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12 results on '"Anne Boissière"'

1. Population genomic evidence of Plasmodium vivax Southeast Asian origin

Author

Barthélémy Ngoubangoye, Sandrine Houzé, Anne Boissière, Josquin Daron, Larson Boundenga, Michael C. Fontaine, François Renaud, Franck Prugnolle, Jean-François Trape, Patrick Durand, Virginie Rougeron, Céline Arnathau, Christine Sidobre, Fontaine lab, Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Centre International de Recherches Médicales de Franceville (CIRMF), Services de Maladies Infectieuses et Tropicales [CHU Bichat], AP-HP - Hôpital Bichat - Claude Bernard [Paris], Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP), Health, Emergence, Adaptation and Transmission (MIVEGEC-HEAT), Processus Écologiques et Évolutifs au sein des Communautés (PEEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes (URMITE), Institut de Recherche pour le Développement (IRD)-Aix Marseille Université (AMU)-Institut National de la Santé et de la Recherche Médicale (INSERM)-IFR48, Institut des sciences biologiques (INSB-CNRS)-Institut des sciences biologiques (INSB-CNRS)-Centre National de la Recherche Scientifique (CNRS), Groningen Institute for Evolutionary Life Sciences [Groningen] (GELIFES), University of Groningen [Groningen], Diversity, ecology, evolution & Adaptation of arthropod vectors (MIVEGEC-DEEVA), Evolution des Systèmes Vectoriels (ESV), INSB-INSB-Centre National de la Recherche Scientifique (CNRS), Fontaine, Michael, Génétique et évolution des maladies infectieuses (GEMI), and Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Génétique et évolution des maladies infectieuses (GEMI)

Subjects
030231 tropical medicine, Population, Plasmodium vivax, Biology, Southeast asian, 03 medical and health sciences, 0302 clinical medicine, [SDV.MHEP.MI]Life Sciences [q-bio]/Human health and pathology/Infectious diseases, parasitic diseases, Genetic variation, [SDV.BID.EVO] Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], Genetics, Clade, education, Research Articles, 030304 developmental biology, Evolutionary Biology, 0303 health sciences, education.field_of_study, Multidisciplinary, Phylogenetic tree, [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], SciAdv r-articles, respiratory system, biology.organism_classification, 3. Good health, [SDE.BE] Environmental Sciences/Biodiversity and Ecology, Genetic marker, Evolutionary biology, [SDV.MHEP.MI] Life Sciences [q-bio]/Human health and pathology/Infectious diseases, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, human activities, Research Article, Founder effect
Abstract

Characterization of the worldwide genetic diversity of 447 P. vivax strains shows evidence for a Southeast Asian origin., Plasmodium vivax is the most common and widespread human malaria parasite. It was recently proposed that P. vivax originates from sub-Saharan Africa based on the circulation of its closest genetic relatives (P. vivax-like) among African great apes. However, the limited number of genetic markers and samples investigated questions the robustness of this hypothesis. Here, we extensively characterized the genomic variations of 447 human P. vivax strains and 19 ape P. vivax-like strains collected worldwide. Phylogenetic relationships between human and ape Plasmodium strains revealed that P. vivax is a sister clade of P. vivax-like, not included within the radiation of P. vivax-like. By investigating various aspects of P. vivax genetic variation, we identified several notable geographical patterns in summary statistics in function of the increasing geographic distance from Southeast Asia, suggesting that P. vivax may have derived from a single area in Asia through serial founder effects.

Published
2021
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2. Lower mgpB diversity in macrolide-resistant Mycoplasma genitalium infecting men visiting two sexually transmitted infection clinics in Montpellier, France

Author

Manon Lounnas, Jennifer Guiraud, Anne-Laure Bañuls, Anne Boissière, Sabine Pereyre, Eric Elguero, Sylvain Godreuil, Chloé Le Roy, Cécile Bébéar, Institut de Recherche pour le Développement (IRD), Laboratoire Mixte International Drug Resistance in Southeast Asia (LMI DRISA), Institut Pasteur du Cambodge, Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP)-Oxford University Clinical Research Unit [Ho Chi Minh City] (OUCRU)-Fondation Mérieux-University of sciences and technologies of hanoi (USTH)-Center of Infectiology Lao-Christophe Mérieux [Vientiane] (CILM), Centre de Recherche en Ecologie et Evolution de la Santé (CREES), USC IHMC - Infections humaines à mycoplasmes et à chlamydiae, Institut National de la Recherche Agronomique (INRA), Du gène à l'écosystème (MIVEGEC-GeneSys), Pathogènes, Environnement, Santé Humaine (EPATH), Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), and Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])

