Glucose-mediated proliferation of a gut commensal bacterium promotes Plasmodium infection by increasing mosquito midgut pH
Summary: 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 o...
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doaj-8f355d844664426697f721e79c38a0ed2021-04-22T13:38:16ZengElsevierCell Reports2211-12472021-04-01353108992Glucose-mediated proliferation of a gut commensal bacterium promotes Plasmodium infection by increasing mosquito midgut pHMengfei Wang0Yanpeng An1Li Gao2Shengzhang Dong3Xiaofeng Zhou4Yuebiao Feng5Penghua Wang6George Dimopoulos7Huiru Tang8Jingwen Wang9State Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai 200438, PRC; Ministry of Education Key Laboratory of Contemporary Anthropology, School of Life Sciences, Fudan University, Shanghai 200438, PRCState Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai 200438, PRC; 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, PRCState Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai 200438, PRC; Ministry of Education Key Laboratory of Contemporary Anthropology, School of Life Sciences, Fudan University, Shanghai 200438, PRCW. Harry Feinstone Department of Molecular Microbiology and Immunology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD 21205, USAHuman Phenome Institute, Fudan University, Shanghai 200433, PRCState Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai 200438, PRC; Ministry of Education Key Laboratory of Contemporary Anthropology, School of Life Sciences, Fudan University, Shanghai 200438, PRCDepartment of Immunology, School of Medicine, The University of Connecticut Health Center, Farmington, CT 06030, USAW. Harry Feinstone Department of Molecular Microbiology and Immunology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD 21205, USAState Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai 200438, PRC; 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; Corresponding authorState Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai 200438, PRC; Ministry of Education Key Laboratory of Contemporary Anthropology, School of Life Sciences, Fudan University, Shanghai 200438, PRC; Corresponding authorSummary: 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.http://www.sciencedirect.com/science/article/pii/S2211124721003065glucosetrehaloseAnopheles stephensiPlasmodiumAsaia bogorensismidgut pH |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Mengfei Wang Yanpeng An Li Gao Shengzhang Dong Xiaofeng Zhou Yuebiao Feng Penghua Wang George Dimopoulos Huiru Tang Jingwen Wang |
spellingShingle |
Mengfei Wang Yanpeng An Li Gao Shengzhang Dong Xiaofeng Zhou Yuebiao Feng Penghua Wang George Dimopoulos Huiru Tang Jingwen Wang Glucose-mediated proliferation of a gut commensal bacterium promotes Plasmodium infection by increasing mosquito midgut pH Cell Reports glucose trehalose Anopheles stephensi Plasmodium Asaia bogorensis midgut pH |
author_facet |
Mengfei Wang Yanpeng An Li Gao Shengzhang Dong Xiaofeng Zhou Yuebiao Feng Penghua Wang George Dimopoulos Huiru Tang Jingwen Wang |
author_sort |
Mengfei Wang |
title |
Glucose-mediated proliferation of a gut commensal bacterium promotes Plasmodium infection by increasing mosquito midgut pH |
title_short |
Glucose-mediated proliferation of a gut commensal bacterium promotes Plasmodium infection by increasing mosquito midgut pH |
title_full |
Glucose-mediated proliferation of a gut commensal bacterium promotes Plasmodium infection by increasing mosquito midgut pH |
title_fullStr |
Glucose-mediated proliferation of a gut commensal bacterium promotes Plasmodium infection by increasing mosquito midgut pH |
title_full_unstemmed |
Glucose-mediated proliferation of a gut commensal bacterium promotes Plasmodium infection by increasing mosquito midgut pH |
title_sort |
glucose-mediated proliferation of a gut commensal bacterium promotes plasmodium infection by increasing mosquito midgut ph |
publisher |
Elsevier |
series |
Cell Reports |
issn |
2211-1247 |
publishDate |
2021-04-01 |
description |
Summary: 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. |
topic |
glucose trehalose Anopheles stephensi Plasmodium Asaia bogorensis midgut pH |
url |
http://www.sciencedirect.com/science/article/pii/S2211124721003065 |
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