Impact of the microbiome on mosquito-borne diseases
Huicheng Shi, Xi Yu, Gong Cheng
Impact of the microbiome on mosquito-borne diseases
Mosquito-borne diseases present a significant threat to human health, with the possibility of outbreaks of new mosquito-borne diseases always looming. Unfortunately, current measures to combat these diseases such as vaccines and drugs are often either unavailable or ineffective. However, recent studies on microbiomes may reveal promising strategies to fight these diseases. In this review, we examine recent advances in our understanding of the effects of both the mosquito and vertebrate microbiomes on mosquito-borne diseases. We argue that the mosquito microbiome can have direct and indirect impacts on the transmission of these diseases, with mosquito symbiotic microorganisms, particularly Wolbachia bacteria, showing potential for controlling mosquito-borne diseases. Moreover, the skin microbiome of vertebrates plays a significant role in mosquito preferences, while the gut microbiome has an impact on the progression of mosquito-borne diseases in humans. As researchers continue to explore the role of microbiomes in mosquito-borne diseases, we highlight some promising future directions for this field. Ultimately, a better understanding of the interplay between mosquitoes, their hosts, pathogens, and the microbiomes of mosquitoes and hosts may hold the key to preventing and controlling mosquito-borne diseases.
microbiome / mosquito / mosquito-borne viruses / malaria / pathogen transmission
[1] |
Aberle JH, Koblischke M, Stiasny K. CD4 T cell responses to flaviviruses. J Clin Virol 2018;108:126–131.
CrossRef
Google scholar
|
[2] |
Achee NL, Grieco JP, Vatandoost H, et al. Alternative strategies for mosquito-borne arbovirus control. PLoS Negl Trop Dis 2019;13:e0006822.
CrossRef
Google scholar
|
[3] |
Aliota MT, Peinado SA, Velez ID, et al. The wMel strain of Wolbachia reduces transmission of Zika virus by Aedes aegypti. Sci Rep 2016;6:28792.
CrossRef
Google scholar
|
[4] |
de Almeida JP, Aguiar ER, Armache JN, et al. The virome of vector mosquitoes. Curr Opin Virol 2021;49:7–12.
CrossRef
Google scholar
|
[5] |
Almire F, Terhzaz S, Terry S, et al. Sugar feeding protects against arboviral infection by enhancing gut immunity in the mosquito vector Aedes aegypti. PLoS Pathog 2021;17:e1009870.
CrossRef
Google scholar
|
[6] |
Amerson-Brown MH, Miller AL, Maxwell CA, et al. Cultivated human vaginal microbiome communities impact Zika and Herpes simplex virus replication in ex vivo vaginal mucosal cultures. Front Microbiol 2019;9:3340.
CrossRef
Google scholar
|
[7] |
Amino R, Thiberge S, Martin B, et al. Quantitative imaging of Plasmodium transmission from mosquito to mammal. Nat Med 2006;12:220–224.
CrossRef
Google scholar
|
[8] |
Amino R, Giovannini D, Thiberge S, et al. Host cell traversal is important for progression of the malaria parasite through the dermis to the liver. Cell Host Microbe 2008;3:88–96.
CrossRef
Google scholar
|
[9] |
Andrews ES, Crain PR, Fu Y, et al. Reactive oxygen species production and Brugia pahangi survivorship in Aedes polynesiensis with artificial Wolbachia infection types. PLoS Pathog 2012;8:e1003075.
CrossRef
Google scholar
|
[10] |
de Angeli Dutra D, Salloum PM, Poulin R. Vector microbiome: will global climate change affect vector competence and pathogen transmission? Parasitol Res 2023;122:11–17.
CrossRef
Google scholar
|
[11] |
Angleró-Rodríguez YI, Talyuli OAC, Blumberg BJ, et al. An Aedes aegypti-associated fungus increases susceptibility to dengue virus by modulating gut trypsin activity. Elife 2017;6:e28844.
CrossRef
Google scholar
|
[12] |
Ant TH, Herd CS, Geoghegan V, et al. The Wolbachia strain wAu provides highly efficient virus transmission blocking in Aedes aegypti. PLoS Pathog 2018;14:e1006815.
CrossRef
Google scholar
|
[13] |
Arévalo-Cortés A, Damania A, Granada Y, et al. Association of Midgut bacteria and their metabolic pathways with Zika infection and insecticide resistance in Colombian Aedes aegypti populations. Viruses 2022;14:2197.
CrossRef
Google scholar
|
[14] |
Ashley EA, Dhorda M, Fairhurst RM, et al. Spread of artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 2014;371:411–423.
CrossRef
Google scholar
|
[15] |
Atoni E, Zhao L, Karungu S, et al. The discovery and global distribution of novel mosquito-associated viruses in the last decade (2007–2017). Rev Med Virol 2019;29:e2079.
CrossRef
Google scholar
|
[16] |
Aželytė J, Wu-Chuang A, Žiegytė R, et al. Anti-microbiota vaccine reduces avian malaria infection within mosquito vectors. Front Immunol 2022;13:841835.
CrossRef
Google scholar
|
[17] |
Bai L, Wang L, Vega-Rodríguez J, et al. A gut symbiotic bacterium serratia marcescens renders mosquito resistance to plasmodium infection through activation of mosquito immune responses. Front Microbiol 2019;10:1580.
CrossRef
Google scholar
|
[18] |
Baidaliuk A, Miot EF, Lequime S, et al. Cell-fusing agent virus reduces arbovirus dissemination in Aedes aegypti mosquitoes in vivo. J Virol 2019;93:e00705–e00719.
CrossRef
Google scholar
|
[19] |
Balaji S, Jayachandran S, Prabagaran SR. Evidence for the natural occurrence of Wolbachia in Aedes aegypti mosquitoes. FEMS Microbiol Lett 2019;366:fnz055.
CrossRef
Google scholar
|
[20] |
Barnard K, Jeanrenaud ACSN, Brooke BD, et al. The contribution of gut bacteria to insecticide resistance and the life histories of the major malaria vector Anopheles arabiensis (Diptera: Culicidae). Sci Rep 2019;9:9117.
CrossRef
Google scholar
|
[21] |
Barreaux AMG, Stone CM, Barreaux P, et al. The relationship between size and longevity of the malaria vector Anopheles gambiae (s.s.) depends on the larval environment. Parasit Vectors 2018;11:485.
CrossRef
Google scholar
|
[22] |
Baton LA, Pacidônio EC, Gonçalves DS, et al. wFlu: characterization and evaluation of a native Wolbachia from the mosquito Aedes fluviatilis as a potential vector control agent. PLoS One 2013;8:e59619.
CrossRef
Google scholar
|
[23] |
Beaumier CM, Rothman AL. Cross-reactive memory CD4+ T cells alter the CD8+ T-cell response to heterologous secondary dengue virus infections in mice in a sequence-specific manner. Viral Immunol 2009;22:215–219.
CrossRef
Google scholar
|
[24] |
Beckmann JF, Ronau JA, Hochstrasser M. A Wolbachia deubiquitylating enzyme induces cytoplasmic incompatibility. Nat Microbiol 2017;2:17007.
CrossRef
Google scholar
|
[25] |
Berg G, Rybakova D, Fischer D, et al. Microbiome definition re-visited: old concepts and new challenges. Microbiome 2020;8:103.
CrossRef
Google scholar
|
[26] |
Bian G, Xu Y, Lu P, et al. The endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti. PLoS Pathog 2010;6:e1000833.
CrossRef
Google scholar
|
[27] |
Bian G, Joshi D, Dong Y, et al. Wolbachia invades Anopheles stephensi populations and induces refractoriness to Plasmodium infection. Science 2013;340:748–751.
CrossRef
Google scholar
|
[28] |
Bird RG, Draper CC, Ellis DS. A cytoplasmic polyhedrosis virus in midgut cells of Anopheles stephensi and in the sporogonic stages of Plasmodium berghei yoelii. Bull World Health Organ 1972;46:337–343.
|
[29] |
Blagrove MSC, Arias-Goeta C, Failloux AB, et al. Wolbachia strain wMel induces cytoplasmic incompatibility and blocks dengue transmission in Aedes albopictus. Proc Natl Acad Sci USA 2012;109:255–260.
