Impact of Mosquito Gut Microbiota on Propagating Pathogenic Infections

PDF

Published: 2023-04-12

DOI: 10.56557/upjoz/2023/v44i53446

Page: 76-89


Biplab Bhowmik

Department of Zoology, Diamond Harbour Women’s University, Sarisha, South 24 Parganas, West Bengal-743368, India.

Swadhin Kumar Saha

Department of Chemistry, Kazi Nazrul University, Asansol, West Bengal-713340, India.

Monalisa Pramanik

Department of Zoology, Diamond Harbour Women’s University, Sarisha, South 24 Parganas, West Bengal-743368, India.

Swarupa Mondal

Department of Zoology, Diamond Harbour Women’s University, Sarisha, South 24 Parganas, West Bengal-743368, India.

Priya Roy *

Department of Zoology, Diamond Harbour Women’s University, Sarisha, South 24 Parganas, West Bengal-743368, India.

*Author to whom correspondence should be addressed.


Abstract

The mosquito vectors of various human diseases host a diversified microbial community. These microbiomes seem to be beneficial in several aspects of mosquito biology. They can influence mosquitoes’ susceptibility to various pathogenic infections, therefore affecting the vectorial capacity of mosquitoes through different direct or indirect mechanisms. These microbes act as natural barriers against several mosquito-transmitted infectious diseases. They may be considered as a new transmission-blocking strategy to limit the transmission of pathogens like Plasmodium, Trypanosome, Zika, Dengue and Chikungunya viruses, and filarial parasites. It is through an understanding of the interaction between the mosquito, its microbiota, and the transmitted pathogens that some promising approaches may be developed for limiting the transmission of pathogenic diseases.In this review, we investigate the role of mosquito’s gut microbiome in the propagation of pathogenic infections. It is summarized here in a brief manner how the current knowledge is used for the purpose of limiting the transmission of mosquito-borne diseases through the alteration of mosquitoes' vector capacities.

Keywords: Mosquito, microbiota, pathogen, vector competence, paratransgenesis


How to Cite

Bhowmik, B., Saha, S. K., Pramanik, M., Mondal, S., & Roy, P. (2023). Impact of Mosquito Gut Microbiota on Propagating Pathogenic Infections. UTTAR PRADESH JOURNAL OF ZOOLOGY, 44(5), 76–89. https://doi.org/10.56557/upjoz/2023/v44i53446

Downloads

Download data is not yet available.

References

Dennison NJ, Jupatanakul N, Dimopoulos G. The mosquito microbiota influences vector competence for human pathogens. Curr Opin Insect Sci Sep 1;3. 2014;3:6-13. DOI: 10.1016/j.cois.2014.07.004, PMID 25584199, PMCID PMC4288011.

Ohkuma M. Termite symbiotic systems: efficient bio-recycling of lignocellulose. Appl Microbiol Biotechnol. 2003;61(1):1-9. doi: 10.1007/s00253-002-1189-z, PMID 12658509. Mar. Epub. 2003;1-9. PMID 12658509.

Dillon RJ, Dillon VM. The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol. 2004;49(1):71-92.

DOI: 10.1146/annurev.ento.49.061802.123416, PMID 14651457.

Charroux B, Royet J. Gut-microbiota interactions in non-mammals: what can we learn from Drosophila? Semin Immunol Feb. 2012;24(1):17-24. DOI: 10.1016/j.smim.2011.11.003, PMID 22284578.

Ryu JH, Kim SH, Lee HY, Bai JY, Nam YD, Bae JW, et al. Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science. Feb 8;319(5864):777-782. 2008;Jan 24(5864):777-82.

DOI: 10.1126/science.1149357, PMID 18218863.

Xi Z, Ramirez JL, Dimopoulos G. The Aedes aegypti toll pathway controls dengue virus infection, 4. 2008;7:e1000098. PMID 18604274, PMCID PMC2435278.

Dong Y, Manfredini F, Dimopoulos G. Implication of the mosquito midgut microbiota in the defense against malaria parasites,May; 5(5). 2009;e1000423. PMID 19424427, PMCID PMC2673032.

Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT, Hedges LM, et al. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, chikungunya, and Plasmodium. Cell. 2009;139(7), Dec 24:1268-78.

