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The reproductive tracts of two malaria vectors are populated by a core microbiome and by gender- and swarm-enriched microbial biomarkers.

Segata N, Baldini F, Pompon J, Garrett WS, Truong DT, Dabiré RK, Diabaté A, Levashina EA, Catteruccia F - Sci Rep (2016)

Bottom Line: Microbes play key roles in shaping the physiology of insects and can influence behavior, reproduction and susceptibility to pathogens.We analyzed the reproductive microbiomes of male and female An. gambiae and An. coluzzii couples collected from natural mating swarms in Burkina Faso. 16S rRNA sequencing on dissected tissues revealed that the reproductive tracts harbor a complex microbiome characterized by a large core group of bacteria shared by both species and all reproductive tissues.Interestingly, we detected a significant enrichment of several gender-associated microbial biomarkers in specific tissues, and surprisingly, similar classes of bacteria in males captured from one mating swarm, suggesting that these males originated from the same larval breeding site.

View Article: PubMed Central - PubMed

Affiliation: Centre for Integrative Biology, University of Trento, Trento, Italy.

ABSTRACT
Microbes play key roles in shaping the physiology of insects and can influence behavior, reproduction and susceptibility to pathogens. In Sub-Saharan Africa, two major malaria vectors, Anopheles gambiae and An. coluzzii, breed in distinct larval habitats characterized by different microorganisms that might affect their adult physiology and possibly Plasmodium transmission. We analyzed the reproductive microbiomes of male and female An. gambiae and An. coluzzii couples collected from natural mating swarms in Burkina Faso. 16S rRNA sequencing on dissected tissues revealed that the reproductive tracts harbor a complex microbiome characterized by a large core group of bacteria shared by both species and all reproductive tissues. Interestingly, we detected a significant enrichment of several gender-associated microbial biomarkers in specific tissues, and surprisingly, similar classes of bacteria in males captured from one mating swarm, suggesting that these males originated from the same larval breeding site. Finally, we identified several endosymbiotic bacteria, including Spiroplasma, which have the ability to manipulate insect reproductive success. Our study provides a comprehensive analysis of the reproductive microbiome of important human disease vectors, and identifies a panel of core and endosymbiotic bacteria that can be potentially exploited to interfere with the transmission of malaria parasites by the Anopheles mosquito.

No MeSH data available.


Related in: MedlinePlus

Whole-metagenome shotgun sequencing of testes and ovaries highlights members of the microbiome at the species level.(A) Species level abundances as estimated by MetaPhlAn highlight the presence of Acinetobacter lwoffi, Propionibacterium acnes, Kocuria, Pseudomonas, Kocuria rhizophila and Micrococcus luteus in at least two of the three samples. The other organisms present in one sample only are Streptococcus mitis, Stenotrophomonas maltophilia and Aereococcus vididans. (B) Mapping of the metagenomic sample with highest A. lwoffii abundance against the genetically closest genome in the species (NIPH 478) highlights a consistent coverage of the large majority of the genes.
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f3: Whole-metagenome shotgun sequencing of testes and ovaries highlights members of the microbiome at the species level.(A) Species level abundances as estimated by MetaPhlAn highlight the presence of Acinetobacter lwoffi, Propionibacterium acnes, Kocuria, Pseudomonas, Kocuria rhizophila and Micrococcus luteus in at least two of the three samples. The other organisms present in one sample only are Streptococcus mitis, Stenotrophomonas maltophilia and Aereococcus vididans. (B) Mapping of the metagenomic sample with highest A. lwoffii abundance against the genetically closest genome in the species (NIPH 478) highlights a consistent coverage of the large majority of the genes.

Mentions: Whole-metagenome shotgun sequencing (WGS)37 of three An. coluzzii reproductive tissues confirmed our results and identified Acinetobacter lwoffii as the species in the Acinetobacter genus previously detected by 16S rRNA sequencing (Fig. 3A,B). Our A. lwoffii reads provided almost complete genome coverage and placed the Anopheles strain close to the previously published NIPH 478 (Fig. 3B). Escherichia coli was the prevalent microorganism in the Enterobacteriaceae family, and Propionibacterium acnes were identified in all three samples. We observed lower intra-sample diversity than in the 16S rRNA dataset likely due to the reduced sensitivity achievable by WGS, especially given the high fraction of host DNA contamination. This may explain the absence of Acinetobacter in one of three samples sequenced (Fig. 3A).


