Glucose-mediated proliferation of a gut commensal bacterium promotes Plasmodium infection by increasing mosquito midgut pH
Plant-nectar-derived sugar is the major energy source for mosquitoes, but its influence on vector competence for malaria parasites remains unclear. Here, we show that Plasmodium berghei infection of Anopheles stephensi results in global metabolome changes, with the most significant impact on glucose...
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| Veröffentlicht in: | Cell reports (Cambridge) Jg. 35; H. 3; S. 108992 |
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20.04.2021
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| Abstract | Plant-nectar-derived sugar is the major energy source for mosquitoes, but its influence on vector competence for malaria parasites remains unclear. Here, we show that Plasmodium berghei infection of Anopheles stephensi results in global metabolome changes, with the most significant impact on glucose metabolism. Feeding on glucose or trehalose (the main hemolymph sugars) renders the mosquito more susceptible to Plasmodium infection by alkalizing the mosquito midgut. The glucose/trehalose diets promote proliferation of a commensal bacterium, Asaia bogorensis, that remodels glucose metabolism in a way that increases midgut pH, thereby promoting Plasmodium gametogenesis. We also demonstrate that the sugar composition from different natural plant nectars influences A. bogorensis growth, resulting in a greater permissiveness to Plasmodium. Altogether, our results demonstrate that dietary glucose is an important determinant of mosquito vector competency for Plasmodium, further highlighting a key role for mosquito-microbiota interactions in regulating the development of the malaria parasite.
[Display omitted]
•Glucose/trehalose supplementation promotes Plasmodium infection in mosquitoes•Glucose/trehalose supplementation promotes the expansion of a gut commensal Asaia•Asaia remodels glucose metabolism and increases midgut pH•The pH increase induces Plasmodium gametogenesis and facilitates parasite infection
Wang et al. show that glucose/trehalose supplementation promotes the expansion of a commensal bacterium Asaia that modulates glucose metabolism, resulting in an increase of mosquito midgut pH. The pH increase promotes Plasmodium berghei sexual development. |
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| AbstractList | Plant-nectar-derived sugar is the major energy source for mosquitoes, but its influence on vector competence for malaria parasites remains unclear. Here, we show that Plasmodium berghei infection of Anopheles stephensi results in global metabolome changes, with the most significant impact on glucose metabolism. Feeding on glucose or trehalose (the main hemolymph sugars) renders the mosquito more susceptible to Plasmodium infection by alkalizing the mosquito midgut. The glucose/trehalose diets promote proliferation of a commensal bacterium, Asaia bogorensis, that remodels glucose metabolism in a way that increases midgut pH, thereby promoting Plasmodium gametogenesis. We also demonstrate that the sugar composition from different natural plant nectars influences A. bogorensis growth, resulting in a greater permissiveness to Plasmodium. Altogether, our results demonstrate that dietary glucose is an important determinant of mosquito vector competency for Plasmodium, further highlighting a key role for mosquito-microbiota interactions in regulating the development of the malaria parasite. Plant-nectar-derived sugar is the major energy source for mosquitoes, but its influence on vector competence for malaria parasites remains unclear. Here, we show that Plasmodium berghei infection of Anopheles stephensi results in global metabolome changes, with the most significant impact on glucose metabolism. Feeding on glucose or trehalose (the main hemolymph sugars) renders the mosquito more susceptible to Plasmodium infection by alkalizing the mosquito midgut. The glucose/trehalose diets promote proliferation of a commensal bacterium, Asaia bogorensis, that remodels glucose metabolism in a way that increases midgut pH, thereby promoting Plasmodium gametogenesis. We also demonstrate that the sugar composition from different natural plant nectars influences A. bogorensis growth, resulting in a greater permissiveness to Plasmodium. Altogether, our results demonstrate that dietary glucose is an important determinant of mosquito vector competency for Plasmodium, further highlighting a key role for mosquito-microbiota interactions in regulating the development of the malaria parasite. Wang et al. show that glucose/trehalose supplementation promotes the expansion of a commensal bacterium Asaia that modulates glucose metabolism, resulting in an increase of mosquito midgut pH. The pH increase promotes Plasmodium