Midgut Microbiota of the Malaria Mosquito Vector Anopheles gambiae and Interactions with Plasmodium falciparum Infection

The susceptibility of Anopheles mosquitoes to Plasmodium infections relies on complex interactions between the insect vector and the malaria parasite. A number of studies have shown that the mosquito innate immune responses play an important role in controlling the malaria infection and that the str...

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Vydané v:	PLoS pathogens Ročník 8; číslo 5; s. e1002742
Hlavní autori:	Boissière, Anne, Tchioffo, Majoline T., Bachar, Dipankar, Abate, Luc, Marie, Alexandra, Nsango, Sandrine E., Shahbazkia, Hamid R., Awono-Ambene, Parfait H., Levashina, Elena A., Christen, Richard, Morlais, Isabelle
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	United States Public Library of Science 01.05.2012 Public Library of Science (PLoS)
Predmet:	Animals Anopheles - genetics Anopheles - immunology Anopheles - microbiology Anopheles - parasitology Aquatic insects Biodiversity Biology Breeding sites Digestive System - microbiology Digestive System - parasitology Disease transmission Enterobacter - genetics Enterobacter - immunology Environmental factors Flora Gene Expression Regulation Genomics Host-Parasite Interactions Insect Vectors - genetics Insect Vectors - immunology Insect Vectors - microbiology Larvae Life Sciences Malaria Malaria, Falciparum - genetics Malaria, Falciparum - immunology Malaria, Falciparum - parasitology Microbiology Mosquitoes Parasites Plasmodium falciparum - genetics Plasmodium falciparum - immunology Plasmodium falciparum - microbiology Populations and Evolution Vector-borne diseases
ISSN:	1553-7374, 1553-7366, 1553-7374
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Abstract	The susceptibility of Anopheles mosquitoes to Plasmodium infections relies on complex interactions between the insect vector and the malaria parasite. A number of studies have shown that the mosquito innate immune responses play an important role in controlling the malaria infection and that the strength of parasite clearance is under genetic control, but little is known about the influence of environmental factors on the transmission success. We present here evidence that the composition of the vector gut microbiota is one of the major components that determine the outcome of mosquito infections. A. gambiae mosquitoes collected in natural breeding sites from Cameroon were experimentally challenged with a wild P. falciparum isolate, and their gut bacterial content was submitted for pyrosequencing analysis. The meta-taxogenomic approach revealed a broader richness of the midgut bacterial flora than previously described. Unexpectedly, the majority of bacterial species were found in only a small proportion of mosquitoes, and only 20 genera were shared by 80% of individuals. We show that observed differences in gut bacterial flora of adult mosquitoes is a result of breeding in distinct sites, suggesting that the native aquatic source where larvae were grown determines the composition of the midgut microbiota. Importantly, the abundance of Enterobacteriaceae in the mosquito midgut correlates significantly with the Plasmodium infection status. This striking relationship highlights the role of natural gut environment in parasite transmission. Deciphering microbe-pathogen interactions offers new perspectives to control disease transmission.
AbstractList	The susceptibility of Anopheles mosquitoes to Plasmodium infections relies on complex interactions between the insect vector and the malaria parasite. A number of studies have shown that the mosquito innate immune responses play an important role in controlling the malaria infection and that the strength of parasite clearance is under genetic control, but little is known about the influence of environmental factors on the transmission success. We present here evidence that the composition of the vector gut microbiota is one of the major components that determine the outcome of mosquito infections. A. gambiae mosquitoes collected in natural breeding sites from Cameroon were experimentally challenged with a wild P. falciparum isolate, and their gut bacterial content was submitted for pyrosequencing analysis. The meta-taxogenomic approach revealed a broader richness of the midgut bacterial flora than previously described. Unexpectedly, the majority of bacterial species were found in only a small proportion of mosquitoes, and only 20 genera were shared by 80% of individuals. We show that observed differences in gut bacterial flora of adult mosquitoes is a result of breeding in distinct sites, suggesting that the native aquatic source where larvae were grown determines the composition of the midgut microbiota. Importantly, the abundance of Enterobacteriaceae in the mosquito midgut correlates significantly with the Plasmodium infection status. This striking relationship highlights the role of natural gut environment in parasite transmission. Deciphering microbe-pathogen interactions offers new perspectives to control disease transmission. The susceptibility of Anopheles mosquitoes to Plasmodium infections relies on complex interactions between the insect vector and the malaria parasite. A number of studies have shown that the mosquito innate immune responses play an important role in controlling the malaria infection and that the strength of parasite clearance is under genetic control, but little is known about the influence of environmental factors on the transmission success. We present here evidence that the composition of the vector gut microbiota is one of the major components that determine the outcome of mosquito infections. A. gambiae mosquitoes collected in natural breeding sites from Cameroon were experimentally challenged with a wild P. falciparum isolate, and their gut bacterial content was submitted for pyrosequencing analysis. The meta-taxogenomic approach revealed a broader richness of the midgut bacterial flora than previously described. Unexpectedly, the majority of bacterial species were found in only a small proportion of mosquitoes, and only 20 genera were shared by 80% of individuals. We show that observed differences in gut bacterial flora of adult mosquitoes is a result of breeding in distinct sites, suggesting that the native aquatic source where larvae were grown determines the composition of the midgut microbiota. Importantly, the abundance of Enterobacteriaceae in the mosquito midgut correlates