CrossRef
Google scholar
|
[30] |
Blagrove MSC, Arias-Goeta C, Di Genua C, et al. A Wolbachia wMel transinfection in Aedes albopictus is not detrimental to host fitness and inhibits Chikungunya virus. PLoS Negl Trop Dis 2013;7:e2152.
CrossRef
Google scholar
|
[31] |
Blander JM, Longman RS, Iliev ID, et al. Regulation of inflammation by microbiota interactions with the host. Nat Immunol 2017;18:851–860.
CrossRef
Google scholar
|
[32] |
Boissière A, Tchioffo MT, Bachar D, et al. Midgut microbiota of the malaria mosquito vector anopheles gambiae and interactions with Plasmodium falciparum infection. PLoS Pathog 2012;8:e1002742.
CrossRef
Google scholar
|
[33] |
Bordenstein SR, Werren JH. Bidirectional incompatibility among divergent Wolbachia and incompatibility level differences among closely related Wolbachia in Nasonia. Heredity (Edinb) 2007;99:278–287.
CrossRef
Google scholar
|
[34] |
Bozic J, Capone A, Pediconi D, et al. Mosquitoes can harbour yeasts of clinical significance and contribute to their environmental dissemination. Environ Microbiol Rep 2017;9:642–648.
CrossRef
Google scholar
|
[35] |
Brennan LJ, Keddie BA, Braig HR, et al. The endosymbiont Wolbachia pipientis induces the expression of host antioxidant proteins in an Aedes albopictus cell line. PLoS One 2008;3:e2083.
CrossRef
Google scholar
|
[36] |
Briant L, Desprès P, Choumet V, et al. Role of skin immune cells on the host susceptibility to mosquito-borne viruses. Virology 2014;46:26–32.
CrossRef
Google scholar
|
[37] |
Busula AO, Takken W, de Boer JG, et al. Variation in host preferences of malaria mosquitoes is mediated by skin bacterial volatiles. Med Vet Entomol 2017;31:320–326.
CrossRef
Google scholar
|
[38] |
Callaini G, Dallai R, Riparbelli MG. Wolbachia-induced delay of paternal chromatin condensation does not prevent maternal chromosomes from entering anaphase in incompatible crosses of Drosophila simulans. J Cell Sci 1997;110:271–280.
CrossRef
Google scholar
|
[39] |
Calle-Tobón A, Holguin-Rocha AF, Moore C, et al. Blood meals with active and heat-inactivated serum modifies the gene expression and microbiome of Aedes albopictus. Front Microbiol 2021;12:724345.
CrossRef
Google scholar
|
[40] |
Cansado-Utrilla C, Zhao SY, McCall PJ, et al. The microbiome and mosquito vectorial capacity: rich potential for discovery and translation. Microbiome 2021;9:111.
CrossRef
Google scholar
|
[41] |
Capone A, Ricci I, Damiani C, et al. Interactions between Asaia, Plasmodium and Anopheles: new insights into mosquito symbiosis and implications in malaria symbiotic control. Parasit Vectors 2013;6:182.
CrossRef
Google scholar
|
[42] |
Cappelli A, Valzano M, Cecarini V, et al. Killer yeasts exert anti-plasmodial activities against the malaria parasite Plasmodium berghei in the vector mosquito Anopheles stephensi and in mice. Parasit Vectors 2019;12:329.
CrossRef
Google scholar
|
[43] |
Caputo B, Moretti R, Manica M, et al. A bacterium against the tiger: preliminary evidence of fertility reduction after release of Aedes albopictus males with manipulated Wolbachia infection in an Italian urban area. Pest Manag Sci 2020;76:1324–1332.
CrossRef
Google scholar
|
[44] |
Caragata EP, Rancès E, O’Neill SL, et al. Competition for amino acids between Wolbachia and the mosquito host, Aedes aegypti. Microb Ecol 2014;67:205–218.
CrossRef
Google scholar
|
[45] |
Caragata EP, Rocha MN, Pereira TN, et al. Pathogen blocking in Wolbachia-infected Aedes aegypti is not affected by Zika and dengue virus co-infection. PLoS Negl Trop Dis 2019;13:e0007443.
CrossRef
Google scholar
|
[46] |
Carissimo G, Pondeville E, McFarlane M, et al. Antiviral immunity of Anopheles gambiae is highly compartmentalized, with distinct roles for RNA interference and gut microbiota. Proc Natl Acad Sci USA 2015;112:E176–E185.
CrossRef
Google scholar
|
[47] |
Chancharoenthana W, Kamolratanakul S, Ariyanon W, et al. Abnormal blood bacteriome, gut dysbiosis, and progression to severe dengue disease. Front Cell Infect Microbiol 2022;12:890817.
CrossRef
Google scholar
|
[48] |
Chao J, Wistreich GA. Microbial isolations from the mid-gut of Culex tarsalis Coquillett. J Insect Pathol 1959;1:311–318.
|
[49] |
Chen R, Vasilakis N. Dengue—Quo tu et quo vadis? Viruses 2011;3:1562–1608.
CrossRef
Google scholar
|
[50] |
Cheng G, Liu Y, Wang P, et al. Mosquito defense strategies against viral infection. Trends Parasitol 2016;32:177–186.
CrossRef
Google scholar
|
[51] |
Chouin-Carneiro T, Ant TH, Herd C, et al. Wolbachia strain wAlbA blocks Zika virus transmission in Aedes aegypti. Med Vet Entomol 2020;34:116–119.
CrossRef
Google scholar
|
[52] |
Cirimotich CM, Ramirez JL, Dimopoulos G. Native microbiota shape insect vector competence for human pathogens. Cell Host Microbe 2011;10:307–310.
CrossRef
Google scholar
|
[53] |
Clemente JC, Ursell LK, Parfrey LW, et al. The impact of the gut microbiota on human health: an integrative view. Cell 2012;148:1258–1270.
CrossRef
Google scholar
|
[54] |
Cohen S, McGregor IA, Carrington S. Gamma-globulin and acquired immunity to human malaria. Nature 1961;192:733–737.
CrossRef
Google scholar
|
[55] |
Conway MJ, Colpitts TM, Fikrig E. Role of the vector in arbovirus transmission. Annu Rev Virol 2014;1:71–88.
CrossRef
Google scholar
|
[56] |
Coon KL, Vogel KJ, Brown MR, et al. Mosquitoes rely on their gut microbiota for development. Mol Ecol 2014;23:2727–2739.
CrossRef
Google scholar
|
[57] |
Coon KL, Brown MR, Strand MR. Mosquitoes host communities of bacteria that are essential for development but vary greatly between local habitats. Mol Ecol 2016;25:5806–5826.
CrossRef
Google scholar
|
[58] |
Coon KL, Valzania L, McKinney DA, et al. Bacteria-mediated hypoxia functions as a signal for mosquito development. Proc Natl Acad Sci USA 2017;114:E5362–E5369.
CrossRef
Google scholar
|
[59] |
Correa MA, Matusovsky B, Brackney DE, et al. Generation of axenic Aedes aegypti demonstrate live bacteria are not required for mosquito development. Nat Commun 2018;9:4464.
CrossRef
Google scholar
|
[60] |
Corrêa R, de Oliveira Santos I, Braz-de-Melo HA, et al. Gut microbiota modulation induced by Zika virus infection in immunocompetent mice. Sci Rep 2021;11:1421.
CrossRef
Google scholar
|
[61] |
Crawford JE, Clarke DW, Criswell V, et al. Efficient production of male Wolbachia-infected Aedes aegypti mosquitoes enables large-scale suppression of wild populations. Nat Biotechnol 2020;38:482–492.
CrossRef
Google scholar
|
[62] |
Crill WD, Roehrig JT. Monoclonal antibodies that bind to domain III of dengue virus E glycoprotein are the most efficient blockers of virus adsorption to Vero cells. J Virol 2001;75:7769–7773.