Subjects
0301 basic medicine, Microbiology (medical), Male, [SDV]Life Sciences [q-bio], 030106 microbiology, Sexually Transmitted Diseases, Single-nucleotide polymorphism, Mycoplasma genitalium, Men who have sex with men, 03 medical and health sciences, Pre-exposure prophylaxis, Sexual and Gender Minorities, 0302 clinical medicine, Antibiotic resistance, Drug Resistance, Bacterial, Prevalence, Medicine, Humans, Pharmacology (medical), Mycoplasma Infections, 030212 general & internal medicine, Typing, Homosexuality, Male, ComputingMilieux_MISCELLANEOUS, Pharmacology, biology, Molecular epidemiology, Transmission (medicine), business.industry, biology.organism_classification, Virology, 3. Good health, Anti-Bacterial Agents, Infectious Diseases, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, Female, France, Macrolides, business
Abstract

Objectives Men engaged in high-risk sexual behaviour, such as MSM, are likely to be infected by resistant Mycoplasma genitalium strains. Understanding the transmission dynamics is challenging. We aimed to investigate the molecular epidemiology of M. genitalium in men visiting sexually transmitted infection (STI) clinics. Patients and methods Between June 2017 and February 2018, 95 M. genitalium-positive specimens from 78 men, including 76.9% MSM, visiting two STI clinics in Montpellier, France, were analysed for SNPs in the mgpB adhesin gene and number of tandem repeats in the MG_309 gene. Macrolide and fluoroquinolone resistance were determined. Typing results were compared with antibiotic resistance, sexual behaviour, sampling site, HIV pre-exposure prophylaxis (PrEP) usage and HIV status. Results Thirty-eight mgpB STs were identified, including 23 new STs, with ST4 being most prevalent. The mgpB/MG_309 typing method identified 52 genetic profiles, resulting in a discriminatory index of 0.979. Macrolide and fluoroquinolone resistance-associated mutations were detected in 58.3% and 10.8% of patients, respectively. The macrolide resistance rate was higher among MSM than among men who have sex with women only (68.4% versus 9.1%; adjusted OR, 1.57; 95% CI, 1.13–2.18; P = 0.007). A lower mgpB diversity of 0.870 was found among macrolide-resistant strains in comparison with 0.978 in macrolide-susceptible strains, with an over-representation of mgpB ST62 and ST153. Conclusions Although macrolide resistance spread appears polyclonal in M. genitalium, the lower diversity of mgpB types among macrolide-resistant strains may reflect the easier spread of a few specific mgpB types or the occurrence of sexual networks among MSM.

Published
2020
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3. Population genomic evidence of a Southeast Asian origin of Plasmodium vivax

Author

Patrick Durant, Anne Boissière, Larson Boundenga, Céline Arnathau, Sandrine Houzé, Christine Sidobre, Virginie Rougeron, François Renaud, Michael C. Fontaine, Franck Prugnolle, Josquin Daron, Barthélémy Ngoubangoye, and Jean-François Trape

Subjects
0303 health sciences, education.field_of_study, biology, 030231 tropical medicine, Plasmodium vivax, Population, biology.organism_classification, Southeast asian, medicine.disease, 3. Good health, 03 medical and health sciences, 0302 clinical medicine, Genetic marker, Evolutionary biology, Genetic variation, parasitic diseases, medicine, Clade, education, Malaria, 030304 developmental biology, Founder effect
Abstract

Plasmodium vivaxis the most prevalent and widespread human malaria parasite, with almost three billion people living at risk of infection. With the discovery of its closest genetic relatives in African great apes (Plasmodium vivax-like), the origin ofP. vivaxhas been proposed to be located in the sub-Saharan African area. However, the limited number of genetic markers and samples investigated questioned the robustness of this result. Here, we examined the population genomic variation of 447 humanP. vivaxstrains and 19 apeP. vivax-likestrains originating from 24 different countries across the world. We identified 2,005,455 high quality single-nucleotide polymorphism loci allowing us to conduct an extensive characterization to date ofP. vivaxworldwide genetic variation. Phylogenetic relationships between human and apePlasmodiumrevealed thatP. vivaxis a sister clade ofP. vivax-like, not included within the radiation ofP. vivax-like. By investigating a variety of aspects ofP. vivaxvariation, we identified several striking geographical patterns in summary statistics as function of increasing geographic distance from Southeast Asia, suggesting thatP. vivaxmay derived from serial founder effects from a single origin located in Asia.

