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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

Relative abundance plot for microbial clades strongly associated with males from a specific swarm (swarm 2.3).Bar plots represent the relative abundance (indicated on the Y-axis) of Shewanella, Rhodocyclaceae, Pseudomonas, and Azospira in mosquito samples from three villages (VK5, VK7 and Soumousso, indicated by different color codes. VK5: green; VK7: blue; Soumousso: pink). Each swarm is identified by a numerical code (top bar). Swarm location is provided in Fig. 1. Reproductive tissues collected from male and female individuals from each swarm are represented by color-coded bars. Ovaries: pink; Lower Reproductive Tract (LRT): yellow; Male Accessory Glands (MAGs): green; Testes: blue. Species are indicated by a different bar outline color (An. gambiae: red; An. coluzzii: black). Shewanella, Rhodocyclaceae, Pseudomonas, and Azospira were highly enriched in male tissues (both MAGs and testes) from a specific swarm (swarm 2.3) from the VK7 village. Please note that some tissues collected from females from swarm 2.3 failed the 16S rRNA sequencing. A detailed list of tissues sequenced for each swarm is provided in Supplementary Table 2.
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f6: Relative abundance plot for microbial clades strongly associated with males from a specific swarm (swarm 2.3).Bar plots represent the relative abundance (indicated on the Y-axis) of Shewanella, Rhodocyclaceae, Pseudomonas, and Azospira in mosquito samples from three villages (VK5, VK7 and Soumousso, indicated by different color codes. VK5: green; VK7: blue; Soumousso: pink). Each swarm is identified by a numerical code (top bar). Swarm location is provided in Fig. 1. Reproductive tissues collected from male and female individuals from each swarm are represented by color-coded bars. Ovaries: pink; Lower Reproductive Tract (LRT): yellow; Male Accessory Glands (MAGs): green; Testes: blue. Species are indicated by a different bar outline color (An. gambiae: red; An. coluzzii: black). Shewanella, Rhodocyclaceae, Pseudomonas, and Azospira were highly enriched in male tissues (both MAGs and testes) from a specific swarm (swarm 2.3) from the VK7 village. Please note that some tissues collected from females from swarm 2.3 failed the 16S rRNA sequencing. A detailed list of tissues sequenced for each swarm is provided in Supplementary Table 2.

Mentions: We found an enrichment in specific bacteria in some swarm locations. Three males collected in the VK7 village from the same mating swarm (swarm 2.3, adjacent to a rice paddy, Fig. 1) showed a highly significant enrichment in Shewanella, Rhodocyclacea, Pseudomonas and Azospira in both testes and MAGs (Fig. 6). These bacteria were detected at much lower abundance in females mated to these males, as well as in males and females from swarm locations at the other end of the VK7 village or in the other villages. Shewanella, Rhodocyclacea and Pseudomonas share some genetic similarities with each other and are often found in water, including rice fields, while some Azospira genera are root bacteria with metal bioactivity. As the reproductive microbiome of adults is largely shaped during larval development, it is likely that local environmental factors have favored the proliferation of these microbes in the rice fields surrounding the swarm location. These findings suggest the hypothesis that males from the same larval breeding sites may tend to swarm together. Genetic analyses will be needed to test the hypothesis of a possible degree of kinship within male swarms.


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)

Relative abundance plot for microbial clades strongly associated with males from a specific swarm (swarm 2.3).Bar plots represent the relative abundance (indicated on the Y-axis) of Shewanella, Rhodocyclaceae, Pseudomonas, and Azospira in mosquito samples from three villages (VK5, VK7 and Soumousso, indicated by different color codes. VK5: green; VK7: blue; Soumousso: pink). Each swarm is identified by a numerical code (top bar). Swarm location is provided in Fig. 1. Reproductive tissues collected from male and female individuals from each swarm are represented by color-coded bars. Ovaries: pink; Lower Reproductive Tract (LRT): yellow; Male Accessory Glands (MAGs): green; Testes: blue. Species are indicated by a different bar outline color (An. gambiae: red; An. coluzzii: black). Shewanella, Rhodocyclaceae, Pseudomonas, and Azospira were highly enriched in male tissues (both MAGs and testes) from a specific swarm (swarm 2.3) from the VK7 village. Please note that some tissues collected from females from swarm 2.3 failed the 16S rRNA sequencing. A detailed list of tissues sequenced for each swarm is provided in Supplementary Table 2.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f6: Relative abundance plot for microbial clades strongly associated with males from a specific swarm (swarm 2.3).Bar plots represent the relative abundance (indicated on the Y-axis) of Shewanella, Rhodocyclaceae, Pseudomonas, and Azospira in mosquito samples from three villages (VK5, VK7 and Soumousso, indicated by different color codes. VK5: green; VK7: blue; Soumousso: pink). Each swarm is identified by a numerical code (top bar). Swarm location is provided in Fig. 1. Reproductive tissues collected from male and female individuals from each swarm are represented by color-coded bars. Ovaries: pink; Lower Reproductive Tract (LRT): yellow; Male Accessory Glands (MAGs): green; Testes: blue. Species are indicated by a different bar outline color (An. gambiae: red; An. coluzzii: black). Shewanella, Rhodocyclaceae, Pseudomonas, and Azospira were highly enriched in male tissues (both MAGs and testes) from a specific swarm (swarm 2.3) from the VK7 village. Please note that some tissues collected from females from swarm 2.3 failed the 16S rRNA sequencing. A detailed list of tissues sequenced for each swarm is provided in Supplementary Table 2.
Mentions: We found an enrichment in specific bacteria in some swarm locations. Three males collected in the VK7 village from the same mating swarm (swarm 2.3, adjacent to a rice paddy, Fig. 1) showed a highly significant enrichment in Shewanella, Rhodocyclacea, Pseudomonas and Azospira in both testes and MAGs (Fig. 6). These bacteria were detected at much lower abundance in females mated to these males, as well as in males and females from swarm locations at the other end of the VK7 village or in the other villages. Shewanella, Rhodocyclacea and Pseudomonas share some genetic similarities with each other and are often found in water, including rice fields, while some Azospira genera are root bacteria with metal bioactivity. As the reproductive microbiome of adults is largely shaped during larval development, it is likely that local environmental factors have favored the proliferation of these microbes in the rice fields surrounding the swarm location. These findings suggest the hypothesis that males from the same larval breeding sites may tend to swarm together. Genetic analyses will be needed to test the hypothesis of a possible degree of kinship within male swarms.

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