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

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          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.

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          Most cited references 85

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          A human gut microbial gene catalogue established by metagenomic sequencing.

          To understand the impact of gut microbes on human health and well-being it is crucial to assess their genetic potential. Here we describe the Illumina-based metagenomic sequencing, assembly and characterization of 3.3 million non-redundant microbial genes, derived from 576.7 gigabases of sequence, from faecal samples of 124 European individuals. The gene set, approximately 150 times larger than the human gene complement, contains an overwhelming majority of the prevalent (more frequent) microbial genes of the cohort and probably includes a large proportion of the prevalent human intestinal microbial genes. The genes are largely shared among individuals of the cohort. Over 99% of the genes are bacterial, indicating that the entire cohort harbours between 1,000 and 1,150 prevalent bacterial species and each individual at least 160 such species, which are also largely shared. We define and describe the minimal gut metagenome and the minimal gut bacterial genome in terms of functions present in all individuals and most bacteria, respectively.
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            A core gut microbiome in obese and lean twins

            The human distal gut harbors a vast ensemble of microbes (the microbiota) that provide us with important metabolic capabilities, including the ability to extract energy from otherwise indigestible dietary polysaccharides1–6. Studies of a small number of unrelated, healthy adults have revealed substantial diversity in their gut communities, as measured by sequencing 16S rRNA genes6–8, yet how this diversity relates to function and to the rest of the genes in the collective genomes of the microbiota (the gut microbiome) remains obscure. Studies of lean and obese mice suggest that the gut microbiota affects energy balance by influencing the efficiency of calorie harvest from the diet, and how this harvested energy is utilized and stored3–5. To address the question of how host genotype, environmental exposures, and host adiposity influence the gut microbiome, we have characterized the fecal microbial communities of adult female monozygotic and dizygotic twin pairs concordant for leanness or obesity, and their mothers. Analysis of 154 individuals yielded 9,920 near full-length and 1,937,461 partial bacterial 16S rRNA sequences, plus 2.14 gigabases from their microbiomes. The results reveal that the human gut microbiome is shared among family members, but that each person’s gut microbial community varies in the specific bacterial lineages present, with a comparable degree of co-variation between adult monozygotic and dizygotic twin pairs. However, there was a wide array of shared microbial genes among sampled individuals, comprising an extensive, identifiable ‘core microbiome’ at the gene, rather than at the organismal lineage level. Obesity is associated with phylum-level changes in the microbiota, reduced bacterial diversity, and altered representation of bacterial genes and metabolic pathways. These results demonstrate that a diversity of organismal assemblages can nonetheless yield a core microbiome at a functional level, and that deviations from this core are associated with different physiologic states (obese versus lean).
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              Sequencing technologies - the next generation.

              Demand has never been greater for revolutionary technologies that deliver fast, inexpensive and accurate genome information. This challenge has catalysed the development of next-generation sequencing (NGS) technologies. The inexpensive production of large volumes of sequence data is the primary advantage over conventional methods. Here, I present a technical review of template preparation, sequencing and imaging, genome alignment and assembly approaches, and recent advances in current and near-term commercially available NGS instruments. I also outline the broad range of applications for NGS technologies, in addition to providing guidelines for platform selection to address biological questions of interest.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Pathog
                PLoS Pathog
                plos
                plospath
                PLoS Pathogens
                Public Library of Science (San Francisco, USA )
                1553-7366
                1553-7374
                May 2012
                May 2012
                31 May 2012
                : 8
                : 5
                Affiliations
                [1 ]UMR MIVEGEC (IRD 224- CNRS 5290- UM1- UM2), Montpellier, France
                [2 ]Laboratoire de Recherche sur le Paludisme, IRD-OCEAC, BP288, Yaoundé, Cameroun
                [3 ]UMR 7138 Systématique Adaptation Evolution, Université de Nice-Sophia Antipolis, Parc Valrose, France
                [4 ]CNRS UPR 9022, Inserm U963, Université de Strasbourg, Strasbourg, France
                [5 ]Área Departamental de Engenharia Electrónica e Computação, Faculdade de Ciências e Tecnologia, Universidade do Algarve, Faro, Portugal
                Institut Pasteur, France
                Author notes

                Conceived and designed the experiments: AB RC IM. Performed the experiments: AB MTT LA AM SEN PHAA RC IM. Analyzed the data: AB DB LA HRS RC IM. Contributed reagents/materials/analysis tools: EAL RC IM. Wrote the paper: AB RC IM.

                Article
                PPATHOGENS-D-11-02633
                10.1371/journal.ppat.1002742
                3364955
                22693451
                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.
                Page count
                Pages: 12
                Categories
                Research Article
                Biology
                Ecology
                Evolutionary Biology
                Genetics
                Genomics
                Immunology
                Microbiology
                Population Biology

                Infectious disease & Microbiology

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