DOI: 10.1016/j.cell.2009.11.042, PMID 20064373.

Cirimotich CM, Ramirez JL, Dimopoulos G. Native microbiota shape insect vector competence for human pathogens. Cell Host Microbe. 2011;10(4):307-10. DOI: 10.1016/j.chom.2011.09.006, PMCID PMC3462649 NIHMSID: NIHMS330700. PMID 22018231.

Romoli O, Gendrin M. The Tripartite Interact Between Mosq Microbiota Plasmodium. 20;11(1). 2018;200. PMID 29558973, PMCID PMC5861617.

Kukutla P, Yan G, Xu J. Wang Y Gilbreath 3rd TM. Dynamic gut microbiome across life history of the malaria mosquito Anopheles gambiae in Kenya. 2011;6(9): e24767. PMID 21957459, PMCID PMC3177825.

Chandler JA, Thongsripong P, Green A, Kittayapong P, Wilcox BA, Schroth GP, et al. Metagenomic shotgun sequencing of a bunyavirus in wild-caught Aedes aegypti from Thailand informs the evolutionary and genomic history of the phleboviruses. Virology. 2014;464-465:312-9. DOI: 10.1016/j.virol.2014.06.036, PMID 25108381, PMCID PMC4157124.

Tchioffo MT, Boissière A, Abate L, Nsango SE, Bayibéki AN, Awono-Ambéné PH, et al. Dynamics of bacterial community composition in the malaria mosquito’s epithelia. Front Microbiol. 2015; 6:1500.eCollection.

DOI: 10.3389/fmicb.2015.01500, PMID 26779155, PMCID PMC4700937.

Gonzalez-Ceron L, Santillan F, Rodriguez MH, Mendez D, Hernandez-Avila JE. Bacteria in midguts of field-collected Anopheles albimanus block Plasmodium vivax sporogonic development. May. J Med Entomol. 2003;40(3):371-4.

DOI: 10.1603/0022-2585-40.3.371, PMID 12943119.

Yoshida S, Ioka D, Matsuoka H, Endo H, Ishii A. Bacteria expressing single-chain immunotoxin inhibit malaria parasite development in mosquitoes. Mol Biochem Parasitol. 2001;113(1):89-96.

DOI: 10.1016/s0166-6851(00)00387-x, PMID 11254957.

Riehle MA, Moreira CK, Lampe D, Lauzon C, Jacobs-Lorena M. Using bacteria to express and display anti-Plasmodium molecules in the mosquito midgut. Int J Parasitol. 2007;37(6): 595-603. DOI: 10.1016/j.ijpara.2006.12.002, PMID 17224154.

Wang S, Ghosh AK, Bongio N, Stebbings KA, Lampe DJ, Jacobs-Lorena M. Fighting malaria with engineered symbiotic bacteria from vector mosquitoes. Proc Natl Acad Sci U S A. 2012;109(31):12734-9.

DOI: 10.1073/pnas.1204158109, PMID 22802646, PMCID PMC3412027.

Lindh JM, Borg-Karlson AK, Faye I. Transstadial and horizontal transfer of bacteria within a colony of Anopheles gambiae (Diptera: Culicidae) and oviposition response to bacteria-containing water. Acta Trop. 2008;107:242-50. DOI: 10.1016/j.actatropica.2008.06.008, PMID 18671931.

Coon KL, Vogel KJ, Brown MR, Strand MR. Mosquitoes rely on their gut microbiota for development. Mol Ecol. 2014;23(11):2727-39. May 16. DOI: 10.1111/mec.12771, PMID 24766707, PMCID PMC4083365.

Favia G, Ricci I, Damiani C, Raddadi N, Crotti E, Marzorati M, et al. Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector. Proc Natl Acad Sci U S A. 2007;104(21):9047-51.

DOI: 10.1073/pnas.0610451104, PMID 17502606, PMCID PMC1885625.

Gabrieli P, Caccia S, Varotto-Boccazzi I, Arnoldi I, Barbieri G, Comandatore F, et al. Mosquito trilogy: microbiota, immunity and pathogens and their implications for the control of disease transmission. Front Microbiol. 2021;12:630438. DOI: 10.3389/fmicb.2021.630438, PMID 33889137.