CrossRef
Google scholar
|
[63] |
Dada N, Sheth M, Liebman K, et al. Whole metagenome sequencing reveals links between mosquito microbiota and insecticide resistance in malaria vectors. Sci Rep 2018;8:2084.
CrossRef
Google scholar
|
[64] |
Dada N, Lol JC, Benedict AC, et al. Pyrethroid exposure alters internal and cuticle surface bacterial communities in Anopheles albimanus. ISME J 2019;13:2447–2464.
CrossRef
Google scholar
|
[65] |
Dada N, Benedict AC, López F, et al. Comprehensive characterization of internal and cuticle surface microbiota of laboratory-reared F1 Anopheles albimanus originating from different sites. Malar J 2021;20:414.
CrossRef
Google scholar
|
[66] |
Damiani C, Ricci I, Crotti E, et al. Mosquito-bacteria symbiosis: the case of Anopheles gambiae and Asaia. Microb Ecol 2010;60:644–654.
CrossRef
Google scholar
|
[67] |
da Silva Voorham JM, Rodenhuis-Zybert IA, Nuñez NVA, et al. Antibodies against the envelope glycoprotein promote infectivity of immature dengue virus serotype 2. PLoS One 2012;7:e29957.
CrossRef
Google scholar
|
[68] |
Dekker T, Geier M, Cardé RT. Carbon dioxide instantly sensitizes female yellow fever mosquitoes to human skin odours. J Exp Biol 2005;208:2963–2972.
CrossRef
Google scholar
|
[69] |
Demeure CE, Brahimi K, Hacini F, et al. Anopheles mosquito bites activate cutaneous mast cells leading to a local inflammatory response and lymph node hyperplasia. J Immunol 2005;174:3932–3940.
CrossRef
Google scholar
|
[70] |
Depinay N, Hacini F, Beghdadi W, et al. Mast cell-dependent down-regulation of antigen-specific immune responses by mosquito bites. J Immunol 2006;176:4141–4146.
CrossRef
Google scholar
|
[71] |
Dey R, Joshi AB, Oliveira F, et al. Gut microbes egested during bites of infected sand flies augment severity of Leishmaniasis via inflammasome- derived IL-1β. Cell Host Microbe 2018;23:134–143.e6.
CrossRef
Google scholar
|
[72] |
Diamond MS, Shrestha B, Marri A, et al. B cells and antibody play critical roles in the immediate defense of disseminated infection by West Nile encephalitis virus. J Virol 2003;77:2578–2586.
CrossRef
Google scholar
|
[73] |
Díaz S, Camargo C, Avila FW. Characterization of the reproductive tract bacterial microbiota of virgin, mated, and blood-fed Aedes aegypti and Aedes albopictus females. Parasit Vectors 2021;14:592.
CrossRef
Google scholar
|
[74] |
Dickson LB, Jiolle D, Minard G, et al. Carryover effects of larval exposure to different environmental bacteria drive adult trait variation in a mosquito vector. Sci Adv 2017;3:e1700585.
CrossRef
Google scholar
|
[75] |
Dobson SL, Bourtzis K, Braig HR, et al. Wolbachia infections are distributed throughout insect somatic and germ line tissues. Insect Biochem Mol Biol 1999;29:153–160.
CrossRef
Google scholar
|
[76] |
Dodson BL, Hughes GL, Paul O, et al. Wolbachia enhances West Nile virus (WNV) infection in the mosquito Culex tarsalis. PLoS NeglTrop Dis 2014;8:e2965.
CrossRef
Google scholar
|
[77] |
Duffy E, Morrin A. Endogenous and microbial volatile organic compounds in cutaneous health and disease. TRAC Trends Anal Chem 2019;111:163–172.
CrossRef
Google scholar
|
[78] |
Dutra HLC, Rocha MN, Dias FBS, et al. Wolbachia blocks currently circulating Zika virus isolates in Brazilian Aedes aegypti mosquitoes. Cell Host Microbe 2016;19:771–774.
CrossRef
Google scholar
|
[79] |
Elong Ngono A, Vizcarra EA, Tang WW, et al. Mapping and role of the CD8+ T cell response during primary Zika virus infection in mice. Cell Host Microbe 2017;21:35–46.
CrossRef
Google scholar
|
[80] |
Engl T, Michalkova V, Weiss BL, et al. Effect of antibiotic treatment and gamma-irradiation on cuticular hydrocarbon profiles and mate choice in tsetse flies (Glossina m. morsitans). BMC Microbiol 2018;18:145.
CrossRef
Google scholar
|
[81] |
Erttmann SF, Swacha P, Aung KM, et al. The gut microbiota prime systemic antiviral immunity via the cGAS-STING-IFN-I axis. Immunity 2022;55:847–861.e10.
CrossRef
Google scholar
|
[82] |
Favia G, Ricci I, Damiani C, et al. Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector. Proc Natl Acad Sci USA 2007;104:9047–9051.
CrossRef
Google scholar
|
[83] |
Feng Y, Peng Y, Song X, et al. Anopheline mosquitoes are protected against parasite infection by tryptophan catabolism in gut microbiota. Nat Microbiol 2022;7:707–715.
CrossRef
Google scholar
|
[84] |
Fernandez E, Kose N, Edeling MA, et al. Mouse and human monoclonal antibodies protect against infection by multiple genotypes of Japanese encephalitis virus. MBio 2018;9:e00008–e00018.
CrossRef
Google scholar
|
[85] |
Figueiredo LTM. Human urban arboviruses can infect wild animals and jump to sylvatic maintenance cycles in South America. Front Cell Infect Microbiol 2019;9:259.
CrossRef
Google scholar
|
[86] |
Flores HA, O’Neill SL. Controlling vector-borne diseases by releasing modified mosquitoes. Nat Rev Microbiol 2018;16:508–518.
CrossRef
Google scholar
|
[87] |
Fouda MA, Hassan MI, Al-Daly AG, et al. Effect of midgut bacteria of Culex pipiens L. on digestion and reproduction. J Egypt Soc Parasitol 2001;31:767–780.
|
[88] |
Franz AWE, Kantor AM, Passarelli AL, et al. Tissue barriers to arbovirus infection in mosquitoes. Viruses 2015;7:3741–3767.
CrossRef
Google scholar
|
[89] |
Frischknecht F, Matuschewski K. Plasmodium sporozoite biology. Cold Spring Harb Perspect Med 2017;7:a025478.
CrossRef
Google scholar
|
[90] |
Gabrieli P, Caccia S, Varotto-Boccazzi I, et al. Mosquito trilogy: microbiota, immunity and pathogens, and their implications for the control of disease transmission. Front Microbiol 2021;12:630438.
CrossRef
Google scholar
|
[91] |
Gaio ADO, Gusmão DS, Santos AV, et al. Contribution of midgut bacteria to blood digestion and egg production in Aedes aegypti (diptera: culicidae) (L.). Parasit Vectors 2011;4:105.
CrossRef
Google scholar
|
[92] |
Ganley JG, Pandey A, Sylvester K, et al. A systematic analysis of mosquito- microbiome biosynthetic gene clusters reveals antimalarial siderophores that reduce mosquito reproduction capacity. Cell Chem Biol 2020;27:817–826.e5.
CrossRef
Google scholar
|
[93] |
Gao L, Song X, Wang J. Gut microbiota is essential in PGRP-LA regulated immune protection against Plasmodium berghei infection. Parasit Vectors 2020;13:3.
CrossRef
Google scholar
|
[94] |
Gao H, Bai L, Jiang Y, et al. A natural symbiotic bacterium drives mosquito refractoriness to Plasmodium infection via secretion of an antimalarial lipase. Nat Microbiol 2021;6:806–817.
CrossRef
Google scholar
|
[95] |
Gatton ML, Chitnis N, Churcher T, et al. The importance of mosquito behavioural adaptations to malaria control in Africa. Evolution 2013;67:1218–1230.