berghei sexual development. Plant-nectar-derived sugar is the major energy source for mosquitoes, but its influence on vector competence for malaria parasites remains unclear. Here, we show that Plasmodium berghei infection of Anopheles stephensi results in global metabolome changes, with the most significant impact on glucose metabolism. Feeding on glucose or trehalose (the main hemolymph sugars) renders the mosquito more susceptible to Plasmodium infection by alkalizing the mosquito midgut. The glucose/trehalose diets promote proliferation of a commensal bacterium, Asaia bogorensis, that remodels glucose metabolism in a way that increases midgut pH, thereby promoting Plasmodium gametogenesis. We also demonstrate that the sugar composition from different natural plant nectars influences A. bogorensis growth, resulting in a greater permissiveness to Plasmodium. Altogether, our results demonstrate that dietary glucose is an important determinant of mosquito vector competency for Plasmodium, further highlighting a key role for mosquito-microbiota interactions in regulating the development of the malaria parasite.Plant-nectar-derived sugar is the major energy source for mosquitoes, but its influence on vector competence for malaria parasites remains unclear. Here, we show that Plasmodium berghei infection of Anopheles stephensi results in global metabolome changes, with the most significant impact on glucose metabolism. Feeding on glucose or trehalose (the main hemolymph sugars) renders the mosquito more susceptible to Plasmodium infection by alkalizing the mosquito midgut. The glucose/trehalose diets promote proliferation of a commensal bacterium, Asaia bogorensis, that remodels glucose metabolism in a way that increases midgut pH, thereby promoting Plasmodium gametogenesis. We also demonstrate that the sugar composition from different natural plant nectars influences A. bogorensis growth, resulting in a greater permissiveness to Plasmodium. Altogether, our results demonstrate that dietary glucose is an important determinant of mosquito vector competency for Plasmodium, further highlighting a key role for mosquito-microbiota interactions in regulating the development of the malaria parasite. Plant-nectar-derived sugar is the major energy source for mosquitoes, but its influence on vector competence for malaria parasites remains unclear. Here, we show that Plasmodium berghei infection of Anopheles stephensi results in global metabolome changes, with the most significant impact on glucose metabolism. Feeding on glucose or trehalose (the main hemolymph sugars) renders the mosquito more susceptible to Plasmodium infection by alkalizing the mosquito midgut. The glucose/trehalose diets promote proliferation of a commensal bacterium, Asaia bogorensis, that remodels glucose metabolism in a way that increases midgut pH, thereby promoting Plasmodium gametogenesis. We also demonstrate that the sugar composition from different natural plant nectars influences A. bogorensis growth, resulting in a greater permissiveness to Plasmodium. Altogether, our results demonstrate that dietary glucose is an important determinant of mosquito vector competency for Plasmodium, further highlighting a key role for mosquito-microbiota interactions in regulating the development of the malaria parasite. [Display omitted] •Glucose/trehalose supplementation promotes Plasmodium infection in mosquitoes•Glucose/trehalose supplementation promotes the expansion of a gut commensal Asaia•Asaia remodels glucose metabolism and increases midgut pH•The pH increase induces Plasmodium gametogenesis and facilitates parasite infection Wang et al. show that glucose/trehalose supplementation promotes the expansion of a commensal bacterium Asaia that modulates glucose metabolism, resulting in an increase of mosquito midgut pH. The pH increase promotes Plasmodium berghei sexual development. |
| ArticleNumber | 108992 |
| Author | Feng, Yuebiao Wang, Penghua Gao, Li An, Yanpeng Wang, Jingwen Wang, Mengfei Dong, Shengzhang Zhou, Xiaofeng Tang, Huiru Dimopoulos, George |
| AuthorAffiliation | 5 Human Phenome Institute, Fudan University, Shanghai 200433, PRC 2 Ministry of Education Key Laboratory of Contemporary Anthropology, School of Life Sciences, Fudan University, Shanghai 200438, PRC 4 W. Harry Feinstone Department of Molecular Microbiology and Immunology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD 21205, USA 3 State Key Laboratory of Genetic Engineering, Zhongshan Hospital and School of Life Sciences, Human Phenome Institute, Metabonomics and Systems Biology Laboratory at Shanghai International Centre for Molecular Phenomics, Fudan University, Shanghai 200438, PRC 1 State Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai 200438, PRC 6 Department of Immunology, School of Medicine, The University of Connecticut Health Center, Farmington, CT 06030, USA 8 Lead contact |
