Characterization of the microbiome of Aedes albopictus populations in different habitats from Spain and São Tomé

WHO. Launch of the Global Arbovirus Initiative. https://www.who.int/news-room/events/detail/2022/03/31/default-calendar/global-arbovirus-initiative (2022).Capinera, J. Encyclopedia of Entomology (Springer, 2008).Manni, M. et al. Genetic evidence for a worldwide chaotic dispersion pattern of the arbovirus vector, Aedes albopictus. PLoS Negl. Trop. Dis. 11, e0005332 (2017).Article 
PubMed 
PubMed Central 

Google Scholar 
Paupy, C., Delatte, H., Bagny, L., Corbel, V. & Fontenille, D. Aedes albopictus, an arbovirus vector: From the darkness to the light. Microbes Infect. 11, 1177–1185 (2009).Article 
CAS 
PubMed 

Google Scholar 
Effler, P. V. et al. Dengue fever, Hawaii, 2001–2002. Emerg. Infect. Dis. https://doi.org/10.3201/eid1105.041063 (2005).Article 
PubMed 
PubMed Central 

Google Scholar 
Ramchurn, S. K., Moheeput, K. & Goorah, S. S. An analysis of a short-lived outbreak of dengue fever in Mauritius. Euro Surveill. 14, (2009).Medlock, J. M. et al. An entomological review of invasive mosquitoes in Europe. Bull. Entomol. Res. https://doi.org/10.1017/S0007485315000103 (2015).Article 
PubMed 

Google Scholar 
Swan, T. et al. A literature review of dispersal pathways of Aedes albopictus across different spatial scales: implications for vector surveillance. Parasites Vectors 15, (2022).Eritja, R., Palmer, J. R. B., Roiz, D., Sanpera-Calbet, I. & Bartumeus, F. Direct evidence of adult Aedes albopictus dispersal by Car. Sci. Rep. 7, 14399 (2017).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Gratz, N. G. Critical review of the vector status of Aedes albopictus. Med. Vet. Entomol. https://doi.org/10.1111/j.0269-283X.2004.00513.x (2004).Article 
PubMed 

Google Scholar 
Hasan, S., Jamdar, S. F., Alalowi, M., Beaiji, A. A. A. & S. M.,. Dengue virus: A global human threat: Review of literature. J. Int. Soc. Prev. Commun. Dent. https://doi.org/10.4103/2231-0762.175416 (2016).Article 

Google Scholar 
Reis, S., Cornel, A. J., Melo, M., Pereira, H. & Loiseau, C. First record of Aedes albopictus (Skuse 1894) on São tomé island. Acta Trop. 171, 86–89 (2017).Article 
PubMed 

Google Scholar 
Goiri, F. et al. Progressive invasion of Aedes albopictus in Northern Spain in the period 2013–2018 and a possible association with the increase in insect bites. Int. J. Environ. Res. Public Health 17, 1678 (2020).Article 
PubMed 
PubMed Central 

Google Scholar 
Loiseau, C. et al. High endemism of mosquitoes on São Tomé and Príncipe Islands: Evaluating the general dynamic model in a worldwide island comparison. Insect. Conserv. Divers. 12, 69–79 (2019).Article 

Google Scholar 
Aranda, C., Eritja, R. & Roiz, D. First record and establishment of the mosquito Aedes albopictus in Spain. Med. Vet. Entomol. 20, 150–152 (2006).Article 
CAS 
PubMed 

Google Scholar 
European Centre for Disease Prevention and Control and European Food Safety Authority. Mosquito maps. European Centre for Disease Prevention and Control (ECDC). https://ecdc.europa.eu/en/disease-vectors/surveillance-and-disease-data/mosquito-maps (2024).Garrido, M. et al. Aedes albopictus in a recently invaded area in Spain: Effects of trap type, locality, and season on mosquito captures. Sci. Rep. 14, 2131 (2024).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Collantes, F. et al. Review of ten-years presence of Aedes albopictus in Spain 2004–2014: Known distribution and public health concerns. Parasit Vectors 8, 1–11 (2015).Article 

