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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

Core reproductive tract microbiome of An. gambiae and An. coluzzii.(A) Genera from both Gram-positive (Staphylococcus, Corynebacterium, Geobacillus, Micrococcus) and Gram-negative (Acinetobacter, Pseudomonas) bacteria constitute the core microbiome of the A. gambiae (Agam) and A. coluzzii (Acol) male and female reproductive tissues collected from three villages (VK5, VK7 and Soumousso). (B) Different core operational taxonomic units (OTUs) are present within the same genus, suggesting that a consistent species-level microbial diversity characterizes the reproductive tract microbiome. Gender, tissues (Ovaries and Lower Reproductive Tract for females, Testes and Male Accessory Glands for males), villages (Soumousso, VK5 and VK7), species (An. gambiae: Agam; and An. coluzzii: Acol) and swarm types (individual species or mixed) are color-coded as described in the legend on the left of the figure.
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f2: Core reproductive tract microbiome of An. gambiae and An. coluzzii.(A) Genera from both Gram-positive (Staphylococcus, Corynebacterium, Geobacillus, Micrococcus) and Gram-negative (Acinetobacter, Pseudomonas) bacteria constitute the core microbiome of the A. gambiae (Agam) and A. coluzzii (Acol) male and female reproductive tissues collected from three villages (VK5, VK7 and Soumousso). (B) Different core operational taxonomic units (OTUs) are present within the same genus, suggesting that a consistent species-level microbial diversity characterizes the reproductive tract microbiome. Gender, tissues (Ovaries and Lower Reproductive Tract for females, Testes and Male Accessory Glands for males), villages (Soumousso, VK5 and VK7), species (An. gambiae: Agam; and An. coluzzii: Acol) and swarm types (individual species or mixed) are color-coded as described in the legend on the left of the figure.

Mentions: Despite this large intra-sample variability, we identified a highly conserved core microbiome present in all samples and comprising OTUs spanning seven different bacterial genera with variable levels of abundance (Fig. 2). Acinetobacter, and specifically OTU 4482598, was the quantitatively dominant microorganism in the majority of the samples (avg. 16.3% s.d. 17.8%, min 0.4%, max 73.3%). This OTU matched the corresponding fragment of several distinct Acinetobacter lwoffii sequences stored in the public repositories, although some identical matches were also detected for other closely related species and unnamed organisms in the same genus. Other OTUs present in the core microbiome included Pseudomonas and Staphylococcus, genera containing species ubiquitous to a large number of environmental and host-associated habitats. Acinetobacter, Pseudomonas and Staphylococcus have also been detected at lower percentages in the midgut of An. gambiae females11 and other anophelines34. Two OTUs assigned to the Enterobacteriaceae were also present in all samples; the 16S rRNA sequence for bacteria in this family can be inconclusive at the genus level, but several organisms in this clade have been reported to colonize the Anopheles gut1135 with potential interaction with Plasmodium111436. Corynebacterium was also identified in all samples. As in previous sequencing studies with similar detection sensitivity11 this genus was only occasionally found in the Anopheles midgut, our finding possibly reflects specificity for reproductive tissues or for our geographical cohort.


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)

Core reproductive tract microbiome of An. gambiae and An. coluzzii.(A) Genera from both Gram-positive (Staphylococcus, Corynebacterium, Geobacillus, Micrococcus) and Gram-negative (Acinetobacter, Pseudomonas) bacteria constitute the core microbiome of the A. gambiae (Agam) and A. coluzzii (Acol) male and female reproductive tissues collected from three villages (VK5, VK7 and Soumousso). (B) Different core operational taxonomic units (OTUs) are present within the same genus, suggesting that a consistent species-level microbial diversity characterizes the reproductive tract microbiome. Gender, tissues (Ovaries and Lower Reproductive Tract for females, Testes and Male Accessory Glands for males), villages (Soumousso, VK5 and VK7), species (An. gambiae: Agam; and An. coluzzii: Acol) and swarm types (individual species or mixed) are color-coded as described in the legend on the left of the figure.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f2: Core reproductive tract microbiome of An. gambiae and An. coluzzii.(A) Genera from both Gram-positive (Staphylococcus, Corynebacterium, Geobacillus, Micrococcus) and Gram-negative (Acinetobacter, Pseudomonas) bacteria constitute the core microbiome of the A. gambiae (Agam) and A. coluzzii (Acol) male and female reproductive tissues collected from three villages (VK5, VK7 and Soumousso). (B) Different core operational taxonomic units (OTUs) are present within the same genus, suggesting that a consistent species-level microbial diversity characterizes the reproductive tract microbiome. Gender, tissues (Ovaries and Lower Reproductive Tract for females, Testes and Male Accessory Glands for males), villages (Soumousso, VK5 and VK7), species (An. gambiae: Agam; and An. coluzzii: Acol) and swarm types (individual species or mixed) are color-coded as described in the legend on the left of the figure.
Mentions: Despite this large intra-sample variability, we identified a highly conserved core microbiome present in all samples and comprising OTUs spanning seven different bacterial genera with variable levels of abundance (Fig. 2). Acinetobacter, and specifically OTU 4482598, was the quantitatively dominant microorganism in the majority of the samples (avg. 16.3% s.d. 17.8%, min 0.4%, max 73.3%). This OTU matched the corresponding fragment of several distinct Acinetobacter lwoffii sequences stored in the public repositories, although some identical matches were also detected for other closely related species and unnamed organisms in the same genus. Other OTUs present in the core microbiome included Pseudomonas and Staphylococcus, genera containing species ubiquitous to a large number of environmental and host-associated habitats. Acinetobacter, Pseudomonas and Staphylococcus have also been detected at lower percentages in the midgut of An. gambiae females11 and other anophelines34. Two OTUs assigned to the Enterobacteriaceae were also present in all samples; the 16S rRNA sequence for bacteria in this family can be inconclusive at the genus level, but several organisms in this clade have been reported to colonize the Anopheles gut1135 with potential interaction with Plasmodium111436. Corynebacterium was also identified in all samples. As in previous sequencing studies with similar detection sensitivity11 this genus was only occasionally found in the Anopheles midgut, our finding possibly reflects specificity for reproductive tissues or for our geographical cohort.

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