| AuthorAffiliation_xml | – name: 4 W. Harry Feinstone Department of Molecular Microbiology and Immunology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD 21205, USA – name: 5 Human Phenome Institute, Fudan University, Shanghai 200433, PRC – name: 1 State Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai 200438, PRC – name: 3 State Key Laboratory of Genetic Engineering, Zhongshan Hospital and School of Life Sciences, Human Phenome Institute, Metabonomics and Systems Biology Laboratory at Shanghai International Centre for Molecular Phenomics, Fudan University, Shanghai 200438, PRC – name: 2 Ministry of Education Key Laboratory of Contemporary Anthropology, School of Life Sciences, Fudan University, Shanghai 200438, PRC – name: 6 Department of Immunology, School of Medicine, The University of Connecticut Health Center, Farmington, CT 06030, USA – name: 8 Lead contact |
| Author_xml | – sequence: 1 givenname: Mengfei surname: Wang fullname: Wang, Mengfei organization: State Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai 200438, PRC – sequence: 2 givenname: Yanpeng surname: An fullname: An, Yanpeng organization: State Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai 200438, PRC – sequence: 3 givenname: Li surname: Gao fullname: Gao, Li organization: State Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai 200438, PRC – sequence: 4 givenname: Shengzhang surname: Dong fullname: Dong, Shengzhang organization: W. Harry Feinstone Department of Molecular Microbiology and Immunology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD 21205, USA – sequence: 5 givenname: Xiaofeng surname: Zhou fullname: Zhou, Xiaofeng organization: Human Phenome Institute, Fudan University, Shanghai 200433, PRC – sequence: 6 givenname: Yuebiao surname: Feng fullname: Feng, Yuebiao organization: State Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai 200438, PRC – sequence: 7 givenname: Penghua surname: Wang fullname: Wang, Penghua organization: Department of Immunology, School of Medicine, The University of Connecticut Health Center, Farmington, CT 06030, USA – sequence: 8 givenname: George surname: Dimopoulos fullname: Dimopoulos, George organization: W. Harry Feinstone Department of Molecular Microbiology and Immunology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD 21205, USA – sequence: 9 givenname: Huiru orcidid: 0000-0002-7139-2756 surname: Tang fullname: Tang, Huiru email: huiru_tang@fudan.edu.cn organization: State Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai 200438, PRC – sequence: 10 givenname: Jingwen orcidid: 0000-0002-6794-2604 surname: Wang fullname: Wang, Jingwen email: jingwenwang@fudan.edu.cn organization: State Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai 200438, PRC |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33882310$$D View this record in MEDLINE/PubMed |
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| Keywords | Plasmodium glucose Anopheles stephensi gametogenesis Asaia bogorensis trehalose midgut pH |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS Conceptualization, M.W. and J.W.; methodology, M.W., Y.A., L.G., Y.F., S.D., G.D., X.Z., H.T., and J.W.; investigation, M.W., Y.A., L.G., G.D., H.T., and J.W.; formal analysis, M.W., Y.A., L.G., X.Z., and S.D.; writing – original draft, M.W., Y.A., L.G., H.T., and J.W.; writing – review & editing, M.W., Y.A., L.G., P.W., G.D., H.T., and J.W.; visualization, M.W., Y.A., L.G., H. T., and J.W.; funding acquisition, J.W.; resources, J.W., supervision, G.D., H.T., and J.W. |
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| SubjectTerms | Acetobacteraceae - growth & development Acetobacteraceae - metabolism Animals Anopheles - drug effects Anopheles - metabolism Anopheles - microbiology Anopheles - parasitology Anopheles stephensi Asaia bogorensis Digestive System - microbiology Digestive System - parasitology Female gametogenesis Gametogenesis - drug effects Gametogenesis - genetics Gene Expression Regulation glucose Glucose - metabolism Glucose - pharmacology Host-Pathogen Interactions - genetics Hydrogen-Ion Concentration Life Cycle Stages - drug effects Life Cycle Stages - genetics Malaria - parasitology Metabolome Microbiota - genetics midgut pH Mosquito Vectors - drug effects Mosquito Vectors - metabolism Mosquito Vectors - microbiology Mosquito Vectors - parasitology Plasmodium Plasmodium berghei - genetics Plasmodium berghei - growth & development Plasmodium berghei - metabolism Protozoan Proteins - genetics Protozoan Proteins - metabolism Symbiosis - genetics trehalose Trehalose - metabolism Trehalose - pharmacology |
| Title | Glucose-mediated proliferation of a gut commensal bacterium promotes Plasmodium infection by increasing mosquito midgut pH |
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