Dynamic Gut Microbiome across Life History of the Malaria Mosquito Anopheles gambiae in Kenya

Abstract

The mosquito gut represents an ecosystem that accommodates a complex, intimately associated microbiome. It is increasingly clear that the gut microbiome influences a wide variety of host traits, such as fitness and immunity. Understanding the microbial community structure and its dynamics across mosquito life is a prerequisite for comprehending the symbiotic relationship between the mosquito and its gut microbial residents. Here we characterized gut bacterial communities across larvae, pupae and adults of Anopheles gambiae reared in semi-natural habitats in Kenya by pyrosequencing bacterial 16S rRNA fragments. Immatures and adults showed distinctive gut community structures. Photosynthetic Cyanobacteria were predominant in the larval and pupal guts while Proteobacteria and Bacteroidetes dominated the adult guts, with core taxa of Enterobacteriaceae and Flavobacteriaceae. At the adult stage, diet regime (sugar meal and blood meal) significantly affects the microbial structure. Intriguingly, blood meals drastically reduced the community diversity and favored enteric bacteria. Comparative genomic analysis revealed that the enriched enteric bacteria possess large genetic redox capacity of coping with oxidative and nitrosative stresses that are associated with the catabolism of blood meal, suggesting a beneficial role in maintaining gut redox homeostasis. Interestingly, gut community structure was similar in the adult stage between the field and laboratory mosquitoes, indicating that mosquito gut is a selective eco-environment for its microbiome. This comprehensive gut metatgenomic profile suggests a concerted symbiotic genetic association between gut inhabitants and host.

Mosquito vector‐associated microbiota: Metabarcoding bacteria and eukaryotic symbionts across habitat types in Thailand endemic for dengue and other arthropod‐borne diseases

“…Previous studies mainly focused on noneukaryotic microbes in the midgut using either culture‐dependent or culture‐independent methods (Minard, Mavingui, & Moro, 2013). Those that applied the culture‐independent deep sequencing approach were mainly restricted to gut bacterial communities (Minard et al., 2012; Wang, Gilbreath, Kukutla, Yan, & Xu, 2011) or other isolated adult arthropod parts (Damiani et al., 2010; Sharma et al., 2014), although one study investigated bacteria diversity from whole Ae. albopictus (Minard et al., 2014).…”

“…For example, a median of 42 bacterial OTUs was estimated from the guts of eight mosquito species (Minard et al., 2012); higher still by at least 200 OTUs was the bacterial richness in the gut of a single adult Anopheles gambiae (Wang et al., 2011). This enormous variability amongst studies, including ours, likely reflects inherent differences in microbiota diversity, composition, and heterogeneity amongst individuals, due to vector species and site of mosquito collection.…”

“…Similarly, we employed multiple trap types to attract a range of mosquito species, but these also target mosquitoes at different physiological states (e.g., recently bloodfed, resting, or host‐seeking). Although some studies suggest that physiological state may affect the composition and diversity of midgut microbiota (Wang et al., 2011; Yadav et al., 2016), others have demonstrated that Ae. aegypti harbors a stable bacterial community during its adult life (David, dos Santos, Vicente, & Maciel‐de‐Freitas, 2016).…”

“…Others have shown that mosquito midgut bacterial communities are dynamic and vary significantly with respect to bloodfed state (Wang et al., 2011). Host DNA is detectable by sequencing even when engorgement is no longer visible (Davey, Casey, Burgess, & Cable, 2007; Lee et al., 2002), and quite interestingly, we identified 18S rRNA sequences belonging to phylum Chordata, class Mammalia, in a few of our mosquito samples.…”

Comparative gut transcriptome analysis reveals differences between virulent and avirulent Russian wheat aphids, Diuraphis noxia

“…The gut transcriptomes of both hematophagous and phytophagous insects have been investigated extensively (Morris et al 2009, Wang et al 2011, Zhang et al 2010, Boissière et al 2012 However, we found it surprising to note the presence of greater sequence diversity in the RWA2 gut library, which shared maximum homology with that of several insect species.…”