CrossRef
Google scholar
|
[96] |
Garrett-Jones, C. Prognosis for Interruption of Malaria Transmission Through Assessment of the Mosquito’s Vectorial Capacity. Nature 1964; 204:1173–1175
CrossRef
Google scholar
|
[97] |
Gavor E, Choong YK, Liu Y, et al. Identification of Aedes aegypti salivary gland proteins interacting with human immune receptor proteins. PLoS Negl Trop Dis 2022;16:e0010743.
CrossRef
Google scholar
|
[98] |
Geoghegan V, Stainton K, Rainey SM, et al. Perturbed cholesterol and vesicular trafficking associated with dengue blocking in Wolbachia-infected Aedes aegypti cells. Nat Commun 2017;8:526.
CrossRef
Google scholar
|
[99] |
Gesto JSM, Pinto SB, Dias FBS, et al. Large-scale deployment and establishment of Wolbachia into the Aedes aegypti population in Rio de Janeiro, Brazil. Front Microbiol 2021a;12:711107.
CrossRef
Google scholar
|
[100] |
Gesto JSM, Ribeiro GS, Rocha MN, et al. Reduced competence to arboviruses following the sustainable invasion of Wolbachia into native Aedes aegypti from Southeastern Brazil. Sci Rep 2021b;11:10039.
CrossRef
Google scholar
|
[101] |
Glaser RL, Meola MA. The native Wolbachia endosymbionts of Drosophila melanogaster and Culex quinquefasciatus increase host resistance to West Nile virus infection. PLoS One 2010;5:e11977.
CrossRef
Google scholar
|
[102] |
Gnambani EJ, Bilgo E, Sanou A, et al. Infection of highly insecticide-resistant malaria vector Anopheles coluzzii with entomopathogenic bacteria Chromobacterium violaceum reduces its survival, blood feeding propensity and fecundity. Malar J 2020;19:352.
CrossRef
Google scholar
|
[103] |
Goenaga S, Kenney JL, Duggal NK, et al. Potential for co-infection of a mosquito-specific Flavivirus, Nhumirim Virus, to Block West Nile Virus transmission in mosquitoes. Viruses 2015;7:5801–5812.
CrossRef
Google scholar
|
[104] |
Gomes FM, Hixson BL, Tyner MDW, et al. Effect of naturally occurring Wolbachia in Anopheles gambiae s.l. mosquitoes from Mali on Plasmodium falciparum malaria transmission. Proc Natl Acad Sci USA 2017;114:12566–12571.
CrossRef
Google scholar
|
[105] |
Gómez M, Martinez D, Muñoz M, et al. Aedes aegypti and A. albopictus microbiome/virome: new strategies for controlling arboviral transmission? Parasit Vectors 2022;15:287.
CrossRef
Google scholar
|
[106] |
Gómez-Govea MA, Ramírez-Ahuja M de L, Contreras-Perera Y, et al. Suppression of Midgut Microbiota impact pyrethroid susceptibility in Aedes aegypti. Front Microbiol 2022;13:761459.
CrossRef
Google scholar
|
[107] |
Goodier MR, Wolf AS, Riley EM. Differentiation and adaptation of natural killer cells for anti-malarial immunity. Immunol Rev 2020;293:25–37.
CrossRef
Google scholar
|
[108] |
Gubler DJ. Dengue, urbanization and globalization: the Unholy Trinity of the 21(st) Century. Trop Med Health 2011;39:3–11.
CrossRef
Google scholar
|
[109] |
Guégan M, Zouache K, Démichel C, et al. The mosquito holobiont: fresh insight into mosquito–microbiota interactions. Microbiome 2018;6:49.
CrossRef
Google scholar
|
[110] |
Guégan M, Tran Van V, Martin E, et al. Who is eating fructose within the Aedes albopictus gut microbiota? Environ Microbiol 2020;22:1193–1206.
CrossRef
Google scholar
|
[111] |
Gusmão DS, Santos AV, Marini DC, et al. Culture-dependent and culture- independent characterization of microorganisms associated with Aedes aegypti (Diptera: Culicidae) (L.) and dynamics of bacterial colonization in the midgut. Acta Trop 2010;115:275–281.
CrossRef
Google scholar
|
[112] |
Haddi K, Tomé HVV, Du Y, et al. Detection of a new pyrethroid resistance mutation (V410L) in the sodium channel of Aedes aegypti: a potential challenge for mosquito control. Sci Rep 2017;7:46549.
CrossRef
Google scholar
|
[113] |
Harapan H, Michie A, Sasmono RT, et al. Dengue: a minireview. Viruses 2020;12:829.
CrossRef
Google scholar
|
[114] |
Hardy JL, Houk EJ, Kramer LD, et al. Intrinsic factors affecting vector competence of mosquitoes for arboviruses. Annu Rev Entomol 1983;28:229–262.
CrossRef
Google scholar
|
[115] |
Hegde S, Khanipov K, Albayrak L, et al. Microbiome interaction networks and community structure from laboratory-reared and field-collected Aedes aegypti, Aedes albopictus, and Culex quinquefasciatus mosquito vectors. Front Microbiol 2018;9:2160.
CrossRef
Google scholar
|
[116] |
Hegedus D, Erlandson M, Gillott C, et al. New insights into peritrophic matrix synthesis, architecture, and function. Annu Rev Entomol 2009;54:285–302.
CrossRef
Google scholar
|
[117] |
Hertig M, Wolbach SB. Studies on Rickettsia-like micro-organisms in insects. J Med Res 1924;44:329–374.7.
|
[118] |
Hien NT, Anh DD, Le NH, et al. Environmental factors influence the local establishment of Wolbachia in Aedes aegypti mosquitoes in two small communities in central Vietnam. Gates Open Res 2022;5:147.
CrossRef
Google scholar
|
[119] |
Hilgenboecker K, Hammerstein P, Schlattmann P, et al. How many species are infected with Wolbachia?—a statistical analysis of current data. FEMS Microbiol Lett 2008;281:215–220.
CrossRef
Google scholar
|
[120] |
Hinman EH. A study of the food of mosquito larvae (Culicidae). Am J Hyg 1930;12:238–270.
CrossRef
Google scholar
|
[121] |
Hoffmann AA, Montgomery BL, Popovici J, et al. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 2011;476:454–457.
CrossRef
Google scholar
|
[122] |
Hoffmann AA, Iturbe-Ormaetxe I, Callahan AG, et al. Stability of the wMel Wolbachia infection following invasion into Aedes aegypti populations. PLoS Negl Trop Dis 2014;8:e3115.
CrossRef
Google scholar
|
[123] |
Holz LE, Fernandez-Ruiz D, Heath WR. Protective immunity to liver- stage malaria. Clin Transl Immunol 2016;5:e105.
CrossRef
Google scholar
|
[124] |
Hughes GL, Koga R, Xue P, et al. Wolbachia infections are virulent and inhibit the human malaria parasite Plasmodium falciparum in Anopheles gambiae. PLoS Pathog 2011;7:e1002043.
CrossRef
Google scholar
|
[125] |
Hughes GL, Vega-Rodriguez J, Xue P, et al. Wolbachia strain wAlbB enhances infection by the rodent malaria parasite Plasmodium berghei in Anopheles gambiae mosquitoes. Appl Environ Microbiol 2012;78:1491–1495.
CrossRef
Google scholar
|
[126] |
Hussain M, Lu G, Torres S, et al. Effect of Wolbachia on replication of West Nile virus in a mosquito cell line and adult mosquitoes. J Virol 2013;87:851–858.
CrossRef
Google scholar
|
[127] |
James AG, Hyliands D, Johnston H. Generation of volatile fatty acids by axillary bacteria. Int J Cosmet Sci 2004;26:149–156.
CrossRef
Google scholar
|
[128] |
Jiggins FM. The spread of Wolbachia through mosquito populations. PLoS Biol 2017;15:e2002780.
CrossRef
Google scholar
|
[129] |
Jiménez-Cortés JG, García-Contreras R, Bucio-Torres MI, et al. Bacterial symbionts in human blood-feeding arthropods: patterns, general mechanisms and effects of global ecological changes. Acta Trop 2018;186:69–101.