Cerenius L, Lee BL, Söderhäll K. The proPO-system: Pros and cons for its role in invertebrate immunity. 2008;29(6):263-71.

Clayton AM, Dong Y, Dimopoulos G. The Anopheles innate immune system in the defense against malaria infection. J Innate Immun. Published online 2013 Aug 28. NIHMSID: NIHMS520940. 2014;6(2):169-81.

DOI: 10.1159/000353602, PMCID PMC3939431. PMID 23988482.

Zakovic S, Levashina EA. NF-κB-like signaling pathway REL2 in immune defenses of the malaria vector Anopheles gambiae. Front Cell Infect Microbiol Jun. 2017;21(7):258. PMID 28680852, PMCID PMC5478692.

Garver LS, Bahia AC, Das S, Souza-Neto JA, Shiao J, Dong Y, et al. Anopheles Imd pathway factors and effectors in infection intensity-dependent anti-Plasmodium action. PLOS Pathog. 2012;8(6): e1002737.

DOI: 10.1371/journal.ppat.1002737, PMID 22685401, PMCID PMC3369948.

Valanne S, Wang JH, Rämet M. The Drosophila Toll signaling pathway. J Immunol. 2011;186(2):649-56 DOI: 10.4049/jimmunol.1002302, PMID 21209287.

Bingsohn L, Knorr E, Billion A, Narva KE, Vilcinskas A. Knockdown of genes in the Toll pathway reveals newlethal RNA interference targets for insect pest control. Insect Mol Biol. 2017;26(1):92-102. DOI: 10.1111/imb.12273, PMID 27862545.

Kumar A, Srivastava P, Sirisena PDNN, Dubey SK, Kumar R, Shrinet J, et al. Mosquito. Innate Immun. 2018;9(3):95. Published online. PMCID PMC6165528. PMID 30096752.

Gao H, Cui C, Wang L, Jacobs-Lorena M, Wang S. Mosquito microbiota and implications for disease control. Trends Parasitol. 2020;36(2):98-111, ISSN 1471-4922. DOI: 10.1016/j.pt.2019.12.001, PMID 31866183.

Gendrin M, Christophides GK. The anopheles mosquito microbiota and their impact on pathogen transmission. Anopheles mosquitoes – New insights into malaria vectors. InTech; 2013.

Scolari F, Casiraghi M, Bonizzoni M. Aedes spp. and Their microbiota: a review. Front Microbiol. 2019;10:2036. DOI: 10.3389/fmicb.2019.02036, PMID 31551973.

Muturi EJ, Ramirez JL, Rooney AP, Kim CH. Comparative analysis of gut microbiota of mosquito communities in central Illinois. PLOS Negl Trop Dis. 2017;11(2):e0005377. DOI: 10.1371/journal.pntd.0005377, PMID 28245239.

Duguma D, Hall MW, Rugman-Jones P, Stouthamer R, Terenius O, Neufeld JD et al. Developmental succession of the microbiome of Culex mosquitoes. BMC Microbiol. 2015;15:140. DOI: 10.1186/s12866-015-0475-8, PMID 26205080.

Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH. How many species are infected with Wolbachia?—A statistical analysis of current data. FEMS Microbiol Lett. 2008; 281(2):215-20.

DOI: 10.1111/j.1574-6968.2008.01110.x, PMID 18312577, PMCID PMC2327208.

Werren JH, Baldo L, Clark ME. Wolbachia: Master manipulators of invertebrate biology. Oct. Nat Rev Microbiol. 2008; 6(10):741-51. DOI: 10.1038/nrmicro1969, PMID 18794912.

O’Connor L, Plichart C, Sang AC, Brelsfoard CL, Bossin HC, Dobson SL. Open release of male mosquitoes infected with a Wolbachia Biopesticide: Field performance and infection containment published. 2012;2012.

Bourtzis K, Dobson SL, Xi Z, Rasgon JL, Calvitti M, Moreira LA, et al. Harnessing mosquito-Wolbachia symbiosis for vector and disease control. Apr. Acta Trop. 2014;132;Suppl:S150-63. Nov 16. DOI: 10.1016/j.actatropica.2013.11.004, PMID 24252486.