Google Scholar 
Lucati, F. et al. Multiple invasions, Wolbachia and human-aided transport drive the genetic variability of Aedes albopictus in the Iberian Peninsula. Sci. Rep. 12, 20682 (2022).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
ECDC. Autochthonous Cases of Dengue in Spain and France (2019).Monge, S. et al. Characterization of the first autochthonous dengue outbreak in Spain (August–September 2018). Acta Trop. 205, 105402 (2020).Article 
PubMed 

Google Scholar 
Navero-Castillejos, J. et al. Molecular characterization of imported and autochthonous dengue in northeastern spain. Viruses 13, 1910 (2021).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Gaio, A. D. O. et al. Contribution of midgut bacteria to blood digestion and egg production in Aedes aegypti (diptera: Culicidae) (L.). Parasit. Vectors 4, 1–10 (2011).Article 

Google Scholar 
Coon, K. L., Brown, M. R. & Strand, M. R. Gut bacteria differentially affect egg production in the anautogenous mosquito Aedes aegypti and facultatively autogenous mosquito Aedes atropalpus (Diptera: Culicidae). Parasit. Vectors 9, 1–12 (2016).Article 

Google Scholar 
Sicard, M., Bonneau, M. & Weill, M. Wolbachia prevalence, diversity, and ability to induce cytoplasmic incompatibility in mosquitoes. Curr. Opin. Insect Sci. https://doi.org/10.1016/j.cois.2019.02.005 (2019).Article 
PubMed 

Google Scholar 
Xi, Z., Ramirez, J. L. & Dimopoulos, G. The Aedes aegypti toll pathway controls dengue virus infection. PLoS Pathog. 4, e1000098 (2008).Article 
PubMed 
PubMed Central 

Google Scholar 
Dickson, L. B. et al. Carryover effects of larval exposure to different environmental bacteria drive adult trait variation in a mosquito vector. Sci. Adv. 3, e1700585 (2017).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Souza-Neto, J. A., Powell, J. R. & Bonizzoni, M. Aedes aegypti vector competence studies: A review. Infect. Genet. Evol. https://doi.org/10.1016/j.meegid.2018.11.009 (2019).Article 
PubMed 

Google Scholar 
Jupatanakul, N., Sim, S. & Dimopoulos, G. The insect microbiome modulates vector competence for arboviruses. Viruses. https://doi.org/10.3390/v6114294 (2014).Article 
PubMed 
PubMed Central 

Google Scholar 
Blagrove, M. S. C., Arias-Goeta, C., Di Genua, C., Failloux, A. B. & Sinkins, S. P. A Wolbachia wMel transinfection in Aedes albopictus is not detrimental to host fitness and inhibits Chikungunya virus. PLoS Negl. Trop. Dis. 7, e2152 (2013).Article 
PubMed 
PubMed Central 

Google Scholar 
Ahmad, N. A., Vythilingam, I., Lim, Y. A. L., Zabari, N. Z. A. M. & Lee, H. L. Detection of Wolbachia in Aedes albopictus and their effects on chikungunya virus. Am. J. Trop. Med. Hyg. 96, 148–156 (2017).Article 
PubMed 
PubMed Central 

Google Scholar 
Novakova, E. et al. Mosquito microbiome dynamics, a background for prevalence and seasonality of West Nile virus. Front. Microbiol. 8, (2017).Dada, N. et al. Considerations for mosquito microbiome research from the Mosquito Microbiome Consortium. Microbiome. https://doi.org/10.1186/s40168-020-00987-7 (2021).Article 
PubMed 
PubMed Central 

Google Scholar 
Collins, F. H. et al. Comparison of DNA-probe and isoenzyme methods for differentiating Anopheles gambiae and Anopheles arabiensis (Diptera: Culicidae). J. Med. Entomol. 25, 116–120 (1988).Article 
CAS 
PubMed 

Google Scholar 
Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200 (2011).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Rognes, T., Flouri, T., Nichols, B., Quince, C. & Mahé, F. VSEARCH: A versatile open source tool for metagenomics. PeerJ 2016, (2016).Eren, A. M. et al. Oligotyping: di erentiating between closely related microbial taxa using 16s rRNA gene data. Methods Ecol. Evol. 4, 1111–11119 (2013).Article 
PubMed 
PubMed Central 

