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French invasive Asian tiger mosquito populations harbor reduced bacterial microbiota and genetic diversity compared to Vietnamese autochthonous relatives.

Minard G, Tran FH, Van VT, Goubert C, Bellet C, Lambert G, Kim KL, Thuy TH, Mavingui P, Valiente Moro C - Front Microbiol (2015)

Bottom Line: The insect-associated microbiota is now recognized to play a significant role in host biology.Overall genetic diversities of both hosts and bacterial microbiota were significantly reduced in recently established populations of France compared to the autochthonous populations of Vietnam.These results open up many important avenues of investigation in order to link the process of geographical invasion to shifts in commensal and symbiotic microbiome communities, as such shifts may have dramatic impacts on the biology and/or vector competence of invading hematophagous insects.

View Article: PubMed Central - PubMed

Affiliation: Ecologie Microbienne, UMR Centre National de la Recherche Scientifique 5557, USC INRA 1364, VetAgro Sup, FR41 BioEnvironment and Health, Université Claude Bernard Lyon 1 Villeurbanne, France.

ABSTRACT
The Asian tiger mosquito Aedes albopictus is one of the most significant pathogen vectors of the twenty-first century. Originating from Asia, it has invaded a wide range of eco-climatic regions worldwide. The insect-associated microbiota is now recognized to play a significant role in host biology. While genetic diversity bottlenecks are known to result from biological invasions, the resulting shifts in host-associated microbiota diversity has not been thoroughly investigated. To address this subject, we compared four autochthonous Ae. albopictus populations in Vietnam, the native area of Ae. albopictus, and three populations recently introduced to Metropolitan France, with the aim of documenting whether these populations display differences in host genotype and bacterial microbiota. Population-level genetic diversity (microsatellite markers and COI haplotype) and bacterial diversity (16S rDNA metabarcoding) were compared between field-caught mosquitoes. Bacterial microbiota from the whole insect bodies were largely dominated by Wolbachia pipientis. Targeted analysis of the gut microbiota revealed a greater bacterial diversity in which a fraction was common between French and Vietnamese populations. The genus Dysgonomonas was the most prevalent and abundant across all studied populations. Overall genetic diversities of both hosts and bacterial microbiota were significantly reduced in recently established populations of France compared to the autochthonous populations of Vietnam. These results open up many important avenues of investigation in order to link the process of geographical invasion to shifts in commensal and symbiotic microbiome communities, as such shifts may have dramatic impacts on the biology and/or vector competence of invading hematophagous insects.

No MeSH data available.


Community structure and OTU-country associations. (A) Non-Metric Multidimentional Scaling plot represents Bray-Curtis β-diversity structure among individuals and populations. The loss function Stress = 0.09 and correlation with true distances R2 = 0.97. NC, Nice; PLV, Porte-lès-Valence; SP, Saint Priest; VT, Vung Tàu City; HCM, Hồ Chí Minh City; BD, Bình Du'o'ng; BGM, Bù Gia Mâp. (B) Difference in OTU abundance between midgut bacterial microbiota of French and Vietnamese Ae. albopictus. Display represents extended error bars of significant fold-changes (P>0.05) between midgut samples from France (F) and Vietnam (V). (C) Venn diagram representing shared OTUs between midgut samples from France and Vietnam. The intersection of both circles represents the number of shared OTUs between France and Vietnam. To avoid size effect, sequences were merged per group, and then subsampled.
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Figure 4: Community structure and OTU-country associations. (A) Non-Metric Multidimentional Scaling plot represents Bray-Curtis β-diversity structure among individuals and populations. The loss function Stress = 0.09 and correlation with true distances R2 = 0.97. NC, Nice; PLV, Porte-lès-Valence; SP, Saint Priest; VT, Vung Tàu City; HCM, Hồ Chí Minh City; BD, Bình Du'o'ng; BGM, Bù Gia Mâp. (B) Difference in OTU abundance between midgut bacterial microbiota of French and Vietnamese Ae. albopictus. Display represents extended error bars of significant fold-changes (P>0.05) between midgut samples from France (F) and Vietnam (V). (C) Venn diagram representing shared OTUs between midgut samples from France and Vietnam. The intersection of both circles represents the number of shared OTUs between France and Vietnam. To avoid size effect, sequences were merged per group, and then subsampled.