Hughes GL, Rasgon JL. Transinfection: a method to investigate Wolbachia-host interactions and control arthropod-borne disease. Insect Mol Biol. 2014;23(2):141-51. DOI: 10.1111/imb.12066, PMID 24329998, PMCID PMC3949162.

Coon KL, Brown MR, Strand MR. Mosquitoes host communities of bacteria that are essential for development but vary greatly between local habitats. Mol Ecol. 2017;25(22):5806-26.

DOI: 10.1111/mec.13877, PMCID PMC5118126 NIHMSID: NIHMS822311. PMID 27718295.

Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT, Hedges LM, et al. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, chikungunya, and Plasmodium. Cell. 2009;139(7), 24 December 2009;1268-78.

DOI: 10.1016/j.cell.2009.11.042, PMID 20064373.

Walker T, Johnson PH, Moreira LA, Iturbe-Ormaetxe I, Frentiu FD, McMeniman CJ, et al. The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature. 2011;476(7361): 450-3.

DOI: 10.1038/nature10355, PMID 21866159.

Joubert DA, Walker T, Carrington LB, Bruyne JTD, Kien DHT, Hoang NLT, et al. Establishment of a Wolbachia superinfection in Aedes aegypti mosquitoes as a potential approach for future resistance management. 2016;2:e1005434. eCollection Feb. PMID 26891349, PMCID PMC4758728.

Hurk AFVD, Hall-Mendelin S, Pyke AT, Frentiu FD, McElroy K, Day A, et al. Impact of Wolbachia on infection with chikungunya and yellow fever viruses in the mosquito vector Aedes aegypti. PLoS Negl Trop Dis. 2012;6(11):e1892.Nov 1. DOI: 10.1371/journal.pntd.0001892, PMID 23133693, PMCID PMC3486898.

Aliota MT, Peinado SA, Osorio JE, Bartholomay LC. Culex pipiens and Aedes triseriatus mosquito susceptibility to Zika virus. Emerg Infect Dis. 2016;22(10):1857-9. DOI: 10.3201/eid2210.161082, PMCID PMC5038408. PMID 27434194.

Dutra HLC, Rocha MN, Dias FBS, Mansur SB, Caragata EP, Moreira LA. Wolbachia blocks currently circulating Zika virus isolates in Brazilian Aedes aegypti mosquitoes. Cell Host Microbe. 2016;19(6):771-4.

DOI: 10.1016/j.chom.2016.04.021, PMID 27156023, PMCID PMC4906366.

Jeffries CL, Walker T. The potential use of Wolbachia-based mosquito biocontrol strategies for Japanese encephalitis. PLoS Negl Trop Dis. 2015;9(6): e0003576.Published online 2015 Jun 18.

DOI: 10.1371/journal.pntd.0003576, PMCID PMC4472807. PMID 26086337.

Blagrove MSC, Arias-Goeta C, Genua CD, Failloux AB, Sinkins SP. A Wolbachia wMel transinfection in Aedes albopictus is not detrimental to host fitness and inhibits Chikungunya virus. PLoS Negl Trop Dis. Published. 2013;7(3):e2152. DOI: 10.1371/journal.pntd.0002152, PMID 23556030.

Glaser RL, Meola MA. The native Wolbachia endosymbionts of Drosophila melanogaster and Culex quinquefasciatus increase host resistance to West Nile virus infection. 2010;8:e11977. PMID 20700535, PMCID PMC2916829.

Mousson L, Martin E, Zouache K, Madec Y, Mavingui P, Failloux AB. Wolbachia modulates chikungunya replication in Aedes albopictus First published. 2010;19:1953-64.

Mousson L, Zouache K, Arias-Goeta C, Raquin V, Mavingui P, Failloux AB. The native Wolbachia symbionts limit transmission of dengue virus in Aedes albopictus. PLoS Negl Trop Dis. 2012;6(12):e1989.

DOI: 10.1371/journal.pntd.0001989, PMID 23301109.

Kambris Z, Blagborough AM, Pinto SB, Blagrove MSC, Godfray HCJ, Sinden RE, et al. Wolbachia stimulates immune gene expression and inhibits Plasmodium development in Anopheles gambiae published: October 7, 2010; 2010.

Bian G, Joshi D, Dong Y, Lu P, Zhou G, Pan X, et al. Wolbachia invades Anopheles stephensi populations and induces refractoriness to Plasmodium infection. Science. 2013;340(6133):748-51. DOI: 10.1126/science.1236192, PMID 23661760.