Published
2020
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4. Mosquito microevolution drives Plasmodium falciparum dynamics

Author

Priscila Bascunan, Assetou Diarra, Parfait Awono-Ambene, Roch K. Dabiré, Modibo Mariko, Isabelle Morlais, Elena A. Levashina, Evans K. Rono, Mouctar Diallo, Flaminia Catteruccia, Paola Carrillo-Bustamante, Julien Pompon, Sandrine E. Nsango, Paul O. Mireji, Cynthia V. Yapto, Markus Gildenhard, Ramata Mariko, Djibril Sangaré, Anne Boissière, Hanne Krüger, Abdulaye Diabaté, Djeneba Camara, Alou Traoré, Yara Reis, Janis Thailayil, Daniel K. Masiga, Pamela B. Seda, Martin K. Rono, Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Université de Douala, Réponse immunitaire et developpement chez les insectes (RIDI - UPR 9002), Institut de biologie moléculaire et cellulaire (IBMC), Université de Strasbourg (UNISTRA)-Centre National de la Recherche Scientifique (CNRS)-Université de Strasbourg (UNISTRA)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Laboratoire d’Entomologie Médicale, Organisation de Coordination pour la lutte contre les Endémies en Afrique Centrale, Institut de Recherche en Sciences de la Santé (IRSS), CNRST, International Centre of Insect Physiology and Ecology (ICIPE), ICIPE, Dipartimento di Medicina Sperimentale e Scienze Biochimiche, Università degli Studi di Perugia (UNIPG), Department of Epidemiology of Parasitic Diseases, Université de Bamako-Malaria Research and Training Centre, Université de Bamako, Savoirs, Textes, Langage (STL) - UMR 8163 (STL), Université de Lille-Centre National de la Recherche Scientifique (CNRS), Université de Strasbourg (UNISTRA)-Institut de biologie moléculaire et cellulaire (IBMC), Université de Strasbourg (UNISTRA)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM), Transmission-Interactions-Adaptations hôtes/vecteurs/pathogènes (MIVEGEC-TRIAD), Evolution des Systèmes Vectoriels (ESV), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), and Università degli Studi di Perugia = University of Perugia (UNIPG)

Subjects
Microbiology (medical), Genotype, Rain, [SDV]Life Sciences [q-bio], Plasmodium falciparum, Immunology, Population, Mosquito Vectors, Mali, Applied Microbiology and Biotechnology, Microbiology, Plasmodium, Article, Evolution, Molecular, 03 medical and health sciences, Species Specificity, Anopheles, parasitic diseases, Prevalence, Genetics, medicine, Animals, Humans, education, Ecosystem, ComputingMilieux_MISCELLANEOUS, 030304 developmental biology, 0303 health sciences, education.field_of_study, [SDV.GEN]Life Sciences [q-bio]/Genetics, biology, 030306 microbiology, Ecology, Temperature, Microevolution, Cell Biology, biology.organism_classification, medicine.disease, Malaria, 3. Good health, Genetic structure, [SDE]Environmental Sciences, Insect Proteins, Evolutionary ecology, Seasons
Abstract

Malaria, a major cause of child mortality in Africa, is engendered by Plasmodium parasites that are transmitted by anopheline mosquitoes. Fitness of Plasmodium parasites is closely linked to the ecology and evolution of its anopheline vector. However, whether the genetic structure of vector populations impacts malaria transmission remains unknown. Here, we describe a partitioning of the African malaria vectors into generalists and specialists that evolve along ecological boundaries. We next identify the contribution of mosquito species to Plasmodium abundance using Granger causality tests for time-series data collected over two rainy seasons in Mali. We find that mosquito microevolution, defined by changes in the genetic structure of a population over short ecological timescales, drives Plasmodium dynamics in nature, whereas vector abundance, infection prevalence, temperature and rain have low predictive values. Our study demonstrates the power of time-series approaches in vector biology and highlights the importance of focusing local vector control strategies on mosquito species that drive malaria dynamics. A combination of genetic analyses of Anopheles species across sub-Saharan Africa, time-series quantification of Plasmodium falciparum prevalence in mosquitoes and Granger causality statistical testing reveals that changes in the genetic structure of a population over short ecological timescales drive Plasmodium dynamics in nature.

Published
2019
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5. An epidemiologically successful Escherichia coli sequence type modulates Plasmodium falciparum infection in the mosquito midgut

Author

Geoffrey Gimonneau, Isabelle Morlais, Anne Boissière, Majoline T. Tchioffo, Antoine Berry, Damien Dubois, Sandrine E. Nsango, Eric Oswald, Luc Abate, Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Transmission-Interactions-Adaptations hôtes/vecteurs/pathogènes (MIVEGEC-TRIAD), Evolution des Systèmes Vectoriels (ESV), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Université de Douala, Laboratoire de Recherche sur le Paludisme, Organization de Coordination pour la lutte contre les Endémies en Afrique Centrale (OCEAC), Organization de Coordination pour la lutte contre les Endémies en Afrique Centrale, Centre de Physiopathologie Toulouse Purpan (CPTP), Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Laboratoire de Bactériologie-Hygiène [Toulouse], and CHU Toulouse [Toulouse]

