambiae. Science. 2011;332:855–858. doi: 10.1126/science.1201618. PubMed DOI PMC

Narasimhan S., Rajeevan N., Liu L., Zhao Y.O., Heisig J., Pan J., Eppler-Epstein R., Deponte K., Fish D., Fikrig E. Gut microbiota of the tick vector Ixodes scapularis modulate colonization of the Lyme disease spirochete. Cell Host Microbe. 2014;15:58–71. doi: 10.1016/j.chom.2013.12.001. PubMed DOI PMC

Pruzinova K., Sadlova J., Seblova V., Homola M., Votypka J., Volf P. Comparison of bloodmeal digestion and the peritrophic matrix in four sand fly species differing in susceptibility to leishmania donovani. PLoS ONE. 2015;10:e0128203. doi: 10.1371/journal.pone.0128203. PubMed DOI PMC

Rodgers F.H., Gendrin M., Wyer C.A.S., Christophides G.K. Microbiota-induced peritrophic matrix regulates midgut homeostasis and prevents systemic infection of malaria vector mosquitoes. PLoS Pathog. 2017;13:e1006391. doi: 10.1371/journal.ppat.1006391. PubMed DOI PMC

Aksoy S. Tsetse peritrophic matrix influences for trypanosome transmission. J. Insect Physiol. 2019;118:103919. doi: 10.1016/j.jinsphys.2019.103919. PubMed DOI PMC

Wang J., Wu Y., Yang G., Aksoy S. Interactions between mutualist Wigglesworthia and tsetse peptidoglycan recognition protein (PGRP-LB) influence trypanosome transmission. Proc. Natl. Acad. Sci. USA. 2009;106:12133–12138. doi: 10.1073/pnas.0901226106. PubMed DOI PMC

Rodrigues J., Brayner F.A., Alves L.C., Dixit R., Barillas-Mury C. Hemocyte Differentiation Mediates Innate Immune Memory in Anopheles gambiae Mosquitoes. Science. 2010;329:1353–1355. doi: 10.1126/science.1190689. PubMed DOI PMC

Fraser J.E., O’Donnell T.B., Duyvestyn J.M., O’Neill S.L., Simmons C.P., Flores H.A. Novel phenotype of Wolbachia strain wPip in Aedes aegypti challenges assumptions on mechanisms of Wolbachia-mediated dengue virus inhibition. PLoS Pathog. 2020;16:e1008410. doi: 10.1371/journal.ppat.1008410. PubMed DOI PMC

Lindsey A., Bhattacharya T., Newton I., Hardy R. Conflict in the intracellular lives of endosymbionts and viruses: A mechanistic look at Wolbachia-Mediated Pathogen-blocking. Viruses. 2018;10:141. doi: 10.3390/v10040141. PubMed DOI PMC

Hussain M., Frentiu F.D., Moreira L.A., O’Neill S.L., Asgari S. Wolbachia uses host microRNAs to manipulate host gene expression and facilitate colonization of the dengue vector Aedes aegypti. Proc. Natl. Acad. Sci. USA. 2011;108:9250–9255. doi: 10.1073/pnas.1105469108. PubMed DOI PMC

Rancès E., Ye Y.H., Woolfit M., McGraw E.A., O’Neill S.L. The relative importance of innate immune priming in Wolbachia-mediated dengue interference. PLoS Pathog. 2012;8:e1002548. doi: 10.1371/journal.ppat.1002548. PubMed DOI PMC

Lu P., Bian G., Pan X., Xi Z. Wolbachia induces density-dependent inhibition to dengue virus in mosquito cells. PLoS Negl. Trop. Dis. 2012;6:e1754. doi: 10.1371/journal.pntd.0001754. PubMed DOI PMC

Zhang G., Hussain M., O’Neill S.L., Asgari S. Wolbachia uses a host microRNA to regulate transcripts of a methyltransferase, contributing to dengue virus inhibition in Aedes aegypti. Proc. Natl. Acad. Sci. USA. 2013;110:10276–10281. doi: 10.1073/pnas.1303603110. PubMed DOI PMC