Buck M, Nilsson LKG, Brunius C, Dabiré RK, Hopkins R, Terenius O. Bacterial associations reveal spatial population dynamics in Anopheles gambiae mosquitoes. 2016;6:22806. PMID 26960555, PMCID PMC4785398.

Shaw WR, Marcenac P, Childs LM, Buckee CO, Baldini F, Sawadogo SP, et al. Wolbachia infections in natural Anopheles populations affect egg laying and negatively correlate with Plasmodium development. Nat Commun. 2016;7(1):Article number: 11772. DOI: 10.1038/ncomms11772

Boissière A, Tchioffo MT, Bachar D, Abate L, Marie A, Nsango SE, et al. Midgut microbiota of the malaria mosquito vector Anopheles gambiae and interactions with Plasmodium falciparum infection. PLOS Pathog. 2012;8(5):e1002742. DOI: 10.1371/journal.ppat.1002742, PMID 22693451, PMCID PMC3364955.

Kwon H, Mohammed M, Franzén O, Ankarklev J, Smith RC. Single-cell analysis of mosquito hemocytes identifies signatures of immune cell subtypes and cell differentiation. 2021;10:e66192. Published online 2021 Jul 28. PMCID PMC8376254, PMID 34318744.

Cirimotich CM, Dong Y, Garver LS, Sim S, Dimopoulos G. Mosquito immune defenses against Plasmodium infection. Dev Comp Immunol. 2010;34(4):387-95. DOI: 10.1016/j.dci.2009.12.005, PMID 20026176, PMCID PMC3462653.

Dimopoulos G, Seeley D, Wolf A, Kafatos FC. Malaria infection of the mosquito Anopheles gambiae activates immune-responsive genes during critical transition stages of the parasite life cycle. 1998;21:6115-23. PMCID PMC1170938. PMID 9799221.

Cansado-Utrilla C, Zhao SY, McCall PJ, Coon KL, Hughes GL. The microbiome and mosquito vectorial capacity: rich potential for discovery and translation. Microbiome. 2021;9(1):111. DOI: 10.1186/s40168-021-01073-2, PMID 34006334.

Hegde S, Voronin D, Casas-Sanchez A, Saldaña MA, Heinz E, Acosta-Serrano A, et al. Gut-associated bacteria invade the midgut epithelium of Aedes aegypti and stimulate innate immunity and suppress Zika virus infection in cells. bioRxiv. 2020;2020:866897.

Sharma P, Sharma S, Maurya RK, Das De T, Thomas T, Lata S et al. Salivary glands harbor more diverse microbial communities than gut in Anopheles culicifacies. Parasit Vectors. 2014;7:235. DOI: 10.1186/1756-3305-7-235, PMID 24886293.

Mancini MV, Damiani C, Accoti A, Tallarita M, Nunzi E, Cappelli A, et al. Estimating bacteria diversity in different organs of nine species of mosquito by next generation sequencing. BMC Microbiol. 2018;18(1): 126.

DOI: 10.1186/s12866-018-1266-9, PMID 30286722.

Gao H, Cui C, Wang L, Jacobs-Lorena M, Wang S. Mosquito microbiota and implications for disease control. Trends Parasitol. 2020;36(2):98-111. DOI: 10.1016/j.pt.2019.12.001, PMID 31866183, PMCID PMC9827750.

Smith DL, McKenzie FE. Statics and dynamics of malaria infection in Anopheles mosquitoes. Malar J. 2004;3(1):13:Article number: 13. DOI: 10.1186/1475-2875-3-13, PMID 15180900.

Pan X, Pike A, Joshi D, Bian G, McFadden MJ, Lu P, et al. The bacterium Wolbachia exploits host innate immunity to establish a symbiotic relationship with the dengue vector mosquito Aedes aegypti. ISME J. 2018;12(1):277-88.

DOI: 10.1038/ismej.2017.174, PMCID PMC5739022. PMID 29099491.

Yen PS, Failloux AB. A review: Wolbachia-based population replacement for mosquito control shares common points with genetically modified control approaches. Pathogens. 2020;9(5):404. DOI: 10.3390/pathogens9050404, PMID 32456036, PMCID PMC7281599.