Subjects
0301 basic medicine, [SDV]Life Sciences [q-bio], L73 - Maladies des animaux, medicine.disease_cause, Plasmodium, Intestin, Interactions biologiques, Parasite inhibition, Intra-specific variation, Malaria, Falciparum, ComputingMilieux_MISCELLANEOUS, Phylogeny, Inhibition, Sequence type (ST95), biology, Anopheles, 3. Good health, Épidémiologie, Infectious Diseases, Insect Proteins, L72 - Organismes nuisibles des animaux, Développement biologique, Signal Transduction, Microbiology (medical), Relation hôte parasite, 030106 microbiology, Plasmodium falciparum, Virulence, Microbiology, 03 medical and health sciences, Variation génétique, parasitic diseases, Genetics, medicine, Escherichia coli, Animals, mécanisme de défense, Molecular Biology, Transmission des maladies, Ecology, Evolution, Behavior and Systematics, fungi, Midgut, biology.organism_classification, medicine.disease, Virology, Gastrointestinal Microbiome, Molecular Typing, 030104 developmental biology, Gene Expression Regulation, Immunité, Digestive System, Bacteria, Malaria
Abstract

Malaria transmission relies on the successful development of Plasmodium parasites in the Anopheles mosquito vector. Within the mosquito midgut, malaria parasites encounter a resident bacterial flora and parasite-bacteria interactions modulate Plasmodium development. The mechanisms by which the bacteria interact with malaria parasites are still unknown. The intestinal microbiota could regulate immune signaling pathways or produce bacterial compounds that block Plasmodium development. In this study, we characterized Escherichia coli strains previously isolated from the Anopheles mosquito midgut and investigated the putative role of two E. coli clones, 444(ST95) and 351(ST73), on parasite development. Sporogonic development was significantly impacted by exposure to clone 444(ST95) whereas prevalence and intensity of infection were not different in mosquitoes challenged with 351(ST73) as compared to control mosquitoes. This result indicates midgut bacteria exhibit intra-specific variation in their ability to inhibit Plasmodium development. Expression patterns of immune genes differed between mosquitoes challenged with 444(ST95) and 351(ST73) and examination of the luminal midgut surface by transmission electron microscopy revealed distinct effects of bacterial exposure on midgut epithelial cells. The 444(ST95) clone strongly affected mosquito survival and parasite development and this could be associated to the Hemolysin F or other toxins released by the bacteria. Further studies will be needed to decipher the virulence factors and to determine their contribution to the observed phenotype of the 444(ST95) E. coli strain that belongs to the epidemiological ST95 clonal group responsible for extra intestinal infections in human and other animals.

Published
2016
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6. Composition of Anopheles coluzzii and Anopheles gambiae microbiota from larval to adult stages

Author

Anne Boissière, Luc Abate, Parfait Awono-Ambene, Geoffrey Gimonneau, Richard Christen, Isabelle Morlais, Majoline T. Tchioffo, Sandrine E. Nsango, Symbiose Marine (SM), Evolution Paris Seine, Université des Antilles et de la Guyane (UAG)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles et de la Guyane (UAG)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS), Institut de Recherche pour le Developpement (IRD), Agence Nationale de la Recherche [ANR-11-BSV7-009-01], European Union [242095-EVIMalaR, 223601-MALVECBLOK], Infectiopole Sud foundation, Université des Antilles et de la Guyane (UAG)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Nice Sophia Antipolis (1965 - 2019) (UNS), and COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles et de la Guyane (UAG)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Nice Sophia Antipolis (1965 - 2019) (UNS)

Subjects
Identification, Anopheles gambiae, Stade de développement animal, habitat, Larve, Insect, L73 - Maladies des animaux, Intestin, Epithelium, RNA, Ribosomal, 16S, Phylogeny, media_common, 0303 health sciences, Larva, Ecology, [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], Microbiota, Anopheles, Environmental exposure, Biodiversity, Anopheles coluzzii, 3. Good health, Infectious Diseases, Epithelia, L72 - Organismes nuisibles des animaux, Microbiology (medical), media_common.quotation_subject, Biology, Microbiology, Life history theory, 03 medical and health sciences, parasitic diseases, Genetics, Animals, Molecular Biology, Ecology, Evolution, Behavior and Systematics, 030304 developmental biology, Life Cycle Stages, Bacteria, 030306 microbiology, Flore microbienne, Larval habitats, fungi, Sequence Analysis, DNA, biology.organism_classification, Malaria, Milieu aquatique, Microbial population biology, Pyrosequencing, Metagenome, flore bactérienne
Abstract

