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Title: Laboratory colonization by Dirofilaria immitis alters the microbiome of female Aedes aegypti mosquitoes

Journal Article · · Parasites & Vectors
 [1];  [2];  [3];  [3];  [3];  [3];  [4]; ORCiD logo [3]
  1. Univ. of Southern Mississippi, Hattiesburg, MS (United States). School of Biological, Environmental, and Earth Sciences. Center for Molecular and Cellular Biosciences
  2. Savannah River Site (SRS), Aiken, SC (United States). Savannah River Ecology Lab. (SREL); Univ. of Georgia, Athens, GA (United States). Warnell School of Forestry and Natural Resources
  3. Univ. of Southern Mississippi, Hattiesburg, MS (United States). School of Biological, Environmental, and Earth Sciences. Center for Molecular and Cellular Biosciences
  4. Savannah River Site (SRS), Aiken, SC (United States). Savannah River Ecology Lab. (SREL)

Background: The ability of blood-feeding arthropods to successfully acquire and transmit pathogens of medical and veterinary importance has been shown to be interfered with, or enhanced by, the arthropod’s native microbiome. Mosquitoes transmit viruses, protozoan and filarial nematodes, the majority of which contribute to the 17% of infectious disease cases worldwide. Diroflaria immitis, a mosquito-transmitted filarial nematodes of dogs and cats, is vectored by several mosquito species including Aedes aegypti. Methods: In this study, we investigated the impact of D. immitis colonization on the microbiome of laboratory reared female Ae. aegypti. Metagenomic analysis of the V3–V4 variable region of the microbial 16S RNA gene was used for identification of the microbial differences down to species level. Results: We generated a total of 1068 OTUs representing 16 phyla, 181 genera and 271 bacterial species. Overall, in order of abundance, Proteobacteria, Bacteroidetes, Actinobacteria and Firmicutes were the most represented phylum with D. immitis-infected mosquitoes having more of Proteobacteria (71%) than uninfected mosquitoes (56.9%). An interesting finding in this study is the detection of Klebsiella oxytoca in relatively similar abundance in infected and uninfected mosquitoes, suggesting a possible endosymbiotic relationship, and has been previously shown to indirectly compete for nutrients with fungi on domestic housefly eggs and larvae. While D. immitis colonization has no effect on the overall species richness, we identified significant differences in the composition of selected bacterial genera and phyla between the two groups. We also reported distinct compositional and phylogenetic differences in the individual bacterial species when commonly identified bacteria were compared. Conclusions: To the best of our knowledge, this is the first study to understand the impact of a filarial infection on the microbiome of its mosquito vector. Further studies are required to identify bacteria species that could play an important role in the mosquito biology. While the microbiome composition of Ae. aegypti mosquito have been previously reported, our study shows that in an effort to establish itself, a filarial nematode modifies and alters the overall microbial diversity within its mosquito host.

Research Organization:
Univ. of Georgia, Athens, GA (United States)
Sponsoring Organization:
USDOE Office of Environmental Management (EM)
Grant/Contract Number:
EM0004391
OSTI ID:
1799589
Journal Information:
Parasites & Vectors, Vol. 13, Issue 1; ISSN 1756-3305
Publisher:
BioMed CentralCopyright Statement
Country of Publication:
United States
Language:
English

References (49)