Dobson SL. Reversing Wolbachia-based population replacement. Trends Parasitol. 2003;19(3):128-33. DOI: 10.1016/s1471-4922(03)00002-3, PMID 12643996.

Werren JH, Jaenike J. Wolbachia and cytoplasmic incompatibility in mycophagous Drosophila and their relatives. 1995;75(3):320-6.

Sumithra GNM, Puttaraju HP. A comparative analysis of long PCR and standard PCR technique in detecting the Wolbachia endosymbiont. Curr Trends Biotechnol Pharm. 2012;6, Issue:4 Print ISSN: 0973-8916. Online ISSN: 2230-7303. Online published on 29 April,2013. 2012;6(4):472–478.

Saridaki A, Bourtzis K. Wolbachia-induced reproductive parasitism and applications. Entomol Hell. 2009;18;18:3-16. Online ISSN: 2459-3885. Print ISSN: 0254-5381.

Joyce JD, Nogueira JR, Bales AA, Pittman KE, Anderson JR. Interactions between la Crosse virus and bacteria isolated from the digestive tract of Aedes albopictus (Diptera: Culicidae). J Med Entomol. 2011;48(2), 1 March 2011:389-94. DOI: 10.1603/me09268, PMID 21485378.

Saraiva RG, Fang J, Kang S, Angleró-Rodríguez YI, 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(4):e0006443.Apr. DOI: 10.1371/journal.pntd.0006443, PMID 29694346, PMCID PMC5937796.

Saraiva RG, Huitt-Roehl CR, Tripathi A, Cheng YQ, Bosch J, Townsend CA, et al. Chromobacterium spp. mediate their anti-Plasmodium activity through secretion of the histone deacetylase inhibitor Romidepsin. 2018;1:6176. PMID 29670144, PMCID PMC5906607.

Londono-Renteria B, Troupin A, Conway MJ, Vesely D, Ledizet M, Roundy CM, et al. Dengue virus infection of Aedes aegypti requires a putative cysteine rich venom protein. PLOS Pathog. 2015;11(10):e1005202.

DOI: 10.1371/journal.ppat.1005202, PPATHOGENS-D-15-01450 (pii). PMID 26491875, PMCID PMC4619585.

Paingankar M, Gokhale MD, Deobagkar DN. Apte-Deshpande A. 2012. Serratia odorifera a midgut inhabitant of Aedes aegypti mosquito enhances its susceptibility to dengue-2 virus;7(7);Jul 27:e40401. PMID 22848375, PMCID PMC3407224.

Paingankar M, Gokhale MD, Deobagkar DN. Apte-Deshpande A. Serratia odorifera mediated enhancement in susceptibility of Aedes aegypti for chikungunya virus. 2014.;139(5):762-8. PMID 25027087, PMCID PMC4140042.

Wu P, Sun P, Nie K, Zhu Y, Shi M, Xiao C et al. A gut commensal bacterium promotes mosquito permissiveness to arboviruses. Cell Host Microbe. 2019;25(1):101-112.e5. DOI: 10.1016/j.chom.2018.11.004, PMID 30595552.

Sharma A, Tripathi P, Kumar S. One-pot synthesis of silver nanocomposites from Achyranthes aspera: an eco-friendly larvicide against Aedes aegypti L. 2020;10 Issue :2 Page :54-64.

Villegas LEM, Campolina TB, Barnabe NR, Orfano AS, Chaves BA, Norris DE, et al. Zika virus infection modulates the bacterial diversity associated with Aedes aegypti as revealed by metagenomic analysis. PLoS One. 2018;13(1):e0190352. DOI: 10.1371/journal.pone.0190352, PMID 29293631.

Zouache K, Michelland RJ, Failloux AB, Grundmann GL, Mavingui P. Chikungunya virus impacts the diversity of symbiotic bacteria in mosquito vector. Mol Ecol. 2012;21:2297-309. DOI: 10.1111/j.1365-294X.2012.05526.x, PMID 22433115.

Muturi EJ, Lagos-Kutz D, Dunlap C, Ramirez JL, Rooney AP, Hartman GL, et al. Mosquito microbiota cluster by host sampling location. Parasit Vectors. 2018;11(1):468. DOI: 10.1186/s13071-018-3036-9, PMID 30107817.

