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Western Kenyan Anopheles gambiae s.s. showing intense permethrin resistance harbor distinct microbiota

View ORCID ProfileDiana Omoke, Mathew Kipsum, Samson Otieno, Edward Esalimba, Mili Sheth, View ORCID ProfileAudrey Lenhart, View ORCID ProfileEzekiel Mugendi Njeru, View ORCID ProfileEric Ochomo, View ORCID ProfileNsa Dada
doi: https://doi.org/10.1101/2020.11.12.378760
Diana Omoke
1Department of Biochemistry, Microbiology and Biotechnology, Kenyatta University, Nairobi, Kenya
2Entomology section, Center for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya
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Mathew Kipsum
2Entomology section, Center for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya
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Samson Otieno
2Entomology section, Center for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya
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Edward Esalimba
2Entomology section, Center for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya
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Mili Sheth
3Biotechnology Core Facility Branch, Division of Scientific Resources, National Center for Emerging & Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA, United States of America
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Audrey Lenhart
4Entomology Branch, Division of Parasitic Diseases and Malaria, Center for Global Health, Centers for Diseases Control and Prevention, Atlanta, GA, United States of America
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Ezekiel Mugendi Njeru
1Department of Biochemistry, Microbiology and Biotechnology, Kenyatta University, Nairobi, Kenya
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Eric Ochomo
2Entomology section, Center for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya
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Nsa Dada
5Faculty of Science and Technology, Norwegian University of Life Science, Aas, Norway
6Public Health and Epidemiology Department, Nigerian Institute of Medical Research
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  • For correspondence: nsa.dada@nmbu.no nsadada@yahoo.com
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Abstract

Background Insecticide resistance poses a growing challenge to malaria vector control in Kenya and around the world. Following evidence of associations between the mosquito microbiota and insecticide resistance, we comparatively characterized the microbiota of An. gambiae s.s. from Tulukuyi village, Bungoma, Kenya, with differing permethrin resistance profiles.

Methods Using the CDC bottle bioassay, 133 2-3 day-old, virgin, non-blood fed female F1 progeny of field-caught An. gambiae s.s. were exposed to five times (107.5μg/ml) the discriminating dose of permethrin. Post bioassay, 50 resistant and 50 susceptible mosquitoes were subsequently screened for kdr East and West mutations, and individually processed for microbial analysis using high throughput sequencing targeting the universal bacterial and archaeal 16S rRNA gene.

Results 47% of the samples tested (n=133) were resistant, and of the 100 selected for further processing, 99% were positive for kdr East and 1% for kdr West. Overall, 84 bacterial taxa were detected across all mosquito samples, with 36 of these shared between resistant and susceptible mosquitoes. A total of 20 were unique to the resistant mosquitoes and 28 were unique to the susceptible mosquitoes. There were significant differences in bacterial composition between resistant and susceptible individuals (F=2.33, P=0.001), with presence of Sphingobacterium, Lysinibacillus and Streptococcus (all known pyrethroid-degrading taxa), and the radiotolerant Rubrobacter, being significantly associated with resistant mosquitoes. On the other hand, the presence of Myxococcus, was significantly associated with susceptible mosquitoes.

Conclusion This is the first report of distinct microbiota in An. gambiae s.s. associated with intense pyrethroid resistance. The findings highlight differentially abundant bacterial taxa between resistant and susceptible mosquitoes, and further suggest a microbe-mediated mechanism of insecticide resistance in mosquitoes. Our results also indicate fixation of the kdr East mutation in this mosquito population, precluding further analysis of its associations with the mosquito microbiota, but presenting the hypothesis that any microbe-mediated mechanism of insecticide resistance would be likely of a metabolic nature. Overall, this study lays initial groundwork for understanding microbe-mediated mechanisms of insecticide resistance in African malaria vectors, and potentially identifying novel microbial markers of insecticide resistance that could supplement existing vector surveillance tools.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted November 12, 2020.
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Western Kenyan Anopheles gambiae s.s. showing intense permethrin resistance harbor distinct microbiota
Diana Omoke, Mathew Kipsum, Samson Otieno, Edward Esalimba, Mili Sheth, Audrey Lenhart, Ezekiel Mugendi Njeru, Eric Ochomo, Nsa Dada
bioRxiv 2020.11.12.378760; doi: https://doi.org/10.1101/2020.11.12.378760
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Western Kenyan Anopheles gambiae s.s. showing intense permethrin resistance harbor distinct microbiota
Diana Omoke, Mathew Kipsum, Samson Otieno, Edward Esalimba, Mili Sheth, Audrey Lenhart, Ezekiel Mugendi Njeru, Eric Ochomo, Nsa Dada
bioRxiv 2020.11.12.378760; doi: https://doi.org/10.1101/2020.11.12.378760

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