The reproductive tracts of two malaria vectors are populated by a core microbiome and by gender- and swarm-enriched microbial biomarkers.

Segata N, Baldini F, Pompon J, Garrett WS, Truong DT, Dabiré RK, Diabaté A, Levashina EA, Catteruccia F - Sci Rep (2016)

Whole-metagenome shotgun sequencing of testes and ovaries highlights members of the microbiome at the species level.(A) Species level abundances as estimated by MetaPhlAn highlight the presence of Acinetobacter lwoffi, Propionibacterium acnes, Kocuria, Pseudomonas, Kocuria rhizophila and Micrococcus luteus in at least two of the three samples. The other organisms present in one sample only are Streptococcus mitis, Stenotrophomonas maltophilia and Aereococcus vididans. (B) Mapping of the metagenomic sample with highest A. lwoffii abundance against the genetically closest genome in the species (NIPH 478) highlights a consistent coverage of the large majority of the genes.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4834568&req=5

f3: Whole-metagenome shotgun sequencing of testes and ovaries highlights members of the microbiome at the species level.(A) Species level abundances as estimated by MetaPhlAn highlight the presence of Acinetobacter lwoffi, Propionibacterium acnes, Kocuria, Pseudomonas, Kocuria rhizophila and Micrococcus luteus in at least two of the three samples. The other organisms present in one sample only are Streptococcus mitis, Stenotrophomonas maltophilia and Aereococcus vididans. (B) Mapping of the metagenomic sample with highest A. lwoffii abundance against the genetically closest genome in the species (NIPH 478) highlights a consistent coverage of the large majority of the genes.
Mentions: Whole-metagenome shotgun sequencing (WGS)37 of three An. coluzzii reproductive tissues confirmed our results and identified Acinetobacter lwoffii as the species in the Acinetobacter genus previously detected by 16S rRNA sequencing (Fig. 3A,B). Our A. lwoffii reads provided almost complete genome coverage and placed the Anopheles strain close to the previously published NIPH 478 (Fig. 3B). Escherichia coli was the prevalent microorganism in the Enterobacteriaceae family, and Propionibacterium acnes were identified in all three samples. We observed lower intra-sample diversity than in the 16S rRNA dataset likely due to the reduced sensitivity achievable by WGS, especially given the high fraction of host DNA contamination. This may explain the absence of Acinetobacter in one of three samples sequenced (Fig. 3A).

Bottom Line: Microbes play key roles in shaping the physiology of insects and can influence behavior, reproduction and susceptibility to pathogens.We analyzed the reproductive microbiomes of male and female An. gambiae and An. coluzzii couples collected from natural mating swarms in Burkina Faso. 16S rRNA sequencing on dissected tissues revealed that the reproductive tracts harbor a complex microbiome characterized by a large core group of bacteria shared by both species and all reproductive tissues.Interestingly, we detected a significant enrichment of several gender-associated microbial biomarkers in specific tissues, and surprisingly, similar classes of bacteria in males captured from one mating swarm, suggesting that these males originated from the same larval breeding site.

View Article: PubMed Central - PubMed

Affiliation: Centre for Integrative Biology, University of Trento, Trento, Italy.

ABSTRACT
Microbes play key roles in shaping the physiology of insects and can influence behavior, reproduction and susceptibility to pathogens. In Sub-Saharan Africa, two major malaria vectors, Anopheles gambiae and An. coluzzii, breed in distinct larval habitats characterized by different microorganisms that might affect their adult physiology and possibly Plasmodium transmission. We analyzed the reproductive microbiomes of male and female An. gambiae and An. coluzzii couples collected from natural mating swarms in Burkina Faso. 16S rRNA sequencing on dissected tissues revealed that the reproductive tracts harbor a complex microbiome characterized by a large core group of bacteria shared by both species and all reproductive tissues. Interestingly, we detected a significant enrichment of several gender-associated microbial biomarkers in specific tissues, and surprisingly, similar classes of bacteria in males captured from one mating swarm, suggesting that these males originated from the same larval breeding site. Finally, we identified several endosymbiotic bacteria, including Spiroplasma, which have the ability to manipulate insect reproductive success. Our study provides a comprehensive analysis of the reproductive microbiome of important human disease vectors, and identifies a panel of core and endosymbiotic bacteria that can be potentially exploited to interfere with the transmission of malaria parasites by the Anopheles mosquito.

No MeSH data available.


Related in: MedlinePlus