Gupta A, Nair S. Dynamics of insect–microbiome interaction influence Host and Microbial Symbiont. Front Microbiol. 2020;11:1357. DOI: 10.3389/fmicb.2020.01357, PMID 32676060.

Tol SV, Dimopoulos G. Influences of the mosquito microbiota on vector competence. In: Raikhel AS, editor. Progress in mosquito research, 2016. Advances in insect physiology. Vol. 51. Academic Press Inc. 2016;243-91.

Wang S, Jacobs-Lorena M. Paratransgenesis applications: fighting malaria with engineered mosquito symbiotic bacteria. Arthropod. Vector control Dis, translator. 2017;1:219-34.

Hoy MA 2013. Chapter 14 - genetic modification of pest and beneficial insects for pest-management programs. Insect Molecular Genetics. 3rd ed Hoy MA, editor. San Diego: Academic Press, 661-736. 3rd ed. April 9, 2013, Hardcover ISBN: 9780124158740, eBook ISBN: 9780240821313.

Wilke AB, Marrelli MT. Paratransgenesis: A promising new strategy for mosquito vector control. Parasit Vectors. 2015;8:342. DOI: 10.1186/s13071-015-0959-2, PMID 26104575, PMCID PMC4489152.

Riehle MA, Moreira CK, Lampe D, Lauzon C, Jacobs-Lorena M. Using bacteria to express and display anti-Plasmodium molecules in the mosquito midgut. Int J Parasitol. 2007;37(6):595-603. DOI: 10.1016/j.ijpara.2006.12.002, PMID 17224154.

Ezemuoka LC, Akorli EA, Aboagye-Antwi F, Akorli J88. Mosquito midgut Enterobacter cloacae and Serratia marcescens affect the fitness of adult female Anopheles gambiae s.l. PLoS One. 2020;15(9):e0238931.

Published online. DOI: 10.1371/journal.pone.0238931, PMCID PMC7500640. PMID 32946471.

Crotti E, Damiani C, Pajoro M, Gonella E, Rizzi A, Ricci I, et al. Asaia, a versatile acetic acid bacterial symbiont, capable of cross-colonizing insects of phylogenetically distant genera and orders. Environ Microbiol. 2009;11(12):3252-64. DOI: 10.1111/j.1462-2920.2009.02048.x, PMID 19735280.

Shane JL, Grogan CL, Cwalina C, Lampe DJ. Blood mealinduced inhibition of vector-borne disease by transgenic microbiota. Nat Commun. 2018;9(1):4127:Article number: 4127. DOI: 10.1038/s41467-018-06580-9, PMID 30297781.

Epis S, Varotto-Boccazzi I, Crotti E, Damiani C, Giovati L, Mandrioli M, et al. Chimeric symbionts expressing a Wolbachia protein stimulate mosquito immunity and inhibit filarial parasite development. Commun Biol. 2020;3(1): 105. DOI: 10.1038/s42003-020-0835-2, PMID 32144396, PMCID PMC7060271.

Aksoy S, Weiss B, Attardo G. Paratransgenesis applied for control of tsetse transmitted sleeping sickness. In: Aksoy S, editor. Transgenesis and the management of vector-borne disease adv exp Med biol. New York: Springer. 2008;35-48. DOI: 10.1007/978-0-387-78225-6_3, PMID 18510012 Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 627).

Ren X, Hoiczyk E, Rasgon JL. Viral paratransgenesis in the malaria vector Anopheles gambiae. PLOS Pathog. 2008;4(8):e1000135. DOI: 10.1371/journal.ppat.1000135, PMID 18725926.

Suzuki Y, Niu G, Hughes GL, Rasgon JL. A viral over-expression system for the major malaria mosquito Anopheles gambiae. Sci Rep. 2014;4:5127:Article number: 5127. DOI: 10.1038/srep05127, PMID 24875042.

Mancini MV, Spaccapelo R, Damiani C, Accoti A, Tallarita M, Petraglia E et al. Paratransgenesis to control malaria vectors: a semi-field pilot study. Parasit Vectors. 2016;9:140:Article number: 140. DOI: 10.1186/s13071-016-1427-3, PMID 26965746.