International audience; During their immature life stages, malaria mosquitoes are exposed to a wide array of microbes and contaminants from the aquatic habitats. Although prior studies have suggested that environmental exposure shapes the microbial community structure in the adult mosquito, most reports have focused on laboratory-based experiments and on a single mosquito epithelium, the gut. In this study, we investigated the influence of the breeding site on the development of the Anopheles coluzzii and Anopheles gambiae microbiota in natural conditions. We characterized bacterial communities from aquatic habitats, at surface microlayer and subsurface water levels, to freshly emerge adult mosquitoes using multiplexed 16S rRNA gene pyrosequencing and we separately analyzed the microbiota associated with the different epithelia of adult individual, midguts, ovaries and salivary glands. We found that the distribution of bacterial communities in the aquatic habitats differed according to the depth of water collections. Inter-individual variation of bacterial composition was large in larvae guts but adult mosquitoes from a same breeding site shared quite similar microbiota. Although some differences in bacterial abundances were highlighted between the different epithelia of freshly emerged An. coluzzii and An. gambiae, an intriguing feature from our study is the particular similarity of the overall bacterial communities. Our results call for further investigations on the bacterial population dynamics in the different tissues to determine the distinctive characteristics of each microbiota during the mosquito lifespan and to identify specific interactions between certain key phyla or species and the insect life history traits.

Published
2014
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7. Correction: Modulation of Malaria Infection in Anopheles gambiae Mosquitoes Exposed to Natural Midgut Bacteria

Author

Anne Boissière, Parfait Awono-Ambene, Antoine Berry, Sandrine E. Nsango, Thomas S. Churcher, Isabelle Morlais, Geoffrey Gimonneau, Richard Christen, Luc Abate, and Majoline T. Tchioffo

Subjects
Veterinary medicine, Multidisciplinary, biology, Science, Anopheles gambiae, Correction, Midgut, biology.organism_classification, medicine.disease, parasitic diseases, medicine, Medicine, Parasite hosting, Bacteria, Malaria
Abstract

There were multiple errors in the second paragraph of the Effect of bacterial challenge on P. falciparum development section of the Results: "When efficacy was measured as changes in oocyst intensity, the bacterial challenge had no effect irrespective of the oocyst intensity in the control group (Figure 3C). However, the reduction in oocyst prevalence due to the bacterial exposure was lower when parasite exposure was higher – in feedings that gave rise to the highest oocyst intensities in the PBS control, the bacterial challenge had almost no effect (Figure 3B)." In addition, an affiliation of the ninth author is missing: In addition to institution number 7, Antoine Berry is also affiliated with the the following institution: Centre de Physiopathologie de Toulouse-Purpan, Institut National de la Sante et de la Recherche Medicale, UMR1043, CNRS UMR5282, Universite de Toulouse Paul Sabatier, Toulouse, France.

Published
2013

8. Evaluation of a real-time quantitative PCR to measure the wild Plasmodium falciparum infectivity rate in salivary glands of Anopheles gambiae

Author

Alexandra Marie, Sylvie Cornelie, Anne Boissière, Anne Poinsignon, Majoline Tchioffo Tsapi, Franck Remoue, Isabelle Morlais, Parfait Awono-Ambene, Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Transmission-Interactions-Adaptations hôtes/vecteurs/pathogènes (MIVEGEC-TRIAD), Evolution des Systèmes Vectoriels (ESV), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Organisation de Coordination pour la lutte contre les Endémies en Afrique Centrale (OCEAC), Vector Control Group (MIVEGEC-VCG), Centre de Recherche Entomologique de Cotonou (CREC), Ministère de la Santé, Savoirs, Textes, Langage (STL) - UMR 8163 (STL), Université de Lille-Centre National de la Recherche Scientifique (CNRS), Laboratoire d’Entomologie Médicale, Organisation de Coordination pour la lutte contre les Endémies en Afrique Centrale, Épidémiologie et prévention : environnement et efficacité des interventions (EPIPREV), Laboratoire de Recherche sur le Paludisme, Organization de Coordination pour la lutte contre les Endémies en Afrique Centrale (OCEAC), and Organization de Coordination pour la lutte contre les Endémies en Afrique Centrale

Subjects
Anopheles gambiae, [SDV]Life Sciences [q-bio], 030231 tropical medicine, Plasmodium falciparum, Real-Time Polymerase Chain Reaction, Sensitivity and Specificity, Parasite Load, Salivary Glands, 03 medical and health sciences, Quantitative PCR, 0302 clinical medicine, CSP, Anopheles, Multiplex polymerase chain reaction, parasitic diseases, medicine, Gametocyte, Animals, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, ComputingMilieux_MISCELLANEOUS, 030304 developmental biology, 0303 health sciences, biology, Salivary gland, Methodology, Multiplex PCR, biology.organism_classification, Virology, Molecular biology, 3. Good health, Circumsporozoite protein, CSP-ELISA, PCR, Infectious Diseases, medicine.anatomical_structure, Real-time polymerase chain reaction, Parasitology, Female, ELISA, Entomology, Quantitative
Abstract