CrossRef
Google scholar
|
[130] |
Jonkmans N, D’Acremont V, Flahault A. Scoping future outbreaks: a scoping review on the outbreak prediction of the WHO Blueprint list of priority diseases. BMJ Glob Health 2021;6:e006623.
CrossRef
Google scholar
|
[131] |
Joubert DA, O’Neill SL. Comparison of stable and transient Wolbachia infection models in Aedes aegypti to block dengue and West Nile Viruses. PLoS Negl Trop Dis 2017;11:e0005275.
CrossRef
Google scholar
|
[132] |
Joubert DA, Walker T, Carrington LB, et al. Establishment of a Wolbachia superinfection in Aedes aegypti mosquitoes as a potential approach for future resistance management. PLoS Pathog 2016;12:e1005434.
CrossRef
Google scholar
|
[133] |
Jurado KA, Yockey LJ, Wong PW, et al. Antiviral CD8 T cells induce Zikavirus- associated paralysis in mice. Nat Microbiol 2018;3:141–147.
CrossRef
Google scholar
|
[134] |
Kambris Z, Cook PE, Phuc HK, et al. Immune activation by life-shortening Wolbachia and reduced filarial competence in mosquitoes. Science 2009;326:134–136.
CrossRef
Google scholar
|
[135] |
Kambris Z, Blagborough AM, Pinto SB, et al. Wolbachia stimulates immune gene expression and inhibits plasmodium development in Anopheles gambiae. PLoS Pathog 2010;6:e1001143.
CrossRef
Google scholar
|
[136] |
Katzelnick LC, Gresh L, Halloran ME, et al. Antibody-dependent enhancement of severe dengue disease in humans. Science 2017;358:929–932.
CrossRef
Google scholar
|
[137] |
Kozlova EV, Hegde S, Roundy CM, et al. Microbial interactions in the mosquito gut determine Serratia colonization and blood-feeding propensity. ISME J 2021;15:93–108.
CrossRef
Google scholar
|
[138] |
Kumar S, Christophides GK, Cantera R, et al. The role of reactive oxygen species on Plasmodium melanotic encapsulation in Anopheles gambiae. Proc Natl Acad Sci USA 2003;100:14139–14144.
CrossRef
Google scholar
|
[139] |
Landmann F. The Wolbachia endosymbionts. Microbiol Spectr 2019;7:1–15.
CrossRef
Google scholar
|
[140] |
Laven H. Eradication of culex pipiens fatigans through cytoplasmic incompatibility. Nature 1967;216:383–384.
CrossRef
Google scholar
|
[141] |
LePage DP, Metcalf JA, Bordenstein SR, et al. Prophage WO genes recapitulate and enhance Wolbachia-induced cytoplasmic incompatibility. Nature 2017;543:243–247.
CrossRef
Google scholar
|
[142] |
Levkovich T, Poutahidis T, Smillie C, et al. Probiotic bacteria induce a ‘glow of health’. PLoS One 2013;8:e53867.
CrossRef
Google scholar
|
[143] |
Lindsey ARI, Bhattacharya T, Newton ILG, et al. Conflict in the intracellular lives of endosymbionts and viruses: a mechanistic look at Wolbachia-mediated pathogen-blocking. Viruses 2018;10:141.
CrossRef
Google scholar
|
[144] |
Ma E, Zhu Y, Liu Z, et al. Interaction of viruses with the insect intestine. Annu Rev Virol 2021;8:115–131.
CrossRef
Google scholar
|
[145] |
Mains JW, Kelly PH, Dobson KL, et al. Localized control of Aedes aegypti (Diptera: Culicidae) in Miami, FL, via inundative releases of Wolbachia-infected male mosquitoes. J Med Entomol 2019;56:1296–1303.
CrossRef
Google scholar
|
[146] |
Mancini MV, Damiani C, Accoti A, et al. Estimating bacteria diversity in different organs of nine species of mosquito by next generation sequencing. BMC Microbiol 2018;18:126.
CrossRef
Google scholar
|
[147] |
Mandal RK, Denny JE, Namazzi R, et al. Dynamic modulation of spleen germinal center reactions by gut bacteria during Plasmodium infection. Cell Rep 2021;35:109094.
CrossRef
Google scholar
|
[148] |
Martin-Martin I, Valenzuela Leon PC, Amo L, et al. Aedes aegypti sialokinin facilitates mosquito blood feeding and modulates host immunity and vascular biology. Cell Rep 2022;39:110648.
CrossRef
Google scholar
|
[149] |
Mateos-Hernández L, Obregón D, Maye J, et al. Anti-tick microbiota vaccine impacts ixodes ricinus performance during feeding. Vaccines 2020;8:702.
CrossRef
Google scholar
|
[150] |
McGraw EA, Merritt DJ, Droller JN, et al. Wolbachia density and virulence attenuation after transfer into a novel host. Proc Natl Acad Sci USA 2002;99:2918–2923.
CrossRef
Google scholar
|
[151] |
Mellink JJ, Vos BJ. Primary lymph node responses to mosquito bites. Z Parasitenkd 1977;51:187–198.
CrossRef
Google scholar
|
[152] |
Menard D, Dondorp A. Antimalarial drug resistance: a threat to malaria elimination. Cold Spring Harb Perspect Med 2017;7:a025619.
CrossRef
Google scholar
|
[153] |
Micieli MV, Glaser RL. Somatic Wolbachia (Rickettsiales: Rickettsiaceae) levels in Culex quinquefasciatus and Culex pipiens (Diptera: Culicidae) and resistance to West Nile virus infection. J Med Entomol 2014;51:189–199.
CrossRef
Google scholar
|
[154] |
Min KT, Benzer S. Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc Natl Acad Sci USA 1997;94:10792–10796.
CrossRef
Google scholar
|
[155] |
Minard G, Tran FH, Raharimalala FN, et al. Prevalence, genomic and metabolic profiles of Acinetobacter and Asaia associated with field-caught Aedes albopictus from Madagascar. FEMS Microbiol Ecol 2013;83:63–73.
CrossRef
Google scholar
|
[156] |
Molloy JC, Sommer U, Viant MR, et al. Wolbachia modulates lipid metabolism in Aedes albopictus mosquito cells. Appl Environ Microbiol 2016;82:3109–3120.
CrossRef
Google scholar
|
[157] |
Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, et al. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 2009;139:1268–1278.
CrossRef
Google scholar
|
[158] |
Mousson L, Martin E, Zouache K, et al. Wolbachia modulates Chikungunya replication in Aedes albopictus. Mol Ecol 2010;19:1953–1964.
CrossRef
Google scholar
|
[159] |
Mousson L, Zouache K, Arias-Goeta C, et al. The native Wolbachia symbionts limit transmission of dengue virus in aedes albopictus. PLoS Negl Trop Dis 2012;6:e1989.
CrossRef
Google scholar
|
[160] |
Mozūraitis R, Hajkazemian M, Zawada JW, et al. Male swarming aggregation pheromones increase female attraction and mating success among multiple African malaria vector mosquito species. Nat Ecol Evol 2020;4:1395–1401.
CrossRef
Google scholar
|
[161] |
Müller JM, Cahill MA, Rupec RA, et al. Antioxidants as well as oxidants activate c-fos via Ras-dependent activation of extracellular-signal-regulated kinase 2 and Elk-1. Eur J Biochem 1997;244:45–52.
CrossRef
Google scholar
|
[162] |
Musso D, Gubler DJ. Zika virus. Clin Microbiol Rev 2016;29:487–524.
CrossRef
Google scholar
|
[163] |
Muturi EJ, Bara JJ, Rooney AP, et al. Midgut fungal and bacterial microbiota of Aedes triseriatus and Aedes japonicus shift in response to La Crosse virus infection. Mol Ecol 2016a;25:4075–4090.
CrossRef
Google scholar
|
[164] |
Muturi EJ, Kim CH, Bara J, et al. Culex pipiens and Culex restuans mosquitoes harbor distinct microbiota dominated by few bacterial taxa. Parasit Vectors 2016b;9:18.
