Genetic dissection of Anopheles gambiae gut epithelial responses to Serratia marcescens.

Genetic variation in the mosquito Anopheles gambiae profoundly influences its ability to transmit malaria. Mosquito gut bacteria are shown to influence the outcome of infections with Plasmodium parasites and are also thought to exert a strong drive on genetic variation through natural selection; how...

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Autores principales:	Stavros Stathopoulos, Daniel E Neafsey, Mara K N Lawniczak, Marc A T Muskavitch, George K Christophides
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2014
Materias:	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/53099800294c4745a3ba38412b9f6398
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spelling	oai:doaj.org-article:53099800294c4745a3ba38412b9f63982021-11-18T06:06:54ZGenetic dissection of Anopheles gambiae gut epithelial responses to Serratia marcescens.1553-73661553-737410.1371/journal.ppat.1003897https://doaj.org/article/53099800294c4745a3ba38412b9f63982014-03-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24603764/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374Genetic variation in the mosquito Anopheles gambiae profoundly influences its ability to transmit malaria. Mosquito gut bacteria are shown to influence the outcome of infections with Plasmodium parasites and are also thought to exert a strong drive on genetic variation through natural selection; however, a link between antibacterial effects and genetic variation is yet to emerge. Here, we combined SNP genotyping and expression profiling with phenotypic analyses of candidate genes by RNAi-mediated silencing and 454 pyrosequencing to investigate this intricate biological system. We identified 138 An. gambiae genes to be genetically associated with the outcome of Serratia marcescens infection, including the peptidoglycan recognition receptor PGRPLC that triggers activation of the antibacterial IMD/REL2 pathway and the epidermal growth factor receptor EGFR. Silencing of three genes encoding type III fibronectin domain proteins (FN3Ds) increased the Serratia load and altered the gut microbiota composition in favor of Enterobacteriaceae. These data suggest that natural genetic variation in immune-related genes can shape the bacterial population structure of the mosquito gut with high specificity. Importantly, FN3D2 encodes a homolog of the hypervariable pattern recognition receptor Dscam, suggesting that pathogen-specific recognition may involve a broader family of immune factors. Additionally, we showed that silencing the gene encoding the gustatory receptor Gr9 that is also associated with the Serratia infection phenotype drastically increased Serratia levels. The Gr9 antibacterial activity appears to be related to mosquito feeding behavior and to mostly rely on changes of neuropeptide F expression, together suggesting a behavioral immune response following Serratia infection. Our findings reveal that the mosquito response to oral Serratia infection comprises both an epithelial and a behavioral immune component.Stavros StathopoulosDaniel E NeafseyMara K N LawniczakMarc A T MuskavitchGeorge K ChristophidesPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 10, Iss 3, p e1003897 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
spellingShingle	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 Stavros Stathopoulos Daniel E Neafsey Mara K N Lawniczak Marc A T Muskavitch George K Christophides Genetic dissection of Anopheles gambiae gut epithelial responses to Serratia marcescens.
description	Genetic variation in the mosquito Anopheles gambiae profoundly influences its ability to transmit malaria. Mosquito gut bacteria are shown to influence the outcome of infections with Plasmodium parasites and are also thought to exert a strong drive on genetic variation through natural selection; however, a link between antibacterial effects and genetic variation is yet to emerge. Here, we combined SNP genotyping and expression profiling with phenotypic analyses of candidate genes by RNAi-mediated silencing and 454 pyrosequencing to investigate this intricate biological system. We identified 138 An. gambiae genes to be genetically associated with the outcome of Serratia marcescens infection, including the peptidoglycan recognition receptor PGRPLC that triggers activation of the antibacterial IMD/REL2 pathway and the epidermal growth factor receptor EGFR. Silencing of three genes encoding type III fibronectin domain proteins (FN3Ds) increased the Serratia load and altered the gut microbiota composition in favor of Enterobacteriaceae. These data suggest that natural genetic variation in immune-related genes can shape the bacterial population structure of the mosquito gut with high specificity. Importantly, FN3D2 encodes a homolog of the hypervariable pattern recognition receptor Dscam, suggesting that pathogen-specific recognition may involve a broader family of immune factors. Additionally, we showed that silencing the gene encoding the gustatory receptor Gr9 that is also associated with the Serratia infection phenotype drastically increased Serratia levels. The Gr9 antibacterial activity appears to be related to mosquito feeding behavior and to mostly rely on changes of neuropeptide F expression, together suggesting a behavioral immune response following Serratia infection. Our findings reveal that the mosquito response to oral Serratia infection comprises both an epithelial and a behavioral immune component.
format	article
author	Stavros Stathopoulos Daniel E Neafsey Mara K N Lawniczak Marc A T Muskavitch George K Christophides
author_facet	Stavros Stathopoulos Daniel E Neafsey Mara K N Lawniczak Marc A T Muskavitch George K Christophides
author_sort	Stavros Stathopoulos
title	Genetic dissection of Anopheles gambiae gut epithelial responses to Serratia marcescens.
title_short	Genetic dissection of Anopheles gambiae gut epithelial responses to Serratia marcescens.
title_full	Genetic dissection of Anopheles gambiae gut epithelial responses to Serratia marcescens.
title_fullStr	Genetic dissection of Anopheles gambiae gut epithelial responses to Serratia marcescens.
title_full_unstemmed	Genetic dissection of Anopheles gambiae gut epithelial responses to Serratia marcescens.
title_sort	genetic dissection of anopheles gambiae gut epithelial responses to serratia marcescens.
publisher	Public Library of Science (PLoS)
publishDate	2014
url	https://doaj.org/article/53099800294c4745a3ba38412b9f6398
work_keys_str_mv	AT stavrosstathopoulos geneticdissectionofanophelesgambiaegutepithelialresponsestoserratiamarcescens AT danieleneafsey geneticdissectionofanophelesgambiaegutepithelialresponsestoserratiamarcescens AT maraknlawniczak geneticdissectionofanophelesgambiaegutepithelialresponsestoserratiamarcescens AT marcatmuskavitch geneticdissectionofanophelesgambiaegutepithelialresponsestoserratiamarcescens AT georgekchristophides geneticdissectionofanophelesgambiaegutepithelialresponsestoserratiamarcescens
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Genetic dissection of Anopheles gambiae gut epithelial responses to Serratia marcescens.

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