significantly with the Plasmodium infection status. This striking relationship highlights the role of natural gut environment in parasite transmission. Deciphering microbe-pathogen interactions offers new perspectives to control disease transmission. The susceptibility of Anopheles mosquitoes to Plasmodium infections relies on complex interactions between the insect vector and the malaria parasite. A number of studies have shown that the mosquito innate immune responses play an important role in controlling the malaria infection and that the strength of parasite clearance is under genetic control, but little is known about the influence of environmental factors on the transmission success. We present here evidence that the composition of the vector gut microbiota is one of the major components that determine the outcome of mosquito infections. A. gambiae mosquitoes collected in natural breeding sites from Cameroon were experimentally challenged with a wild P. falciparum isolate, and their gut bacterial content was submitted for pyrosequencing analysis. The meta-taxogenomic approach revealed a broader richness of the midgut bacterial flora than previously described. Unexpectedly, the majority of bacterial species were found in only a small proportion of mosquitoes, and only 20 genera were shared by 80% of individuals. We show that observed differences in gut bacterial flora of adult mosquitoes is a result of breeding in distinct sites, suggesting that the native aquatic source where larvae were grown determines the composition of the midgut microbiota. Importantly, the abundance of Enterobacteriaceae in the mosquito midgut correlates significantly with the Plasmodium infection status. This striking relationship highlights the role of natural gut environment in parasite transmission. Deciphering microbe-pathogen interactions offers new perspectives to control disease transmission.The susceptibility of Anopheles mosquitoes to Plasmodium infections relies on complex interactions between the insect vector and the malaria parasite. A number of studies have shown that the mosquito innate immune responses play an important role in controlling the malaria infection and that the strength of parasite clearance is under genetic control, but little is known about the influence of environmental factors on the transmission success. We present here evidence that the composition of the vector gut microbiota is one of the major components that determine the outcome of mosquito infections. A. gambiae mosquitoes collected in natural breeding sites from Cameroon were experimentally challenged with a wild P. falciparum isolate, and their gut bacterial content was submitted for pyrosequencing analysis. The meta-taxogenomic approach revealed a broader richness of the midgut bacterial flora than previously described. Unexpectedly, the majority of bacterial species were found in only a small proportion of mosquitoes, and only 20 genera were shared by 80% of individuals. We show that observed differences in gut bacterial flora of adult mosquitoes is a result of breeding in distinct sites, suggesting that the native aquatic source where larvae were grown determines the composition of the midgut microbiota. Importantly, the abundance of Enterobacteriaceae in the mosquito midgut correlates significantly with the Plasmodium infection status. This striking relationship highlights the role of natural gut environment in parasite transmission. Deciphering microbe-pathogen interactions offers new perspectives to control disease transmission. The susceptibility of Anopheles mosquitoes to Plasmodium infections relies on complex interactions between the insect vector and the malaria parasite. A number of studies have shown that the mosquito innate immune responses play an important role in controlling the malaria infection and that the strength of parasite clearance is under genetic control, but little is known about the influence of environmental factors on the transmission success. We present here evidence that the composition of the vector gut microbiota is one of the major components that determine the outcome of mosquito infections. A. gambiae mosquitoes collected in natural breeding sites from Cameroon were experimentally challenged with a wild P. falciparum isolate, and their gut bacterial content was submitted for pyrosequencing analysis. The meta-taxogenomic approach revealed a broader richness of the midgut bacterial flora than previously described. Unexpectedly, the majority of bacterial species were found in only a small proportion of mosquitoes, and only 20 genera were shared by 80% of individuals. We show that observed differences in gut bacterial flora of adult mosquitoes is a result of breeding in distinct sites, suggesting that the native aquatic source where larvae were grown determines the composition of the midgut microbiota. Importantly, the abundance of Enterobacteriaceae in the mosquito midgut correlates significantly with the Plasmodium infection status. This striking relationship highlights the role of natural gut environment in parasite transmission. Deciphering microbe-pathogen interactions offers new perspectives to control disease transmission. During their development in the mosquito vector, Plasmodium parasites undergo complex developmental steps and incur severe bottlenecks. The largest parasite losses occur in the mosquito midgut where robust immune responses are activated. Variability in P. falciparum infection levels indicates that parasite transmission is the result of complex interactions between vectors and parasites, which rely on both genetic and environmental factors. However, in contrast to genetically encoded factors, the role of environmental factors in parasite transmission has received little attention. In this study, we characterized the midgut microbiota of mosquitoes derived from diverse breeding sites using pyrosequencing. We show that the composition of the midgut microbiota in adult mosquitoes exhibits great variability, which is likely determined by bacterial richness of the larval habitats. When field mosquitoes were collected at late immature stages in natural breeding sites and the emerging females challenged with Plasmodium falciparum in the laboratory, significant correlation was observed between P. falciparum infection and the presence of Enterobacteriaceae in the mosquito midgut. Greater understanding of these malaria-bacteria interactions may lead to novel malaria control strategies.