Google Scholar 
Eren, A. M. et al. Minimum entropy decomposition: Unsupervised oligotyping for sensitive partitioning of high-throughput marker gene sequences. ISME J. 9, 968–979 (2015).Article 
CAS 
PubMed 

Google Scholar 
Angly, F. E. et al. CopyRighter: A rapid tool for improving the accuracy of microbial community profiles through lineage-specific gene copy number correction. Microbiome 2, (2014).Zhou, W., Rousset, F. & O’Neill, S. Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc. R. Soc. B Biol. Sci. 265, 209–515 (1998).Article 

Google Scholar 
Vassarstats. Vassarstats: Website for Statistical Computation). http://vassarstats.net/newcs.html.Bennett, K. L. et al. Dynamics and diversity of bacteria associated with the disease vectors Aedes aegypti and Aedes albopictus. Sci. Rep. 9, 12160 (2019).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Zhao, T. et al. Metagenome sequencing reveals the microbiome of Aedes albopictus and its possible relationship with dengue virus susceptibility. Front. Microbiol. 13, 891151 (2022).Article 
PubMed 
PubMed Central 

Google Scholar 
Scolari, F., Casiraghi, M. & Bonizzoni, M. Aedes spp. and their microbiota: A review. Front. Microbiol. https://doi.org/10.3389/fmicb.2019.02036 (2019).Article 
PubMed 
PubMed Central 

Google Scholar 
Vicente, C. S. L. et al. Characterization of bacterial communities associated with the pine sawyer beetle Monochamus galloprovincialis, the insect vector of the pinewood nematode Bursaphelenchus xylophilus. FEMS Microbiol. Lett. https://doi.org/10.1111/1574-6968.12232 (2013).Article 
PubMed 

Google Scholar 
Zhukova, M., Sapountzis, P., Schiøtt, M. & Boomsma, J. J. Diversity and transmission of gut bacteria in Atta and Acromyrmex leaf-cutting ants during development. Front. Microbiol. 8, 1942 (2017).Article 
PubMed 
PubMed Central 

Google Scholar 
Santos-Garcia, D., Mestre-Rincon, N., Zchori-Fein, E. & Morin, S. Inside out: Microbiota dynamics during host-plant adaptation of whiteflies. ISME J. 14, 847–856 (2020).Article 
PubMed 
PubMed Central 

Google Scholar 
Tabbabi, A., Mizushima, D., Yamamoto, D. S. & Kato, H. Sand flies and their microbiota. Parasitologia 2, 71–87 (2022).Article 

Google Scholar 
Lin, D. et al. Bacterial composition of midgut and entire body of laboratory colonies of Aedes aegypti and Aedes albopictus from Southern China. Parasit. Vectors 14, 1–13 (2021).Article 

Google Scholar 
Minard, G. et al. Pyrosequencing 16S rRNA genes of bacteria associated with wild tiger mosquito Aedes albopictus: A pilot study. Front. Cell Infect. Microbiol. 4, 59 (2014).Article 
PubMed 
PubMed Central 

Google Scholar 
Rosso, F. et al. Reduced diversity of gut microbiota in two Aedes mosquitoes species in areas of recent invasion. Sci. Rep. 8, 16091 (2018).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Brinker, P., Fontaine, M. C., Beukeboom, L. W. & Falcao Salles, J. Host, symbionts, and the microbiome: The missing tripartite interaction. Trends Microbiol. https://doi.org/10.1016/j.tim.2019.02.002 (2019).Article 
PubMed 

Google Scholar 
Scolari, F. et al. Exploring changes in the microbiota of Aedes albopictus: Comparison among breeding site water, larvae, and adults. Front. Microbiol. 12, 624170 (2021).Article 
PubMed 
PubMed Central 

Google Scholar 
Tuanudom, R., Yurayart, N., Rodkhum, C. & Tiawsirisup, S. Diversity of midgut microbiota in laboratory-colonized and field-collected Aedes albopictus (Diptera: Culicidae): A preliminary study. Heliyon 7, e08259 (2021).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Tortosa, P. et al. Wolbachia age-sex-specific density in Aedes albopictus: A host evolutionary response to Cytoplasmic Incompatibility?. PLoS One 5, e9700 (2010).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Lo, N., Casiraghi, M., Salati, E., Bazzocchi, C. & Bandi, C. How many Wolbachia supergroups exist?. Mol. Biol. Evol. https://doi.org/10.1093/oxfordjournals.molbev.a004087 (2002).Article 
PubMed 