Heartworm Disease (Dirofilaria immitis) and Their Vectors in Europe – New Distribution Trends journal January 2012
Larval competition alters susceptibility of adult Aedes mosquitoes to dengue infection journal December 2007
Manipulation of the microbiota of mass-reared Mediterranean fruit flies Ceratitis capitata (Diptera: Tephritidae) improves sterile male sexual performance journal July 2009
The Tick Microbiome: Why Non-pathogenic Microorganisms Matter in Tick Biology and Pathogen Transmission journal June 2017
Tick-Pathogen Interactions and Vector Competence: Identification of Molecular Drivers for Tick-Borne Diseases journal April 2017
Relative contributions of various endogenous and exogenous factors to the mosquito microbiota journal December 2020
Factors influencing U.S. canine heartworm (Dirofilaria immitis) prevalence journal January 2014
Estimating bacteria diversity in different organs of nine species of mosquito by next generation sequencing journal October 2018
Wolbachia infection alters the relative abundance of resident bacteria in adult Aedes aegypti mosquitoes, but not larvae journal December 2017
Mosquitoes rely on their gut microbiota for development journal May 2014
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments journal March 2010
Isolation of Zika Virus from Aedes Aegypti Mosquitoes in Malaysia * journal May 1969
Increasing incidence of Dirofilaria immitis in dogs in USA with focus on the southeast region 2013–2016 journal January 2018
Bacteria on housefly eggs, Musca domestica, suppress fungal growth in chicken manure through nutrient depletion or antifungal metabolites journal July 2009
Macrocyclic lactone resistance in Dirofilaria immitis: Failure of heartworm preventives and investigation of genetic markers for resistance journal June 2015
Reciprocal Tripartite Interactions between the Aedes aegypti Midgut Microbiota, Innate Immune System and Dengue Virus Influences Vector Competence journal March 2012
Gut bacteria differentially affect egg production in the anautogenous mosquito Aedes aegypti and facultatively autogenous mosquito Aedes atropalpus (Diptera: Culicidae) journal June 2016
Comparative Susceptibility of Four Strains of Aedes Aegypti (Diptera: Culicidae) to Infection with Dirofilaria Immitis journal September 1981
Aedes aegypti vector competence studies: A review journal January 2019
Forecasting United States heartworm Dirofilaria immitis prevalence in dogs journal October 2016
Composition and functional roles of the gut microbiota in mosquitoes journal August 2018
Differential responses of the mosquito Aedes albopictus from the Indian Ocean region to two chikungunya isolates journal January 2010
Natural Microbe-Mediated Refractoriness to Plasmodium Infection in Anopheles gambiae journal May 2011
Macrocyclic lactone resistance in Dirofilaria immitis journal September 2011
Contribution of midgut bacteria to blood digestion and egg production in Aedes aegypti (diptera: culicidae) (L.) journal January 2011
The Composition of Midgut Bacteria in Aedes aegypti (Diptera: Culicidae) That Are Naturally Susceptible or Refractory to Dengue Viruses journal November 2018
The mosquito holobiont: fresh insight into mosquito-microbiota interactions journal March 2018
DADA2: High-resolution sample inference from Illumina amplicon data journal May 2016
The gut microbiota of insects – diversity in structure and function journal September 2013
Mosquito Infection Responses to Developing Filarial Worms journal October 2009
Multidrug resistant Enterobacteriaceae and extended spectrum β-lactamase producing Escherichia coli: a cross-sectional study in National Kidney Center, Nepal journal October 2015
MicrobiomeAnalyst: a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data journal April 2017
Use of MALDI-TOF MS to identify the culturable midgut microbiota of laboratory and wild mosquitoes journal December 2019
The mosquito microbiota influences vector competence for human pathogens journal September 2014
Dirofilaria immitis Infection of a Snow Leopard (Uncia uncia) in a Japanese Zoo with Mitochondrial DNA Analysis journal January 2003
Development of an in vitro bioassay for measuring susceptibility to macrocyclic lactone anthelmintics in Dirofilaria immitis journal December 2013
Using MicrobiomeAnalyst for comprehensive statistical, functional, and meta-analysis of microbiome data journal January 2020
Public health aspects of dirofilariasis in the United States journal October 2005
The NIH-NIAID Filariasis Research Reagent Resource Center journal November 2011
Exploring A nopheles gut bacteria for P lasmodium blocking activity: Anti- Plasmodium microbes journal February 2014
The functional microbiome of arthropods journal May 2017
Diversity and function of bacterial microbiota in the mosquito holobiont journal January 2013
Dynamic Gut Microbiome across Life History of the Malaria Mosquito Anopheles gambiae in Kenya journal September 2011
Evidence for Macrocyclic Lactone Anthelmintic Resistance in Dirofilaria immitis journal November 2011
Mosquito Vectors of Dog Heartworm in the United States: Vector Status and Factors Influencing Transmission Efficiency journal November 2011
Heartworm Biology, Treatment, and Control journal November 2009
Reactive Oxygen Species Modulate Anopheles gambiae Immunity against Bacteria and Plasmodium journal February 2008
Activation of mosquito immunity blocks the development of transmission-stage filarial nematodes journal February 2020
16S Metagenomic Comparison of Plasmodium falciparum–Infected and Noninfected Anopheles gambiae and Anopheles funestus Microbiota from Senegal journal December 2018