A Gut Commensal Bacterium Promotes Mosquito Permissiveness to Arboviruses

被引:183
作者
Wu, Pa [1 ,2 ]
Sun, Peng [1 ,2 ]
Nie, Kaixiao [1 ,2 ]
Zhu, Yibin [1 ,2 ,3 ]
Shi, Mingyu [1 ]
Xiao, Changguang [1 ]
Liu, Han [1 ]
Liu, Qiyong [4 ]
Zhao, Tongyan [5 ]
Chen, Xiaoguang [6 ]
Zhou, Hongning [7 ]
Wang, Penghua [8 ]
Cheng, Gong [1 ,2 ]
机构
[1] Tsinghua Univ, Tsinghua Peking Ctr Life Sci, Sch Med, Beijing 100084, Peoples R China
[2] Shenzhen Ctr Dis Control & Prevent, Inst Pathogen Organisms, Shenzhen 518055, Guangdong, Peoples R China
[3] Tsinghua Univ, Sch Life Sci, Beijing 100084, Peoples R China
[4] China CDC, CCID, ICDC, State Key Lab Infect Dis Prevent & Control, Beijing 102206, Peoples R China
[5] Beijing Inst Microbiol & Epidemiol, State Key Lab Pathogen & Biosecur, Beijing 100071, Peoples R China
[6] Southern Med Univ, Sch Publ Hlth, Dept Pathogen Biol, Guangdong Prov Key Lab Trop Dis Res, Guangzhou 510515, Guangdong, Peoples R China
[7] Yunnan Inst Parasit Dis, Puer 650034, Yunnan, Peoples R China
[8] Univ Connecticut, Hlth Ctr, Dept Immunol, Sch Med, Farmington, CT 06030 USA
基金
中国国家自然科学基金; 美国国家卫生研究院;
关键词
AEDES-AEGYPTI DIPTERA; PERITROPHIC MATRIX; VECTOR COMPETENCE; MICROBIOTA; MIDGUT; DENGUE; MUCIN; PROTEIN; MICROORGANISMS; ARCHITECTURE;
D O I
10.1016/j.chom.2018.11.004
中图分类号
Q93 [微生物学];
学科分类号
071005 ; 100705 ;
摘要
Mosquitoes are hematophagous vectors that can acquire human viruses in their intestinal tract. Here, we define a mosquito gut commensal bacterium that promotes permissiveness to arboviruses. Antibiotic depletion of gut bacteria impaired arboviral infection of a lab-adapted Aedes aegypti mosquito strain. Reconstitution of individual cultivable gut bacteria in antibiotic-treated mosquitoes identified Serratia marcescens as a commensal bacterium critical for efficient arboviral acquisition. S. marcescens facilitates arboviral infection through a secreted protein named SmEnhancin, which digests membrane-bound mucins on the mosquito gut epithelia, thereby enhancing viral dissemination. Field Aedes mosquitoes positive for S. marcescens were more permissive to dengue virus infection than those free of S. marcescens. Oral introduction of S. marcescens into field mosquitoes that lack this bacterium rendered these mosquitoes highly susceptible to arboviruses. This study defines a commensal-driven mechanism that contributes to vector competence, and extends our understanding of multipartite interactions among hosts, the gut microbiome, and viruses.
引用
收藏
页码:101 / +
页数:17
相关论文
共 53 条
[1]   Commensal bacteria mediated defenses against pathogens [J].
Abt, Michael C. ;
Pamer, Eric G. .
CURRENT OPINION IN IMMUNOLOGY, 2014, 29 :16-22
[2]   An Aedes aegypti-associated fungus increases susceptibility to dengue virus by modulating gut trypsin activity [J].
Anglero-Rodriguez, Yesseinia I. ;
Talyuli, Octavio A. C. ;
Blumberg, Benjamin J. ;
Kang, Seokyoung ;
Demby, Celia ;
Shields, Alicia ;
Carlson, Jenny ;
Jupatanakul, Natapong ;
Dimopoulos, George .
ELIFE, 2017, 6
[3]   Serratia odorifera a Midgut Inhabitant of Aedes aegypti Mosquito Enhances Its Susceptibility to Dengue-2 Virus [J].
Apte-Deshpande, Anjali ;
Paingankar, Mandar ;
Gokhale, Mangesh D. ;
Deobagkar, Dileep N. .
PLOS ONE, 2012, 7 (07)
[4]   Host-bacterial mutualism in the human intestine [J].
Bäckhed, F ;
Ley, RE ;
Sonnenburg, JL ;
Peterson, DA ;
Gordon, JI .
SCIENCE, 2005, 307 (5717) :1915-1920
[5]   Intra-specific diversity of Serratia marcescens in Anopheles mosquito midgut defines Plasmodium transmission capacity [J].
Bando, Hironori ;
Okado, Kiyoshi ;
Guelbeogo, Wamdaogo M. ;
Badolo, Athanase ;
Aonuma, Hiroka ;
Nelson, Bryce ;
Fukumoto, Shinya ;
Xuan, Xuenan ;
Sagnon, N'Fale ;
Kanuka, Hirotaka .
SCIENTIFIC REPORTS, 2013, 3
[6]   Role of the Microbiota in Immunity and Inflammation [J].
Belkaid, Yasmine ;
Hand, Timothy W. .
CELL, 2014, 157 (01) :121-141
[7]   Variation in vector competence for dengue 2 virus among 24 collections of Aedes aegypti from Mexico and the United States [J].
Bennett, KE ;
Olson, KE ;
Muñoz, MD ;
Fernandez-Salas, I ;
Farfan-Ale, JA ;
Higgs, S ;
Black, WC ;
Beaty, BJ .
AMERICAN JOURNAL OF TROPICAL MEDICINE AND HYGIENE, 2002, 67 (01) :85-92
[8]   Mosquito Defense Strategies against Viral Infection [J].
Cheng, Gong ;
Liu, Yang ;
Wang, Penghua ;
Xiao, Xiaoping .
TRENDS IN PARASITOLOGY, 2016, 32 (03) :177-186
[9]   Epidemiological Characteristics and Space-Time Analysis of the 2015 Dengue Outbreak in the Metropolitan Region of Tainan City, Taiwan [J].
Chuang, Ting-Wu ;
Ng, Ka-Chon ;
Thi Luong Nguyen ;
Fernando Chaves, Luis .
INTERNATIONAL JOURNAL OF ENVIRONMENTAL RESEARCH AND PUBLIC HEALTH, 2018, 15 (03)
[10]   Effects of environment, dietary regime and ageing on the dengue vector microbiota: evidence of a core microbiota throughout Aedes aegypti lifespan [J].
David, Mariana Rocha ;
Barbosa dos Santos, Lilha Maria ;
Paulo Vicente, Ana Carolina ;
Maciel-de-Freitas, Rafael .
MEMORIAS DO INSTITUTO OSWALDO CRUZ, 2016, 111 (09) :577-587