Google Scholar 
Shaikevich, E., Bogacheva, A. & Ganushkina, L. Dirofilaria and Wolbachia in mosquitoes (Diptera: Culicidae) in central European Russia and on the Black Sea coast. Parasite. 26, (2019).Hu, Y. et al. Identification and molecular characterization of Wolbachia strains in natural populations of Aedes albopictus in China. Parasit. Vectors. 13, (2020).Puerta-Guardo, H. et al. Wolbachia in native populations of Aedes albopictus (Diptera: Culicidae) from Yucatan Peninsula, Mexico. J. Insect Sci. 20, (2020).Bueno-Marí, R. et al. Infecciones por Wolbachia pipientis en poblaciones de Aedes albopictus en la ciudad de València (España): Implicaciones para el control de mosquitos. Rev. Esp. Salud. Publica. 97, (2023).Werren, J. H., Windsor, D. & Guo, L. Distribution of Wolbachia among neotropical arthropods. Proc. R. Soc. B Biol. Sci. 262, 197–204 (1995).Article 
ADS 

Google Scholar 
Belo, F. Wolbachia Infection in European Populations of Aedes albopictus (Universidade Nova de Lisboa Instituto de Higiene e Medicina Tropical, 2021).
Google Scholar 
Kittayapong, P., Baisley, K. J., Sharpe, R. G., Baimai, V. & O’Neill, S. L. Maternal transmission efficiency of Wolbachia superinfections in Aedes albopictus populations in Thailand. Am. J. Trop. Med. Hyg. 66, 103–107 (2002).Article 
PubMed 

Google Scholar 
Bi, J. & Wang, Y. F. The effect of the endosymbiont Wolbachia on the behavior of insect hosts. Insect Sci. https://doi.org/10.1111/1744-7917.12731 (2020).Article 
PubMed 

Google Scholar 
Wiwatanaratanabutr, I. & Kittayapong, P. Effects of crowding and temperature on Wolbachia infection density among life cycle stages of Aedes albopictus. J. Invertebr. Pathol. 102, 220–224 (2009).Article 
PubMed 

Google Scholar 
Bamou, R. et al. Wolbachia detection in field-collected mosquitoes from Cameroon. Insects 12, 1133 (2021).Article 
PubMed 
PubMed Central 

Google Scholar 
Dobson, S. L., Rattanadechakul, W. & Marsland, E. J. Fitness advantage and cytoplasmic incompatibility in Wolbachia single- and superinfected Aedes albopictus. Heredity (Edinb) 93, 135–142 (2004).Article 
CAS 
PubMed 

Google Scholar 
Joanne, S. et al. Distribution and dynamics of Wolbachia infection in Malaysian Aedes albopictus. Acta Trop. 148, 38–45 (2015).Article 
PubMed 

Google Scholar 
Pichler, V. et al. Complex interplay of evolutionary forces shaping population genomic structure of invasive Aedes albopictus in southern Europe. PLoS Negl. Trop. Dis. 13, e0007554 (2019).Article 
PubMed 
PubMed Central 

Google Scholar 
Kotsakiozi, P. et al. Population genomics of the Asian tiger mosquito, Aedes albopictus: Insights into the recent worldwide invasion. Ecol. Evol. 7, 10143–10157 (2017).Article 
PubMed 
PubMed Central 

Google Scholar 
Alphey, L. Genetic control of mosquitoes. Annu. Rev. Entomol. 59, 205–224 (2014).Article 
CAS 
PubMed 

Google Scholar 
Mains, J. W., Brelsfoard, C. L., Rose, R. I. & Dobson, S. L. Female adult Aedes albopictus suppression by Wolbachia-infected male mosquitoes. Sci. Rep. 6, 33846 (2016).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Caputo, B. 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. 76, 1324–1332 (2020).Article 
CAS 
PubMed 

Google Scholar 

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