TY - JOUR
T1 - Amino acid metabolic signaling influences Aedes aegypti midgut microbiome variability
AU - Short, Sarah M.
AU - Mongodin, Emmanuel F.
AU - MacLeod, Hannah J.
AU - Talyuli, Octavio A.C.
AU - Dimopoulos, George
N1 - Funding Information:
This work was funded by the National Institutes of Health, National Institute for Allergy and Infectious Disease, grants R01AI101431 and R01 AI081877. SMS was supported by a Ruth L. Kirschstein National Research Service Award F32AI112208-01A1. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We would like to thank Carol Thompson in the Johns Hopkins Biostatistics Center for assistance with statistical analysis. We also thank the insectary personnel at the Johns Hopkins Malaria Research Institute for assistance with mosquito rearing and the Microarray Core Facilities at the Johns Hopkins School of Public Health and School of Medicine for help with array scanning.
Publisher Copyright:
© 2017 Short et al.
PY - 2017/7/28
Y1 - 2017/7/28
N2 - The mosquito midgut microbiota has been shown to influence vector competence for multiple human pathogens. The microbiota is highly variable in the field, and the sources of this variability are not well understood, which limits our ability to understand or predict its effects on pathogen transmission. In this work, we report significant variation in female adult midgut bacterial load between strains of A. aegypti which vary in their susceptibility to dengue virus. Composition of the midgut microbiome was similar overall between the strains, with 81–92% of reads coming from the same five bacterial families, though we did detect differences in the presence of some bacterial families including Flavobacteriaceae and Entobacteriaceae. We conducted transcriptomic analysis on the two mosquito strains that showed the greatest difference in bacterial load, and found that they differ in transcript abundance of many genes implicated in amino acid metabolism, in particular the branched chain amino acid degradation pathway. We then silenced this pathway by targeting multiple genes using RNA interference, which resulted in strain-specific bacterial proliferation, thereby eliminating the difference in midgut bacterial load between the strains. This suggests that the branched chain amino acid (BCAA) degradation pathway controls midgut bacterial load, though the mechanism underlying this remains unclear. Overall, our results indicate that amino acid metabolism can act to influence the midgut microbiota. Moreover, they suggest that genetic or physiological variation in BCAA degradation pathway activity may in part explain midgut microbiota variation in the field.
AB - The mosquito midgut microbiota has been shown to influence vector competence for multiple human pathogens. The microbiota is highly variable in the field, and the sources of this variability are not well understood, which limits our ability to understand or predict its effects on pathogen transmission. In this work, we report significant variation in female adult midgut bacterial load between strains of A. aegypti which vary in their susceptibility to dengue virus. Composition of the midgut microbiome was similar overall between the strains, with 81–92% of reads coming from the same five bacterial families, though we did detect differences in the presence of some bacterial families including Flavobacteriaceae and Entobacteriaceae. We conducted transcriptomic analysis on the two mosquito strains that showed the greatest difference in bacterial load, and found that they differ in transcript abundance of many genes implicated in amino acid metabolism, in particular the branched chain amino acid degradation pathway. We then silenced this pathway by targeting multiple genes using RNA interference, which resulted in strain-specific bacterial proliferation, thereby eliminating the difference in midgut bacterial load between the strains. This suggests that the branched chain amino acid (BCAA) degradation pathway controls midgut bacterial load, though the mechanism underlying this remains unclear. Overall, our results indicate that amino acid metabolism can act to influence the midgut microbiota. Moreover, they suggest that genetic or physiological variation in BCAA degradation pathway activity may in part explain midgut microbiota variation in the field.
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U2 - 10.1371/journal.pntd.0005677
DO - 10.1371/journal.pntd.0005677
M3 - Article
C2 - 28753661
AN - SCOPUS:85026726969
SN - 1935-2727
VL - 11
JO - PLoS Neglected Tropical Diseases
JF - PLoS Neglected Tropical Diseases
IS - 7
M1 - e0005677
ER -