Mentions: The insect gut is a key organ in insect physiology and immunity. Moreover, previous studies have demonstrated that this organ harbored low concentration of Wolbachia in Ae. albopictus adults (Zouache et al., 2009), opening up the possibility to extend the depth of analysis of the gut-associated microbial community. For this purpose, V5-V6 rrs amplicons from 32 individual midgut samples (from 3 to 5 individuals per sampling site) were sequenced with MiSeq technology. Analysis of a negative control showed the presence of bacterial sequences that probably derived from contamination during laboratory sample handling (Table S6). However, the diversity of this control was dissimilar from those of all mosquito samples (Bray-Curtis dissimilarity > 68.6%). For subsequent analysis of sequences associated with mosquito samples, OTUs potentially originating from laboratory contamination were trimmed from the whole dataset. Based on this analysis, a total of 2,088 OTUs were identified in all the midgut samples (between 306 and 1,272 OTUs per sample), with a total of 68 OTUs exceeding 1% in abundance. These OTU numbers were consistent with those previously obtained by high throughput sequencing of midguts from various mosquito species (Osei-Poku et al., 2012). The genus Dysgonomonas was the most prevalent and abundant OTU retrieved from the midgut samples (Figure S3), although its abundance varied from 3% (HCM8) to 72% (SP7) between samples (Figure 3). AMOVA analysis and ordinations were performed to detect the degree of differentiation at various hierarchical levels. No significant variation was observed between sites, indicating a low variability between individuals belonging to a given population. In contrast, variation between countries was found to be significant for the β-diversity measure, explaining a large part of the variation for Bray-Curtis dissimilarities (AMOVA, 22.79%, p < 10−4) (Table 1, Figure 4A). Similar structures were obtained with Unifrac phylogeny based β-diversity distances (Table S3). Consequently, further comparisons of populations were performed at the country level. When compared with the four populations from Vietnam, consisting of a total of 14 individuals, the three populations from France composed of 18 individuals harbored less diverse and more homogeneous bacterial microbiota, indicated by lower values for the Chao 1 richness estimator (Mann–Whitney Wilcoxon, p = 0.002), Shannon-Weather α-diversity (Mann–Whitney Wilcoxon, p < 10−3) and variance of abundance-weighted β-diversity (Figure S2). However, Bray-Curtis (Beta-dispersion, p = 0.33) distances were not significantly different between populations of the two countries.


French invasive Asian tiger mosquito populations harbor reduced bacterial microbiota and genetic diversity compared to Vietnamese autochthonous relatives.

Minard G, Tran FH, Van VT, Goubert C, Bellet C, Lambert G, Kim KL, Thuy TH, Mavingui P, Valiente Moro C - Front Microbiol (2015)

Community structure and OTU-country associations. (A) Non-Metric Multidimentional Scaling plot represents Bray-Curtis β-diversity structure among individuals and populations. The loss function Stress = 0.09 and correlation with true distances R2 = 0.97. NC, Nice; PLV, Porte-lès-Valence; SP, Saint Priest; VT, Vung Tàu City; HCM, Hồ Chí Minh City; BD, Bình Du'o'ng; BGM, Bù Gia Mâp. (B) Difference in OTU abundance between midgut bacterial microbiota of French and Vietnamese Ae. albopictus. Display represents extended error bars of significant fold-changes (P>0.05) between midgut samples from France (F) and Vietnam (V). (C) Venn diagram representing shared OTUs between midgut samples from France and Vietnam. The intersection of both circles represents the number of shared OTUs between France and Vietnam. To avoid size effect, sequences were merged per group, and then subsampled.
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Related In: Results  -  Collection