CrossRef
Google scholar
|
[165] |
Nelemans T, Kikkert M. Viral innate immune evasion and the pathogenesis of emerging RNA virus infections. Viruses 2019;11:961.
CrossRef
Google scholar
|
[166] |
Newton ILG, Savytskyy O, Sheehan KB. Wolbachia utilize host actin for efficient maternal transmission in Drosophila melanogaster. PLoS Pathog 2015;11:e1004798.
CrossRef
Google scholar
|
[167] |
Nguyen TH, Nguyen H Le, Nguyen TY, et al. Field evaluation of the establishment potential of wMelPop Wolbachia in Australia and Vietnam for dengue control. Parasit Vectors 2015;8:563.
CrossRef
Google scholar
|
[168] |
Nogaro SI, Hafalla JC, Walther B, et al. The breadth, but not the magnitude, of circulating memory B cell responses to P. falciparum increases with age/exposure in an area of low transmission. PLoS One 2011;6:e25582.
CrossRef
Google scholar
|
[169] |
Olajiga OM, Maldonado-Ruiz LP, Fatehi S, et al. Association of dengue infection with anti-alpha-gal antibodies, IgM, IgG, IgG1, and IgG2. Front Immunol 2022;13:1021016.
CrossRef
Google scholar
|
[170] |
Onyango MG, Ciota AT, Kramer LD. The vector—host—pathogen interface: the next frontier in the battle against mosquito-borne viral diseases? Front Cell Infect Microbiol 2020;10:564518.
CrossRef
Google scholar
|
[171] |
Onyango MG, Lange R, Bialosuknia S, et al. Zika virus and temperature modulate Elizabethkingia anophelis in Aedes albopictus. Parasit Vectors 2021;14:573.
CrossRef
Google scholar
|
[172] |
Osborne SE, Iturbe-Ormaetxe I, Brownlie JC, et al. Antiviral protection and the importance of Wolbachia density and tissue tropism in Drosophila simulans. Appl Environ Microbiol 2012;78:6922–6929.
CrossRef
Google scholar
|
[173] |
Osei-Poku J, Mbogo CM, Palmer WJ, et al. Deep sequencing reveals extensive variation in the gut microbiota of wild mosquitoes from Kenya. Mol Ecol 2012;21:5138–5150.
CrossRef
Google scholar
|
[174] |
Osier FHA, Fegan G, Polley SD, et al. Breadth and magnitude of antibody responses to multiple Plasmodium falciparum merozoite antigens are associated with protection from clinical malaria. Infect Immun 2008;76:2240–2248.
CrossRef
Google scholar
|
[175] |
Pan X, Zhou G, Wu J, et al. 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.
CrossRef
Google scholar
|
[176] |
Pang X, Xiao X, Liu Y, et al. Mosquito C-type lectins maintain gut microbiome homeostasis. Nat Microbiol 2016;1:16023.
CrossRef
Google scholar
|
[177] |
Pereira TN, Rocha MN, Sucupira PHF, et al. Wolbachia significantly impacts the vector competence of Aedes aegypti for Mayaro virus. Sci Rep 2018;8:6889.
CrossRef
Google scholar
|
[178] |
Perlmutter JI, Bordenstein SR. Microorganisms in the reproductive tissues of arthropods. Nat Rev Microbiol 2020;18:97–111.
CrossRef
Google scholar
|
[179] |
Prioritizing Diseases for Research and Development in Emergency Contexts. who.int/activities/prioritizing-diseases-for-research-and-development-in-emergency-contexts (30 January 2023, date last accessed).
|
[180] |
Petersen LR, Brault AC, Nasci RS. West Nile virus: review of the literature. JAMA 2013;310:308–315.
CrossRef
Google scholar
|
[181] |
Pierson TC, Diamond MS. The continued threat of emerging flaviviruses. Nat Microbiol 2020;5:796–812.
CrossRef
Google scholar
|
[182] |
Pike A, Dong Y, Dizaji NB, et al. Changes in the microbiota cause genetically modified Anopheles to spread in a population. Science 2017;357:1396–1399.
CrossRef
Google scholar
|
[183] |
Pinto SB, Riback TIS, Sylvestre G, 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.
CrossRef
Google scholar
|
[184] |
Pohl K, Cockburn IA. Innate immunity to malaria: the good, the bad and the unknown. Front Immunol 2022;13:914598.
CrossRef
Google scholar
|
[185] |
Ramirez JL, Souza-Neto J, Cosme RT, et al. Reciprocal tripartite interactions between the Aedes aegypti midgut microbiota, innate immune system and dengue virus influences vector competence. PLoS Negl Trop Dis 2012;6:e1561.
CrossRef
Google scholar
|
[186] |
Ramirez JL, Short SM, Bahia AC, et al. Chromobacterium Csp_P reduces malaria and dengue infection in vector mosquitoes and has entomopathogenic and in vitro anti-pathogen activities. PLoS Pathog 2014;10:e1004398.
CrossRef
Google scholar
|
[187] |
Rancès E, Ye YH, Woolfit M, et al. The relative importance of innate immune priming in Wolbachia-mediated dengue interference. PLoS Pathog 2012;8:e1002548.
CrossRef
Google scholar
|
[188] |
Ren N, Wang S, Shi C, et al. Dynamic surveillance of mosquitoes and their viromes in Wuhan during 2020. Zoonoses 2021;1:8.
CrossRef
Google scholar
|
[189] |
Ricci I, Damiani C, Scuppa P, et al. The yeast Wickerhamomyces anomalus (Pichia anomala) inhabits the midgut and reproductive system of the Asian malaria vector Anopheles stephensi. Environ Microbiol 2011;13:911–921.
CrossRef
Google scholar
|
[190] |
Rio RVM, Attardo GM, Weiss BL. Grandeur alliances: symbiont metabolic integration and obligate arthropod hematophagy. Trends Parasitol 2016;32:739–749.
CrossRef
Google scholar
|
[191] |
Rodgers FH, Gendrin M, Wyer CAS, et al. Microbiota-induced peritrophic matrix regulates midgut homeostasis and prevents systemic infection of malaria vector mosquitoes. PLoS Pathog 2017;13:e1006391.
CrossRef
Google scholar
|
[192] |
Romo H, Kenney JL, Blitvich BJ, et al. Restriction of Zika virus infection and transmission in Aedes aegypti mediated by an insect-specific flavivirus. Emerg Microbes Infect 2018;7:181.
CrossRef
Google scholar
|
[193] |
Romoli O, Schönbeck JC, Hapfelmeier S, et al. Production of germfree mosquitoes via transient colonisation allows stage-specific investigation of host–microbiota interactions. Nat Commun 2021;12:942.
CrossRef
Google scholar
|
[194] |
Rossi P, Ricci I, Cappelli A, et al. Mutual exclusion of Asaia and Wolbachia in the reproductive organs of mosquito vectors. Parasit Vectors 2015;8:278.
CrossRef
Google scholar
|
[195] |
Ryan PA, Turley AP, Wilson G, 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 2020;3:1547.
CrossRef
Google scholar
|
[196] |
Salem I, Ramser A, Isham N, et al. The gut microbiome as a major regulator of the gut–skin axis. Front Microbiol 2018;9:1459.
CrossRef
Google scholar
|
[197] |
Sannino DR, Dobson AJ, Edwards K, et al. The Drosophila melanogaster gut microbiota provisions thiamine to its host. MBio 2018;9:e00155–e00118.
CrossRef
Google scholar
|
[198] |
Saraiva RG, Fang J, Kang S, et al. Aminopeptidase secreted by Chromobacterium sp. Panama inhibits dengue virus infection by degrading the E protein. PLoS Negl Trop Dis 2018a;12:e0006443.
CrossRef
Google scholar
|
[199] |
Saraiva RG, Huitt-Roehl CR, Tripathi A, et al. Chromobacterium spp. mediate their anti-Plasmodium activity through secretion of the histone deacetylase inhibitor romidepsin. Sci Rep 2018b;8:6176.