Background: Evaluation of malaria sporozoite rates in the salivary glands of Anopheles gambiae is essential for estimating the number of infective mosquitoes, and consequently, the entomological inoculation rate (EIR). EIR is a key indicator for evaluating the risk of malaria transmission. Although the enzyme-linked immunosorbent assay specific for detecting the circumsporozoite protein (CSP-ELISA) is routinely used in the field, it presents several limitations. A multiplex PCR can also be used to detect the four species of Plasmodium in salivary glands. The aim of this study was to evaluate the efficacy of a real-time quantitative PCR in detecting and quantifying wild Plasmodium falciparum in the salivary glands of An. gambiae. Methods: Anopheles gambiae (n=364) were experimentally infected with blood from P. falciparum gametocyte carriers, and P. falciparum in the sporozoite stage were detected in salivary glands by using a real-time quantitative PCR (qPCR) assay. The sensitivity and specificity of this qPCR were compared with the multiplex PCR applied from the Padley method. CSP-ELISA was also performed on carcasses of the same mosquitoes. Results: The prevalence of P. falciparum and the intensity of infection were evaluated using qPCR. This method had a limit of detection of six sporozoites per mu L based on standard curves. The number of P. falciparum genomes in the salivary gland samples reached 9,262 parasites/mu L (mean: 254.5; 95% CI: 163.5-345.6). The qPCR showed a similar sensitivity (100%) and a high specificity (60%) compared to the multiplex PCR. The agreement between the two methods was "substantial" (k = 0.63, P < 0.05). The number of P. falciparum-positive mosquitoes evaluated with the qPCR (76%), multiplex PCR (59%), and CSP-ELISA (83%) was significantly different (P < 0.005). Conclusions: The qPCR assay can be used to detect P. falciparum in salivary glands of An. gambiae. The qPCR is highly sensitive and is more specific than multiplex PCR, allowing an accurate measure of infective An. gambiae. The results also showed that the CSP-ELISA overestimates the sporozoite rate, detecting sporozoites in the haemolymph in addition to the salivary glands.

Published
2013
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9. Modulation of malaria infection in Anopheles gambiae mosquitoes exposed to natural midgut bacteria

Author

Geoffrey Gimonneau, Richard Christen, Isabelle Morlais, Sandrine E. Nsango, Antoine Berry, Anne Boissière, Majoline T. Tchioffo, Thomas S. Churcher, Parfait Awono-Ambene, Luc Abate, Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Laboratoire de Recherche sur le Paludisme, Organization de Coordination pour la lutte contre les Endémies en Afrique Centrale (OCEAC), Organization de Coordination pour la lutte contre les Endémies en Afrique Centrale, Imperial College London, Symbiose Marine (SM), Evolution Paris Seine, Université des Antilles et de la Guyane (UAG)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles et de la Guyane (UAG)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS), Centre de Physiopathologie de Toulouse Purpan, Institut National de la Recherche Agronomique (INRA), Institut de Recherche pour le Developpement (IRD), Agence Nationale de la Recherche [ANR-11-BSV7-009-01], APEGE programme from the Institut Ecologie et Environnement, European Union [242095- EVIMalaR, 223601- MALVECBLOK], Infectiopole Sud foundation, IRD, Organisation de Coordination pour la lutte contre les Endémies en Afrique Centrale (OCEAC), Université des Antilles et de la Guyane (UAG)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Nice Sophia Antipolis (1965 - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles et de la Guyane (UAG)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Nice Sophia Antipolis (1965 - 2019) (UNS), and Medical Research Council (MRC)

Subjects
Anopheles gambiae, DIVERSITY, Colony Count, Microbial, INDEPENDENT METHODS, L73 - Maladies des animaux, Plasmodium, Interactions biologiques, Hôte, 0302 clinical medicine, RNA, Ribosomal, 16S, Cameroon, Malaria, Falciparum, VERTICAL TRANSMISSION, 0303 health sciences, Multidisciplinary, PLASMODIUM-FALCIPARUM, [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], Anopheles, Facteur du milieu, MICROBIOTA, 3. Good health, Épidémiologie, Multidisciplinary Sciences, Flore intestinale, Science & Technology - Other Topics, Medicine, SPOROGONIC DEVELOPMENT, Infection, L72 - Organismes nuisibles des animaux, Research Article, Genre humain, Symbiotic bacteria, General Science & Technology, Relation hôte parasite, Science, Molecular Sequence Data, Plasmodium falciparum, 030231 tropical medicine, Biology, Microbiology, 03 medical and health sciences, CULICIDAE, SYMBIONTS, parasitic diseases, Escherichia coli, Animals, Humans, Microbiome, PARASITE, 030304 developmental biology, Science & Technology, Bacteria, Base Sequence, Flore microbienne, Oocysts, Genetic Variation, Midgut, biology.organism_classification, Malaria, DIPTERA, Digestive System
Abstract