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Figure 4: Community structure and OTU-country associations. (A) Non-Metric Multidimentional Scaling plot represents Bray-Curtis β-diversity structure among individuals and populations. The loss function Stress = 0.09 and correlation with true distances R2 = 0.97. NC, Nice; PLV, Porte-lès-Valence; SP, Saint Priest; VT, Vung Tàu City; HCM, Hồ Chí Minh City; BD, Bình Du'o'ng; BGM, Bù Gia Mâp. (B) Difference in OTU abundance between midgut bacterial microbiota of French and Vietnamese Ae. albopictus. Display represents extended error bars of significant fold-changes (P>0.05) between midgut samples from France (F) and Vietnam (V). (C) Venn diagram representing shared OTUs between midgut samples from France and Vietnam. The intersection of both circles represents the number of shared OTUs between France and Vietnam. To avoid size effect, sequences were merged per group, and then subsampled.
Mentions: The insect gut is a key organ in insect physiology and immunity. Moreover, previous studies have demonstrated that this organ harbored low concentration of Wolbachia in Ae. albopictus adults (Zouache et al., 2009), opening up the possibility to extend the depth of analysis of the gut-associated microbial community. For this purpose, V5-V6 rrs amplicons from 32 individual midgut samples (from 3 to 5 individuals per sampling site) were sequenced with MiSeq technology. Analysis of a negative control showed the presence of bacterial sequences that probably derived from contamination during laboratory sample handling (Table S6). However, the diversity of this control was dissimilar from those of all mosquito samples (Bray-Curtis dissimilarity > 68.6%). For subsequent analysis of sequences associated with mosquito samples, OTUs potentially originating from laboratory contamination were trimmed from the whole dataset. Based on this analysis, a total of 2,088 OTUs were identified in all the midgut samples (between 306 and 1,272 OTUs per sample), with a total of 68 OTUs exceeding 1% in abundance. These OTU numbers were consistent with those previously obtained by high throughput sequencing of midguts from various mosquito species (Osei-Poku et al., 2012). The genus Dysgonomonas was the most prevalent and abundant OTU retrieved from the midgut samples (Figure S3), although its abundance varied from 3% (HCM8) to 72% (SP7) between samples (Figure 3). AMOVA analysis and ordinations were performed to detect the degree of differentiation at various hierarchical levels. No significant variation was observed between sites, indicating a low variability between individuals belonging to a given population. In contrast, variation between countries was found to be significant for the β-diversity measure, explaining a large part of the variation for Bray-Curtis dissimilarities (AMOVA, 22.79%, p < 10−4) (Table 1, Figure 4A). Similar structures were obtained with Unifrac phylogeny based β-diversity distances (Table S3). Consequently, further comparisons of populations were performed at the country level. When compared with the four populations from Vietnam, consisting of a total of 14 individuals, the three populations from France composed of 18 individuals harbored less diverse and more homogeneous bacterial microbiota, indicated by lower values for the Chao 1 richness estimator (Mann–Whitney Wilcoxon, p = 0.002), Shannon-Weather α-diversity (Mann–Whitney Wilcoxon, p < 10−3) and variance of abundance-weighted β-diversity (Figure S2). However, Bray-Curtis (Beta-dispersion, p = 0.33) distances were not significantly different between populations of the two countries.

Bottom Line: The insect-associated microbiota is now recognized to play a significant role in host biology.Overall genetic diversities of both hosts and bacterial microbiota were significantly reduced in recently established populations of France compared to the autochthonous populations of Vietnam.These results open up many important avenues of investigation in order to link the process of geographical invasion to shifts in commensal and symbiotic microbiome communities, as such shifts may have dramatic impacts on the biology and/or vector competence of invading hematophagous insects.

View Article: PubMed Central - PubMed

Affiliation: Ecologie Microbienne, UMR Centre National de la Recherche Scientifique 5557, USC INRA 1364, VetAgro Sup, FR41 BioEnvironment and Health, Université Claude Bernard Lyon 1 Villeurbanne, France.

ABSTRACT
The Asian tiger mosquito Aedes albopictus is one of the most significant pathogen vectors of the twenty-first century. Originating from Asia, it has invaded a wide range of eco-climatic regions worldwide. The insect-associated microbiota is now recognized to play a significant role in host biology. While genetic diversity bottlenecks are known to result from biological invasions, the resulting shifts in host-associated microbiota diversity has not been thoroughly investigated. To address this subject, we compared four autochthonous Ae. albopictus populations in Vietnam, the native area of Ae. albopictus, and three populations recently introduced to Metropolitan France, with the aim of documenting whether these populations display differences in host genotype and bacterial microbiota. Population-level genetic diversity (microsatellite markers and COI haplotype) and bacterial diversity (16S rDNA metabarcoding) were compared between field-caught mosquitoes. Bacterial microbiota from the whole insect bodies were largely dominated by Wolbachia pipientis. Targeted analysis of the gut microbiota revealed a greater bacterial diversity in which a fraction was common between French and Vietnamese populations. The genus Dysgonomonas was the most prevalent and abundant across all studied populations. Overall genetic diversities of both hosts and bacterial microbiota were significantly reduced in recently established populations of France compared to the autochthonous populations of Vietnam. These results open up many important avenues of investigation in order to link the process of geographical invasion to shifts in commensal and symbiotic microbiome communities, as such shifts may have dramatic impacts on the biology and/or vector competence of invading hematophagous insects.

No MeSH data available.