CrossRef
Google scholar
|
[200] |
Sato Y, Ries S, Stenzel W, et al. The liver-stage plasmodium infection is a critical checkpoint for development of experimental cerebral malaria. Front Immunol 2019;10:2554.
CrossRef
Google scholar
|
[201] |
Schmid MA, Glasner DR, Shah S, et al. Mosquito saliva increases endothelial permeability in the skin, immune cell migration, and dengue pathogenesis during antibody-dependent enhancement. PLoS Pathog 2016;12:e1005676.
CrossRef
Google scholar
|
[202] |
Schneider BS, Soong L, Coffey LL, et al. Aedes aegypti saliva alters leukocyte recruitment and cytokine signaling by antigen-presenting cells during West Nile virus infection. PLoS One 2010;5:e11704.
CrossRef
Google scholar
|
[203] |
Schoggins JW. Interferon-stimulated genes: roles in viral pathogenesis. Curr Opin Virol 2014;6:40–46.
CrossRef
Google scholar
|
[204] |
Schreck CE, James J. Broth cultures of bacteria that attract female mosquitoes. Mosq News 1968;28:33–38.
|
[205] |
Scolari F, Casiraghi M, Bonizzoni M. Aedes spp. and their microbiota: a review. Front Microbiol 2019;10:2036.
CrossRef
Google scholar
|
[206] |
Segata N, Baldini F, Pompon J, et al. The reproductive tracts of two malaria vectors are populated by a core microbiome and by gender- and swarm-enriched microbial biomarkers. Sci Rep 2016;6:24207.
CrossRef
Google scholar
|
[207] |
Sharma P, Sharma S, Maurya RK, et al. Salivary glands harbor more diverse microbial communities than gut in Anopheles culicifacies. Parasit Vectors 2014;7:235.
CrossRef
Google scholar
|
[208] |
Sharma P, Rani J, Chauhan C, et al. Altered gut microbiota and immunity defines plasmodium vivax survival in Anopheles stephensi. Front Immunol 2020;11:609.
CrossRef
Google scholar
|
[209] |
Sharon G, Segal D, Ringo JM, et al. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc Natl Acad Sci USA 2010;107:20051–20056.
CrossRef
Google scholar
|
[210] |
Sharon G, Segal D, Zilber-Rosenberg I, et al. Symbiotic bacteria are responsible for diet-induced mating preference in Drosophila melanogaster, providing support for the hologenome concept of evolution. Gut Microbes 2011;2:190–192.
CrossRef
Google scholar
|
[211] |
Shaw WR, Marcenac P, Childs LM, et al. Wolbachia infections in natural Anopheles populations affect egg laying and negatively correlate with Plasmodium development. Nat Commun 2016;7:11772.
CrossRef
Google scholar
|
[212] |
Sheehan KB, Martin M, Lesser CF, et al. Identification and characterization of a Candidate Wolbachia pipientis Type IV effector that interacts with the actin cytoskeleton. MBio 2016;7:e00622–e00616.
CrossRef
Google scholar
|
[213] |
Shi C, Beller L, Wang L, et al. Bidirectional interactions between arboviruses and the bacterial and viral microbiota in Aedes aegypti and Culex quinquefasciatus. MBio 2022;13:e0102122.
CrossRef
Google scholar
|
[214] |
Shragai T, Tesla B, Murdock C, et al. Zika and chikungunya: mosquito- borne viruses in a changing world. Ann N Y Acad Sci 2017;1399:61–77.
CrossRef
Google scholar
|
[215] |
Silva JBL, Alves DM, Bottino-Rojas V, et al. Wolbachia and dengue virus infection in the mosquito Aedes fluviatilis (Diptera: Culicidae). PLoS One 2017;12:e181678.
CrossRef
Google scholar
|
[216] |
Sitati EM, Diamond MS. CD4+ T-cell responses are required for clearance of West Nile virus from the central nervous system. J Virol 2006;80:12060–12069.
CrossRef
Google scholar
|
[217] |
Skelton E, Rancès E, Frentiu FD, et al. A native Wolbachia endosymbiont does not limit dengue virus infection in the mosquito aedes notoscriptus (Diptera: Culicidae). J Med Entomol 2016;53:401–408.
CrossRef
Google scholar
|
[218] |
Sommer F, Bäckhed F. The gut microbiota-masters of host development and physiology. Nat Rev Microbiol 2013;11:227–238.
CrossRef
Google scholar
|
[219] |
Song X, Wang M, Dong L, et al. PGRP-LD mediatesA. stephensi vector competency by regulating homeostasis of microbiota-induced peritrophic matrix synthesis. PLoS Pathog 2018;14:e1006899.
CrossRef
Google scholar
|
[220] |
Song X, Zhong Z, Gao L, et al. Metabolic interactions between disease- transmitting vectors and their microbiota. Trends Parasitol 2022;38:697–708.
CrossRef
Google scholar
|
[221] |
Spitzen J, Smallegange RC, Takken W. Effect of human odours and positioning of CO2 release point on trap catches of the malaria mosquito Anopheles gambiae sensu stricto in an olfactometer. Physiol Entomol 2008;33:116–122.
CrossRef
Google scholar
|
[222] |
St. John AL, Rathore APS. Adaptive immune responses to primary and secondary dengue virus infections. Nat Rev Immunol 2019;19:218–230.
CrossRef
Google scholar
|
[223] |
Strand MR. Composition and functional roles of the gut microbiota in mosquitoes. Curr Opin Insect Sci 2018;28:59–65.
CrossRef
Google scholar
|
[224] |
Styer LM, Lim P-Y, Louie KL, et al. Mosquito saliva causes enhancement of West Nile virus infection in mice. J Virol 2011;85:1517–1527.
CrossRef
Google scholar
|
[225] |
Sun P, Nie K, Zhu Y, et al. A mosquito salivary protein promotes flavivirus transmission by activation of autophagy. Nat Commun 2020;11:260.
CrossRef
Google scholar
|
[226] |
Tawidian P, Coon KL, Jumpponen A, et al. Host-environment interplay shapes fungal diversity in mosquitoes. mSphere 2021;6:e0064621.
CrossRef
Google scholar
|
[227] |
Tchioffo MT, Boissière A, Abate L, et al. Dynamics of bacterial community composition in the malaria mosquito’s epithelia. Front Microbiol 2016;6:1500.
CrossRef
Google scholar
|
[228] |
Thackray LB, Handley SA, Gorman MJ, et al. Oral antibiotic treatment of mice exacerbates the disease severity of multiple flavivirus infections. Cell Rep 2018;22:3440–3453.e6.
CrossRef
Google scholar
|
[229] |
Thiberville SD, Moyen N, Dupuis-Maguiraga L, et al. Chikungunya fever: epidemiology, clinical syndrome, pathogenesis and therapy. Antiviral Res 2013;99:345–370.
CrossRef
Google scholar
|
[230] |
Travanty NV, Apperson CS, Ponnusamy L. A Diverse microbial community supports larval development and survivorship of the Asian Tiger Mosquito (Diptera: Culicidae). J Med Entomol 2019;56:632–640.
CrossRef
Google scholar
|
[231] |
Tremaroli V, Bäckhed F. Functional interactions between the gut microbiota and host metabolism. Nature 2012;489:242–249.
CrossRef
Google scholar
|
[232] |
Trzebny A, Slodkowicz-Kowalska A, Björkroth J, et al. Microsporidian infection in mosquitoes (Culicidae) is associated with gut microbiome composition and predicted gut microbiome functional content. Microb Ecol 2021;2021:1–17.
CrossRef
Google scholar
|
[233] |
Utarini A, Indriani C, Ahmad RA, et al; AWED Study Group. Efficacy of Wolbachia-infected mosquito deployments for the control of dengue. N Engl J Med 2021;384:2177–2186.
CrossRef
Google scholar
|
[234] |
Valzania L, Coon KL, Vogel KJ, et al. Hypoxia-induced transcription factor signaling is essential for larval growth of the mosquito Aedes aegypti. Proc Natl Acad Sci USA 2018a;115:457–465.
