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...

Full description

Bibliographic Details
Main Authors: Mengfei Wang, Yanpeng An, Li Gao, Shengzhang Dong, Xiaofeng Zhou, Yuebiao Feng, Penghua Wang, George Dimopoulos, Huiru Tang, Jingwen Wang
Format: Article
Language:English
Published: Elsevier 2021-04-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124721003065
id doaj-8f355d844664426697f721e79c38a0ed
record_format Article
spelling 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
work_keys_str_mv AT mengfeiwang glucosemediatedproliferationofagutcommensalbacteriumpromotesplasmodiuminfectionbyincreasingmosquitomidgutph
AT yanpengan glucosemediatedproliferationofagutcommensalbacteriumpromotesplasmodiuminfectionbyincreasingmosquitomidgutph
AT ligao glucosemediatedproliferationofagutcommensalbacteriumpromotesplasmodiuminfectionbyincreasingmosquitomidgutph
AT shengzhangdong glucosemediatedproliferationofagutcommensalbacteriumpromotesplasmodiuminfectionbyincreasingmosquitomidgutph
AT xiaofengzhou glucosemediatedproliferationofagutcommensalbacteriumpromotesplasmodiuminfectionbyincreasingmosquitomidgutph
AT yuebiaofeng glucosemediatedproliferationofagutcommensalbacteriumpromotesplasmodiuminfectionbyincreasingmosquitomidgutph
AT penghuawang glucosemediatedproliferationofagutcommensalbacteriumpromotesplasmodiuminfectionbyincreasingmosquitomidgutph
AT georgedimopoulos glucosemediatedproliferationofagutcommensalbacteriumpromotesplasmodiuminfectionbyincreasingmosquitomidgutph
AT huirutang glucosemediatedproliferationofagutcommensalbacteriumpromotesplasmodiuminfectionbyincreasingmosquitomidgutph
AT jingwenwang glucosemediatedproliferationofagutcommensalbacteriumpromotesplasmodiuminfectionbyincreasingmosquitomidgutph
_version_ 1721514253848936448