Walker T., Johnson P.H., Moreira L.A., Iturbe-Ormaetxe I., Frentiu F.D., McMeniman C.J., Leong Y.S., Dong Y., Axford J., Kriesner P., et al. The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature. 2011;476:450–453. doi: 10.1038/nature10355. PubMed DOI

Geoghegan V., Stainton K., Rainey S.M., Ant T.H., Dowle A.A., Larson T., Hester S., Charles P.D., Thomas B., Sinkins S.P. Perturbed cholesterol and vesicular trafficking associated with dengue blocking in Wolbachia-infected Aedes aegypti cells. Nat. Commun. 2017;8:526. doi: 10.1038/s41467-017-00610-8. PubMed DOI PMC

Caragata E.P., Rancès E., Hedges L.M., Gofton A.W., Johnson K.N., O’Neill S.L., McGraw E.A. Dietary cholesterol modulates pathogen blocking by Wolbachia. PLoS Pathog. 2013;9:e1003459. doi: 10.1371/journal.ppat.1003459. PubMed DOI PMC

Koh C., Islam M.N., Ye Y.H., Chotiwan N., Graham B., Belisle J.T., Kouremenos K.A., Dayalan S., Tull D.L., Klatt S., et al. Dengue virus dominates lipid metabolism modulations in Wolbachia-coinfected Aedes aegypti. Commun. Biol. 2020;3:518. doi: 10.1038/s42003-020-01254-z. PubMed DOI PMC

Chotiwan N., Andre B.G., Sanchez-Vargas I., Islam M.N., Grabowski J.M., Hopf-Jannasch A., Gough E., Nakayasu E., Blair C.D., Belisle J.T., et al. Dynamic remodeling of lipids coincides with dengue virus replication in the midgut of Aedes aegypti mosquitoes. PLOS Pathog. 2018;14:e1006853. doi: 10.1371/journal.ppat.1006853. PubMed DOI PMC

Manokaran G., Flores H.A., Dickson C.T., Narayana V.K., Kanojia K., Dayalan S., Tull D., McConville M.J., Mackenzie J.M., Simmons C.P. Modulation of acyl-carnitines, the broad mechanism behind Wolbachia-mediated inhibition of medically important flaviviruses in Aedes aegypti. Proc. Natl. Acad. Sci. USA. 2020;117:24475–24483. doi: 10.1073/pnas.1914814117. PubMed DOI PMC

Haqshenas G., Terradas G., Paradkar P.N., Duchemin J.B., McGraw E.A., Doerig C. A Role for the insulin receptor in the suppression of dengue virus and zika virus in Wolbachia-infected mosquito cells. Cell Rep. 2019;26:529–535.e3. doi: 10.1016/j.celrep.2018.12.068. PubMed DOI

Schooneman M.G., Vaz F.M., Houten S.M., Soeters M.R. Acylcarnitines. Diabetes. 2013;62:1–8. doi: 10.2337/db12-0466. PubMed DOI PMC

Molloy J.C., Sommer U., Viant M.R., Sinkins S.P. Wolbachia modulates lipid metabolism in Aedes albopictus mosquito cells. Appl. Environ. Microbiol. 2016;82:3109–3120. doi: 10.1128/AEM.00275-16. PubMed DOI PMC

O’Neill S.L., Ryan P.A., Turley A.P., Wilson G., Hurst T.P., Retzki K., Brown-Kenyon J., Hodgson L., Kenny N., Cook H., et al. Establishment of wMel Wolbachia in Aedes aegypti mosquitoes and reduction of local dengue transmission in Cairns and surrounding locations in northern Queensland, Australia. Gates Open Res. 2019;3:1547. doi: 10.12688/gatesopenres.13061.1. PubMed DOI PMC