International audience; The development of Plasmodium falciparum within the Anopheles gambiae mosquito relies on complex vector-parasite interactions, however the resident midgut microbiota also plays an important role in mediating parasite infection. In natural conditions, the mosquito microbial flora is diverse, composed of commensal and symbiotic bacteria. We report here the isolation of culturable midgut bacteria from mosquitoes collected in the field in Cameroon and their identification based on the 16S rRNA gene sequencing. We next measured the effect of selected natural bacterial isolates on Plasmodium falciparum infection prevalence and intensity over multiple infectious feedings and found that the bacteria significantly reduced the prevalence and intensity of infection. These results contrast with our previous study where the abundance of Enterobacteriaceae positively correlated with P. falciparum infection (Boissiere et al. 2012). The oral infection of bacteria probably led to the disruption of the gut homeostasis and activated immune responses, and this pinpoints the importance of studying microbe-parasite interactions in natural conditions. Our results indicate that the effect of bacterial exposure on P. falciparum infection varies with factors from the parasite and the human host and calls for deeper dissection of these parameters for accurate interpretation of bacterial exposure results in laboratory settings.

Published
2013
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10. Application of a qPCR assay in the investigation of susceptibility to malaria infection of the M and S Molecular Forms of An. gambiae s.s. in Cameroon

Author

Geoffrey Gimonneau, Parfait Awono-Ambene, Luc Abate, Sandrine E. Nsango, Majoline T. Tchioffo, Anne Boissière, Isabelle Morlais, Albert N. Bayibéki, Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Laboratoire de Recherche sur le Paludisme, Organization de Coordination pour la lutte contre les Endémies en Afrique Centrale (OCEAC), Organization de Coordination pour la lutte contre les Endémies en Afrique Centrale, Organisation de Coordination pour la lutte contre les Endémies en Afrique Centrale (OCEAC), Savoirs, Textes, Langage (STL) - UMR 8163 (STL), Université de Lille-Centre National de la Recherche Scientifique (CNRS), Institut de Recherche pour le Développement (IRD), Transmission-Interactions-Adaptations hôtes/vecteurs/pathogènes (MIVEGEC-TRIAD), Evolution des Systèmes Vectoriels (ESV), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Laboratoire d’Entomologie Médicale, Organisation de Coordination pour la lutte contre les Endémies en Afrique Centrale, and Université de Douala

Subjects
Epidemiology, Anopheles gambiae, [SDV]Life Sciences [q-bio], lcsh:Medicine, law.invention, 0302 clinical medicine, law, Genotype, lcsh:Science, Polymerase chain reaction, ComputingMilieux_MISCELLANEOUS, 0303 health sciences, Multidisciplinary, Ecology, biology, Anopheles, 3. Good health, Épidémiologie, Infectious Diseases, PCR, Sympatric speciation, S50 - Santé humaine, Medicine, Infection, L72 - Organismes nuisibles des animaux, Research Article, 030231 tropical medicine, Plasmodium falciparum, Allopatric speciation, Infectious Disease Epidemiology, 03 medical and health sciences, Analyse quantitative, parasitic diseases, Genetics, Parasitic Diseases, medicine, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, Biology, Transmission des maladies, 030304 developmental biology, Population Biology, lcsh:R, Tropical Diseases (Non-Neglected), Morbidité, biology.organism_classification, medicine.disease, Virology, Malaria, lcsh:Q, U30 - Méthodes de recherche
Abstract

Plasmodium falciparum is the causative agent of malaria, a disease that kills almost one million persons each year, mainly in sub-Saharan Africa. P. falciparum is transmitted to the human host by the bite of an Anopheles female mosquito, and Anopheles gambiae sensus stricto is the most tremendous malaria vector in Africa, widespread throughout the afro-tropical belt. An. gambiae s.s. is subdivided into two distinct molecular forms, namely M and S forms. The two molecular forms are morphologically identical but they are distinct genetically, and differ by their distribution and their ecological preferences. The epidemiological importance of the two molecular forms in malaria transmission has been poorly investigated so far and gave distinct results in different areas. We have developed a real-time quantitative PCR (qPCR) assay, and used it to detect P. falciparum at the oocyst stage in wild An. gambiae s.s. mosquitoes experimentally infected with natural isolates of parasites. Mosquitoes were collected at immature stages in sympatric and allopatric breeding sites and further infected at the adult stage. We next measured the infection prevalence and intensity in female mosquitoes using the qPCR assay and correlated the infection success with the mosquito molecular forms. Our results revealed different prevalence of infection between the M and S molecular forms of An. gambiae s.s. in Cameroon, for both sympatric and allopatric populations of mosquitoes. However, no difference in the infection intensity was observed. Thus, the distribution of the molecular forms of An. gambiae s.s. may impact on the malaria epidemiology, and it will be important to monitor the efficiency of malaria control interventions on the two M and S forms.