Author	Tchioffo, Majoline T. Shahbazkia, Hamid R. Marie, Alexandra Nsango, Sandrine E. Bachar, Dipankar Abate, Luc Morlais, Isabelle Awono-Ambene, Parfait H. Christen, Richard Levashina, Elena A. Boissière, Anne
AuthorAffiliation	Institut Pasteur, France 1 UMR MIVEGEC (IRD 224- CNRS 5290- UM1- UM2), Montpellier, France 5 Área Departamental de Engenharia Electrónica e Computação, Faculdade de Ciências e Tecnologia, Universidade do Algarve, Faro, Portugal 4 CNRS UPR 9022, Inserm U963, Université de Strasbourg, Strasbourg, France 3 UMR 7138 Systématique Adaptation Evolution, Université de Nice-Sophia Antipolis, Parc Valrose, France 2 Laboratoire de Recherche sur le Paludisme, IRD-OCEAC, BP288, Yaoundé, Cameroun
AuthorAffiliation_xml	– name: 1 UMR MIVEGEC (IRD 224- CNRS 5290- UM1- UM2), Montpellier, France – name: 3 UMR 7138 Systématique Adaptation Evolution, Université de Nice-Sophia Antipolis, Parc Valrose, France – name: 4 CNRS UPR 9022, Inserm U963, Université de Strasbourg, Strasbourg, France – name: 5 Área Departamental de Engenharia Electrónica e Computação, Faculdade de Ciências e Tecnologia, Universidade do Algarve, Faro, Portugal – name: Institut Pasteur, France – name: 2 Laboratoire de Recherche sur le Paludisme, IRD-OCEAC, BP288, Yaoundé, Cameroun
Author_xml	– sequence: 1 givenname: Anne surname: Boissière fullname: Boissière, Anne – sequence: 2 givenname: Majoline T. surname: Tchioffo fullname: Tchioffo, Majoline T. – sequence: 3 givenname: Dipankar surname: Bachar fullname: Bachar, Dipankar – sequence: 4 givenname: Luc surname: Abate fullname: Abate, Luc – sequence: 5 givenname: Alexandra surname: Marie fullname: Marie, Alexandra – sequence: 6 givenname: Sandrine E. surname: Nsango fullname: Nsango, Sandrine E. – sequence: 7 givenname: Hamid R. surname: Shahbazkia fullname: Shahbazkia, Hamid R. – sequence: 8 givenname: Parfait H. surname: Awono-Ambene fullname: Awono-Ambene, Parfait H. – sequence: 9 givenname: Elena A. surname: Levashina fullname: Levashina, Elena A. – sequence: 10 givenname: Richard surname: Christen fullname: Christen, Richard – sequence: 11 givenname: Isabelle surname: Morlais fullname: Morlais, Isabelle
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/22693451$$D View this record in MEDLINE/PubMed https://hal.science/hal-01546176$$DView record in HAL
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Copyright	2012 Boissière et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Boissière A, Tchioffo MT, Bachar D, Abate L, Marie A, et al. (2012) Midgut Microbiota of the Malaria Mosquito Vector Anopheles gambiae and Interactions with Plasmodium falciparum Infection. PLoS Pathog 8(5): e1002742. doi:10.1371/journal.ppat.1002742 Distributed under a Creative Commons Attribution 4.0 International License Boissière et al. 2012
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Snippet	The susceptibility of Anopheles mosquitoes to Plasmodium infections relies on complex interactions between the insect vector and the malaria parasite. A number... The susceptibility of Anopheles mosquitoes to Plasmodium infections relies on complex interactions between the insect vector and the malaria parasite. A...
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SubjectTerms	Animals Anopheles - genetics Anopheles - immunology Anopheles - microbiology Anopheles - parasitology Aquatic insects Biodiversity Biology Breeding sites Digestive System - microbiology Digestive System - parasitology Disease transmission Enterobacter - genetics Enterobacter - immunology Environmental factors Flora Gene Expression Regulation Genomics Host-Parasite Interactions Insect Vectors - genetics Insect Vectors - immunology Insect Vectors - microbiology Larvae Life Sciences Malaria Malaria, Falciparum - genetics Malaria, Falciparum - immunology Malaria, Falciparum - parasitology Microbiology Mosquitoes Parasites Plasmodium falciparum - genetics Plasmodium falciparum - immunology Plasmodium falciparum - microbiology Populations and Evolution Vector-borne diseases
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Title	Midgut Microbiota of the Malaria Mosquito Vector Anopheles gambiae and Interactions with Plasmodium falciparum Infection
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