Tantowijoyo W., Andari B., Arguni E., Budiwati N., Nurhayati I., Fitriana I., Ernesia I., Daniwijaya E.W., Supriyati E., Yusdiana D.H., et al. Stable establishment of WMEL Wolbachia in Aedes aegypti populations in Yogyakarta, Indonesia. PLoS Negl. Trop. Dis. 2020;14:e0008157. doi: 10.1371/journal.pntd.0008157. PubMed DOI PMC

Gesto J.S.M., Ribeiro G.S., Rocha M.N., Dias F.B.S., Peixoto J., Carvalho F.D., Pereira T.N., Moreira L.A. Reduced competence to arboviruses following the sustainable invasion of Wolbachia into native Aedes aegypti from Southeastern Brazil. Sci. Rep. 2021;11:1–14. doi: 10.1038/s41598-021-89409-8. PubMed DOI PMC

Carr J.P., Donnelly R., Tungadi T., Murphy A.M., Jiang S., Bravo-Cazar A., Yoon J.Y., Cunniffe N.J., Glover B.J., Gilligan C.A. Viral Manipulation of plant stress responses and host interactions with insects. Adv. Virus Res. 2018;102:177–197. doi: 10.1016/bs.aivir.2018.06.004. PubMed DOI

Kaur N., Hasegawa D.K., Ling K.S., Wintermantel W.M. Application of genomics for understanding plant virus-insect vector interactions and insect vector control. Phytopathology. 2016;106:1213–1222. doi: 10.1094/PHYTO-02-16-0111-FI. PubMed DOI

Frank J.H., Frank J.H., Thomas M.C., Yousten A.A., Howard F.W., Giblin-davis R.M., Heppner J.B., Zuparko R.L., Sánchez N.E., Luna M.G., et al. Encyclopedia of Entomology. Springer; Dordrecht, The Netherlands: 2008. Plant Viruses and Insects; pp. 2938–2945.

Gong J.-T., Li Y., Li T.-P., Liang Y., Hu L., Zhang D., Zhou C.-Y., Yang C., Zhang X., Zha S.-S., et al. Stable introduction of plant-virus-inhibiting Wolbachia into Planthoppers for Rice Protection. Curr. Biol. 2020;30:4837–4845. doi: 10.1016/j.cub.2020.09.033. PubMed DOI

Ramalho M.O., Duplais C., Orivel J., Dejean A., Gibson J.C., Suarez A.V., Moreau C.S. Development but not diet alters microbial communities in the Neotropical arboreal trap jaw ant Daceton armigerum: An exploratory study. Sci. Rep. 2020;10:7350. doi: 10.1038/s41598-020-64393-7. PubMed DOI PMC

Segers F.H.I.D., Kaltenpoth M., Foitzik S. Abdominal microbial communities in ants depend on colony membership rather than caste and are linked to colony productivity. Ecol. Evol. 2019;9:13450–13467. doi: 10.1002/ece3.5801. PubMed DOI PMC

Salem H., Bauer E., Strauss A.S., Vogel H., Marz M., Kaltenpoth M. Vitamin supplementation by gut symbionts ensures metabolic homeostasis in an insect host. Proc. R. Soc. B Biol. Sci. 2014;281:20141838. doi: 10.1098/rspb.2014.1838. PubMed DOI PMC

Douglas A.E. The B vitamin nutrition of insects: The contributions of diet, microbiome and horizontally acquired genes. Curr. Opin. Insect Sci. 2017;23:65–69. doi: 10.1016/j.cois.2017.07.012. PubMed DOI

Kaltenpoth M., Göttler W., Herzner G., Strohm E. Symbiotic bacteria protect wasp larvae from fungal infestation. Curr. Biol. 2005;15:475–479. doi: 10.1016/j.cub.2004.12.084. PubMed DOI

