Variation between the oral and faecal microbiota in a free-living passerine bird, the great tit (Parus major)

Abstract

The gastrointestinal tract of vertebrates is inhabited by diverse bacterial communities that induce marked effects on the host physiology and health status. The composition of the gastrointestinal microbiota is characterized by pronounced taxonomic and functional variability among different regions of the vertebrate gastrointestinal tract. Despite the relatively solid knowledge on the among-region variations of the gastrointestinal microbiota in model mammalian species, there are only a few studies concerning among-region variations of the gastrointestinal microbiota in free-living non-mammalian vertebrate taxa. We used Illumina MiSeq sequencing of bacterial 16S rRNA amplicons to compare the diversity as well as taxonomic composition of bacterial communities in proximal vs. distal parts of the gastrointestinal tract (represented by oral swabs and faecal samples, respectively) in a wild passerine bird, the great tit (Parus major). The diversity of the oral microbiota was significantly higher compared to the faecal microbiota, whereas interindividual variation was higher in faecal than in oral samples. We also observed a pronounced difference in taxonomic content between the oral and faecal microbiota. Bacteria belonging to the phyla Proteobacteria, Firmicutes and Actinobacteria typically dominated in both oral and faecal samples. A high abundance of bacteria belonging to Tenericutes was observed only in faecal samples. Surprisingly, we found only a slight correlation between the faecal and oral microbiota at the within-individual level, suggesting that the microbial composition in these body sites is shaped by independent regulatory processes. Given the independence of these two communities at the individual level, we propose that simultaneous sampling of the faecal and oral microbiota will extend our understanding of host vs. microbiota interactions in wild populations.

Cloacal swabs and alcohol bird specimens are good proxies for compositional analyses of gut microbial communities of Great tits (Parus major)

“…We first demonstrated that digestive tract regions of wild P. major differ in gut microbial communities, but that these differences are not as prominent as previous studies have documented in other bird species [2,5,30,31]. While compositions differed between cloacal swabs and different gut regions, swabs qualitatively portrayed bacterial community compositions in the entire digestive tract, aligning with a previous study of wild birds [32], as well as reflected gut community compositions from a previous study of wild P. major fecal samples [16]. Microbial communities of alcohol-preserved gut regions did not differ significantly from fresh samples, supporting that museum collections represent a promising resource for analyses of gut microbiomes [37].…”

“…Most bird microbiome studies have utilized feces [e.g., 11,13,14,[16][17][18][19][20] or cloacal swabs [e.g., [21][22][23][24][25][26][27][28][29], but a handful of studies have demonstrated that bacterial communities are compartmentalized across different digestive tract regions [2,5,30,31]. This questions whether non-invasive methods only capture fecal and cloacal bacterial communities.…”

Flexibility and resilience of Great tit (Parus major) gut microbiomes to changing diets

“…Previous studies on wild birds have demonstrated low bacterial diversity and community composition differences in the midgut region (stomach and small intestine) compared to the crop microbiota. This suggests that the highly-acidic conditions in the midgut region acts as a barrier for environmental and foodborne bacteria [14,66,76,77]. This is further evident when we look at previously published mealworm gut microbiomes [78], where only a small fraction of the microbiome consists of bacterial genera that we identi ed in the gut microbiomes of mealworm-fed P. major.…”

Fecal microbiota associated with phytohaemagglutinin‐induced immune response in nestlings of a passerine bird

“…On the other hand, S. saprophyticus is opportunistic pathogen causing inflammatory diseases of urinary tract in humans (Hovelius & Mårdh, ) and Dysgonomonas can cause gut inflammation in immunocompromised human subjects (Bangsborg, Frederiksen, & Bruun, ). Both these OTUs were previously detected in bird GM (Kropáčková, Pechmanová, et al., ; Kropáčková, Těšický, et al., ; Xenoulis et al., ). However, their effect on physiology and health of avian are still unknown.…”

“…However, Enterococcus genus includes also several pathogenic strains, whose infection can directly affect host's immunity (Fisher & Phillips, 2009 (Hovelius & Mårdh, 1984) and Dysgonomonas can cause gut inflammation in immunocompromised human subjects (Bangsborg, Frederiksen, & Bruun, 1990). Both these OTUs were previously detected in bird GM (Kropáčková, Pechmanová, et al, 2017;Kropáčková, Těšický, et al, 2017;Xenoulis et al, 2010). We propose that these seemingly contrasting results are related to both interaction complexity between bacteria and the verte-…”