Published
2013
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11. Midgut microbiota of the malaria mosquito vector Anopheles gambiae and interactions with Plasmodium falciparum infection

Author

Anne Boissière, Majoline T. Tchioffo, Alexandra Marie, Parfait Awono-Ambene, Richard Christen, Luc Abate, Isabelle Morlais, Sandrine E. Nsango, Hamid Reza Shahbazkia, Dipankar Bachar, Elena A. Levashina, Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Organisation de Coordination pour la lutte contre les Endémies en Afrique Centrale (OCEAC), Modèles Insectes de l'Immunité Innée (M3I), Institut de biologie moléculaire et cellulaire (IBMC), Université de Strasbourg (UNISTRA)-Centre National de la Recherche Scientifique (CNRS)-Université de Strasbourg (UNISTRA)-Centre National de la Recherche Scientifique (CNRS)-Université de Strasbourg (UNISTRA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Symbiose Marine (SM), Evolution Paris Seine, Université des Antilles et de la Guyane (UAG)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Nice Sophia Antipolis (1965 - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles et de la Guyane (UAG)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Nice Sophia Antipolis (1965 - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS), Institut de Recherche pour le Developpement (IRD), French Agence Nationale pour la Recherche [ANR-11-BSV7-009-01], European Community [242095, 223601], Laboratoire de Recherche sur le Paludisme, Organization de Coordination pour la lutte contre les Endémies en Afrique Centrale (OCEAC), Organization de Coordination pour la lutte contre les Endémies en Afrique Centrale, Centre National de la Recherche Scientifique (CNRS)-Université de Strasbourg (UNISTRA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut de biologie moléculaire et cellulaire (IBMC), Université de Strasbourg (UNISTRA)-Centre National de la Recherche Scientifique (CNRS)-Université de Strasbourg (UNISTRA)-Centre National de la Recherche Scientifique (CNRS), Université des Antilles et de la Guyane (UAG)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Nice Sophia Antipolis (... - 2019) (UNS), and COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles et de la Guyane (UAG)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Nice Sophia Antipolis (... - 2019) (UNS)

Subjects
Molecular-forms, Intestinal microbiota, Anopheles gambiae, Plasmodium, Malaria, Falciparum, lcsh:QH301-705.5, 0303 health sciences, Ecology, [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], Anopheles, Genomics, 3. Good health, Research Article, lcsh:Immunologic diseases. Allergy, Burkholderia, Immunology, Plasmodium falciparum, Enterobacter, Zoology, Paratransgenesis, Gut microbiota, Environment, Biology, Microbiology, Host-Parasite Interactions, 03 medical and health sciences, Virology, parasitic diseases, medicine, Genetics, Animals, Molecular Biology, 030304 developmental biology, Evolutionary Biology, Population Biology, 030306 microbiology, Diptera, Communities, fungi, Midgut, Sporogonic development, biology.organism_classification, medicine.disease, Insect Vectors, Culicidae, Bacterial diversity, Gene Expression Regulation, lcsh:Biology (General), Vector (epidemiology), Parasitology, lcsh:RC581-607, Digestive System, Malaria
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., Author Summary 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.

Published
2012
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12. The Anopheles Mosquito Microbiota and Their Impact on Pathogen Transmission

Author

Mathilde Gendrin, George K. Christophides, Department of Life Sciences, Imperial College London, London, United Kingdom, Imperial College London, and We thank Jiannong Xu, Jewelna Osei-Poku, Anne Boissière and Isabelle Morlais for providing example sequences of some of the bacterial genera shown in Table 1 and Thierry Lefèvre for helping with mosquito pictures presented in Figure 1.

Subjects
0303 health sciences, biology, [SDV]Life Sciences [q-bio], 030231 tropical medicine, Anopheles, Zoology, biology.organism_classification, law.invention, 03 medical and health sciences, 0302 clinical medicine, Transmission (mechanics), law, Pathogen, ComputingMilieux_MISCELLANEOUS, 030304 developmental biology
Abstract

International audience

Published
2013
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