Vizcaino M.I., Guo X., Crawford J.M. Merging chemical ecology with bacterial genome mining for secondary metabolite discovery. J. Ind. Microbiol. Biotechnol. 2014;41:285–299. doi: 10.1007/s10295-013-1356-5. PubMed DOI PMC

Klassen J.L. Microbial secondary metabolites and their impacts on insect symbioses. Curr. Opin. Insect Sci. 2014;4:15–22. doi: 10.1016/j.cois.2014.08.004. PubMed DOI

Hurst G.D.D., Frost C.L. Reproductive parasitism: Maternally inherited symbionts in a biparental world. Cold Spring Harb. Perspect. Biol. 2015;7:a017699. doi: 10.1101/cshperspect.a017699. PubMed DOI PMC

Jiggins F.M., Hurst G.D.D., Majerus M.E.N. Sex-ratio-distorting Wolbachia causes sex-role reversal in its butterfly host. Proc. R. Soc. B Biol. Sci. 2000;267:69–73. doi: 10.1098/rspb.2000.0968. PubMed DOI PMC

Abe J., Kamimura Y., Kondo N., Shimada M. Extremely female-biased sex ratio and lethal male-male combat in a parasitoid wasp, Melittobia australica (Eulophidae) Behav. Ecol. 2003;14:34–39. doi: 10.1093/beheco/14.1.34. DOI

Stouthamer R., Breeuwer J.A.J., Hurst G.D.D. Wolbachia pipientis: Microbial manipulator of arthropod reproduction. Annu. Rev. Microbiol. 1999;53:71–102. doi: 10.1146/annurev.micro.53.1.71. PubMed DOI

Mateos M., Castrezana S.J., Nankivell B.J., Estes A.M., Markow T.A., Moran N.A. Heritable endosymbionts of Drosophila. Genetics. 2006;174:363–376. doi: 10.1534/genetics.106.058818. PubMed DOI PMC

Goodacre S.L., Martin O.Y., Thomas C.F.G., Hewitt G.M. Wolbachia and other endosymbiont infections in spiders. Mol. Ecol. 2006;15:517–527. doi: 10.1111/j.1365-294X.2005.02802.x. PubMed DOI

Konecka E., Olszanowski Z. A screen of maternally inherited microbial endosymbionts in oribatid mites (Acari: Oribatida) Microbiology. 2015;161:1561–1571. doi: 10.1099/mic.0.000114. PubMed DOI

Kenyon S.G., Hunter M.S. Manipulation of oviposition choice of the parasitoid wasp, Encarsia pergandiella, by the endosymbiotic bacterium Cardinium. J. Evol. Biol. 2007;20:707–716. doi: 10.1111/j.1420-9101.2006.01238.x. PubMed DOI

Hughes D.P., Andersen S.B., Hywel-Jones N.L., Himaman W., Billen J., Boomsma J.J. Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection. BMC Ecol. 2011;11:13. doi: 10.1186/1472-6785-11-13. PubMed DOI PMC

Zurek L., Wes Watson D., Krasnoff S.B., Schal C. Effect of the entomopathogenic fungus, Entomophthora muscae (Zygomycetes: Entomophthoraceae), on sex pheromone and other cuticular hydrocarbons of the house fly, Musca domestica. J. Invertebr. Pathol. 2002;80:171–176. doi: 10.1016/S0022-2011(02)00109-X. PubMed DOI

Adamo S.A., Kovalko I., Easy R.H., Stoltz D. A viral aphrodisiac in the cricket Gryllus texensis. J. Exp. Biol. 2014;217:1970–1976. doi: 10.1242/jeb.103408. PubMed DOI

Cheng D., Chen S., Huang Y., Pierce N.E., Riegler M., Yang F., Zeng L., Lu Y., Liang G., Xu Y. Symbiotic microbiota may reflect host adaptation by resident to invasive ant species. PLOS Pathog. 2019;15:e1007942. doi: 10.1371/journal.ppat.1007942. PubMed DOI PMC