CrossRef
Google scholar
|
[235] |
Valzania L, Martinson VG, Harrison RE, et al. Both living bacteria and eukaryotes in the mosquito gut promote growth of larvae. PLoS Negl Trop Dis 2018b;12:e0006638e6638.
CrossRef
Google scholar
|
[236] |
Valzano M, Cecarini V, Cappelli A, et al. A yeast strain associated to Anopheles mosquitoes produces a toxin able to kill malaria parasites. Malar J 2016;15:21.
CrossRef
Google scholar
|
[237] |
van den Hurk AF, Hall-Mendelin S, Pyke AT, 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:e1892.
CrossRef
Google scholar
|
[238] |
Verhulst NO, Takken W, Dicke M, et al. Chemical ecology of interactions between human skin microbiota and mosquitoes. FEMS Microbiol Ecol 2010;74:1–9.
CrossRef
Google scholar
|
[239] |
Verhulst NO, Qiu YT, Beijleveld H, et al. Composition of human skin microbiota affects attractiveness to malaria mosquitoes. PLoS One 2011;6:e28991.
CrossRef
Google scholar
|
[240] |
Villarino NF, LeCleir GR, Denny JE, et al. Composition of the gut microbiota modulates the severity of malaria. Proc Natl Acad Sci USA 2016;113:2235–2240.
CrossRef
Google scholar
|
[241] |
Vue D, Tang Q. Zika virus overview: transmission, origin, pathogenesis, animal model and diagnosis. Zoonoses 2021;1:14.
CrossRef
Google scholar
|
[242] |
Waldock J, Olson KE, Christophides GK. Anopheles gambiae antiviral immune response to systemic O’nyong-nyong infection. PLoS Negl Trop Dis 2012;6:e1565.
CrossRef
Google scholar
|
[243] |
Walker GM. Pichia anomala: cell physiology and biotechnology relative to other yeasts. Antonie Van Leeuwenhoek 2011;99:25–34.
CrossRef
Google scholar
|
[244] |
Walker T, Johnson PH, Moreira LA, et al. The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 2011;476:450–453.
CrossRef
Google scholar
|
[245] |
Wang Y, Gilbreath TM, Kukutla P, et al. Dynamic gut microbiome across life history of the malaria mosquito Anopheles gambiae in Kenya. PLoS One 2011;6:e24767.
CrossRef
Google scholar
|
[246] |
Wang M, An Y, Gao L, et al. Glucose-mediated proliferation of a gut commensal bacterium promotes Plasmodium infection by increasing mosquito midgut pH. Cell Rep 2021a;35:108992.
CrossRef
Google scholar
|
[247] |
Wang Y, Eum JH, Harrison RE, et al. Riboflavin instability is a key factor underlying the requirement of a gut microbiota for mosquito development. Proc Natl Acad Sci USA 2021b;118:e2101080118.
CrossRef
Google scholar
|
[248] |
Wang YT, Shen RX, Xing D, et al. Metagenome sequencing reveals the midgut microbiota makeup of Culex pipiens quinquefasciatus and its possible relationship with insecticide resistance. Front Microbiol 2021c;12:228.
CrossRef
Google scholar
|
[249] |
Wang GH, Du J, Chu CY, et al. Symbionts and gene drive: two strategies to combat vector-borne disease. Trends Genet 2022;38:708–723.
CrossRef
Google scholar
|
[250] |
Weaver SC, Forrester NL. Chikungunya: evolutionary history and recent epidemic spread. Antiviral Res 2015;120:32–39.
CrossRef
Google scholar
|
[251] |
Weaver SC, Charlier C, Vasilakis N, et al. Zika, Chikungunya, and other emerging vector-borne viral diseases. Annu Rev Med 2018;69:395–408.
CrossRef
Google scholar
|
[252] |
Weiss GE, Traore B, Kayentao K, et al. The Plasmodium falciparum-specific human memory B cell compartment expands gradually with repeated malaria infections. PLoS Pathog 2010;6:e10009121–e10009113.
CrossRef
Google scholar
|
[253] |
Werren JH, Baldo L, Clark ME. Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 2008;6:741–751.
CrossRef
Google scholar
|
[254] |
White NJ, Pukrittayakamee S, Hien TT, et al. Malaria. Lancet 2014;383:723–735.
CrossRef
Google scholar
|
[255] |
Wilke ABB, Marrelli MT. Paratransgenesis: a promising new strategy for mosquito vector control. Parasit Vectors 2015;8:1–9.
CrossRef
Google scholar
|
[256] |
Winkler ES, Shrihari S, Hykes BL, et al. The intestinal microbiome restricts alphavirus infection and dissemination through a bile acid-Type I IFN signaling axis. Cell 2020;182:901–918.e18.
CrossRef
Google scholar
|
[257] |
World malaria report. 2022. who.int/teams/global-malaria-programme/reports/world-malaria-report-2022 (17 January 2023, date last accessed).
|
[258] |
Wu P, Sun P, Nie K, et al. A gut commensal bacterium promotes mosquito permissiveness to arboviruses. Cell Host Microbe 2019;25:101–112.e5.
CrossRef
Google scholar
|
[259] |
Xu J, Hopkins K, Sabin L, et al. ERK signaling couples nutrient status to antiviral defense in the insect gut. Proc Natl Acad Sci USA 2013;110:15025–15030.
CrossRef
Google scholar
|
[260] |
Yauch LE, Zellweger RM, Kotturi MF, et al. A protective role for dengue virus-specific CD8+ T cells. J Immunol 2009;182:4865–4873.
CrossRef
Google scholar
|
[261] |
Yauch LE, Prestwood TR, May MM, et al. CD4+ T cells are not required for the induction of dengue virus-specific CD8+ T Cell or antibody responses but contribute to protection after vaccination. J Immunol 2010;185:5405–5416.
CrossRef
Google scholar
|
[262] |
Yen JH, Barr AR. New hypothesis of the cause of cytoplasmic incompatibility in Culex pipiens L. Nature 1971;232:657–658.
CrossRef
Google scholar
|
[263] |
Yilmaz B, Portugal S, Tran TM, et al. Gut microbiota elicits a protective immune response against malaria transmission. Cell 2014;159:1277–1289.
CrossRef
Google scholar
|
[264] |
Yin C, Sun P, Yu X, et al. Roles of symbiotic microorganisms in arboviral infection of arthropod vectors. Trends Parasitol 2020;36:607–615.
CrossRef
Google scholar
|
[265] |
Yooseph S, Kirkness EF, Tran TM, et al. Stool microbiota composition is associated with the prospective risk of Plasmodium falciparum infection. BMC Genomics 2015;16:631.
CrossRef
Google scholar
|
[266] |
Yu X, Tong L, Zhang L, et al. Lipases secreted by a gut bacterium inhibit arbovirus transmission in mosquitoes. PLoS Pathog 2022;18:e1010552.
CrossRef
Google scholar
|
[267] |
Zélé F, Nicot A, Berthomieu A, et al. Wolbachia increases susceptibility to Plasmodium infection in a natural system. Proc Biol Sci 2014;281:20132837.
CrossRef
Google scholar
|
[268] |
Zhang G, Asad S, Khromykh AA, et al. Cell fusing agent virus and dengue virus mutually interact in Aedes aegypti cell lines. Sci Rep 2017;7:6935.
CrossRef
Google scholar
|
[269] |
Zhang H, Zhu Y, Liu Z, et al. A volatile from the skin microbiota of flavivirus-infected hosts promotes mosquito attractiveness. Cell 2022;185:2510–2522.e16.
CrossRef
Google scholar
|
[270] |
Zheng X, Zhang D, Li Y, et al. Incompatible and sterile insect techniques combined eliminate mosquitoes. Nature 2019;572:56–61.
CrossRef
Google scholar
|
[271] |
Zhou W, Rousset F, O’Neill S. Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc Biol Sci 1998;265:509–515.
CrossRef
Google scholar
|
[272] |
Zhu Y, Tong L, Nie K, et al. Host serum iron modulates dengue virus acquisition by mosquitoes. Nat Microbiol 2019;4:2405–2415.
CrossRef
Google scholar
|
/
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