Sgritta M., Dooling S.W., Buffington S.A., Momin E.N., Francis M.B., Britton R.A., Costa-Mattioli M. Mechanisms underlying microbial-mediated changes in social behavior in mouse models of autism spectrum disorder. Neuron. 2019;101:246–259.e6. doi: 10.1016/j.neuron.2018.11.018. PubMed DOI PMC

Zhu F., Guo R., Wang W., Ju Y., Wang Q., Ma Q., Sun Q., Fan Y., Xie Y., Yang Z., et al. Transplantation of microbiota from drug-free patients with schizophrenia causes schizophrenia-like abnormal behaviors and dysregulated kynurenine metabolism in mice. Mol. Psychiatry. 2020;25:2905–2918. doi: 10.1038/s41380-019-0475-4. PubMed DOI

Wada-Katsumata A., Zurek L., Nalyanya G., Roelofs W.L., Zhang A., Schal C. Gut bacteria mediate aggregation in the German cockroach. Proc. Natl. Acad. Sci. USA. 2015;112:15678–15683. doi: 10.1073/pnas.1504031112. PubMed DOI PMC

Wong A.C.N., Wang Q.P., Morimoto J., Senior A.M., Lihoreau M., Neely G.G., Simpson S.J., Ponton F. Gut microbiota modifies olfactory-guided microbial preferences and foraging decisions in Drosophila. Curr. Biol. 2017;27:2397–2404.e4. doi: 10.1016/j.cub.2017.07.022. PubMed DOI

Carthey A.J.R., Gillings M.R., Blumstein D.T. The Extended Genotype: Microbially mediated olfactory communication. Trends Ecol. Evol. 2018;33:885–894. doi: 10.1016/j.tree.2018.08.010. PubMed DOI

DeNieu M., Mounts K., Manier M. Two gut microbes are necessary and sufficient for normal cognition in Drosophila melanogaster. bioRxiv. 2019:593723. doi: 10.1101/593723. DOI

Teseo S., van Zweden J.S., Pontieri L., Kooij P.W., Sørensen S.J., Wenseleers T., Poulsen M., Boomsma J.J., Sapountzis P. The scent of symbiosis: Gut bacteria may affect social interactions in leaf-cutting ants. Anim. Behav. 2019;150:239–254. doi: 10.1016/j.anbehav.2018.12.017. DOI

Westfall S., Lomis N., Prakash S. A novel synbiotic delays Alzheimer’s disease onset via combinatorial gut-brain-axis signaling in Drosophila melanogaster. PLoS ONE. 2019;14:e0214985. doi: 10.1371/journal.pone.0214985. PubMed DOI PMC

Chen K., Luan X., Liu Q., Wang J., Chang X., Snijders A.M., Mao J.H., Secombe J., Dan Z., Chen J.H., et al. Drosophila histone demethylase KDM5 regulates social behavior through immune control and gut microbiota maintenance. Cell Host Microbe. 2019;25:537–552.e8. doi: 10.1016/j.chom.2019.02.003. PubMed DOI PMC

Van Moll L., De Smet J., Cos P., Van Campenhout L. Microbial symbionts of insects as a source of new antimicrobials: A review. Crit. Rev. Microbiol. 2021;47:562–579. doi: 10.1080/1040841X.2021.1907302. PubMed DOI

Xu L., Xu S., Sun L., Zhang Y., Luo J., Bock R., Zhang J. Synergistic action of the gut microbiota in environmental RNA interference in a leaf beetle. Microbiome. 2021;9:98. doi: 10.1186/s40168-021-01066-1. PubMed DOI PMC

Whitten M., Dyson P. Gene silencing in non-model insects: Overcoming hurdles using symbiotic bacteria for trauma-free sustainable delivery of RNA interference: Sustained RNA interference in insects mediated by symbiotic bacteria: Applications as a genetic tool and as a biocid. BioEssays. 2017;39:1600247. doi: 10.1002/bies.201600247. PubMed DOI

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