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

Abstract

Background Gut microbial communities play important roles in nutrient management and can change in response to host diets. The extent of this flexibility and the concomitant resilience is largely unknown in wild animals. To untangle the dynamics of avian-gut microbiome symbiosis associated with diet changes, we exposed Parus major (Great tits) fed with a standard diet (seeds and mealworms) to either a mixed (seeds, mealworms and fruits), a seed, or a mealworm diet for 4 weeks, and examined the flexibility of gut microbiomes to these compositionally different diets. To assess microbiome resilience (recovery potential), all individuals were subsequently reversed to a standard diet for another 4 weeks. Cloacal microbiomes were collected weekly and characterised through sequencing the v4 region of the 16S rRNA gene using Illumina MiSeq. Results Initial microbiomes changed significantly with the diet manipulation, but the communities did not differ significantly between the three diet groups (mixed, seed and mealworm), despite multiple diet-specific changes in certain bacterial genera. Reverting birds to the standard diet led only to a partial recovery in gut community compositions. The majority of the bacterial taxa that increased significantly during diet manipulation decreased in relative abundance after reversion to the standard diet; however, bacterial taxa that decreased during the manipulation rarely increased after diet reversal Conclusions The gut microbial response and partial resilience to dietary changes support that gut bacterial communities of P. major play a role in accommodating dietary changes experienced by wild avian hosts. This may be a contributing factor to the relaxed association between microbiome composition and the bird phylogeny. Our findings further imply that interpretations of wild bird gut microbiome analyses from single-time point sampling, especially for omnivorous species or species with seasonally changing diets, should be done with caution. The partial community recovery implies that ecologically relevant diet changes (e.g., seasonality and migration) open up gut niches that may be filled by previously abundant microbes or replaced by different symbiont lineages, which has important implications for the integrity and specificity of long-term avian-symbiont associations.

Covariation of the Fecal Microbiome with Diet in Nonpasserine Birds

“…We found that Clostridium was significantly enriched in the foliage food group (Wilcoxon rank sum test, P , 0.05), followed by the fruit and omnivore food groups (Fig. 2C), which is consistent with the results observed in passerine birds that have plant-based diets (33). A similar CAZyme profile appeared in these 3 groups (foliage, fruit, and omnivore), whose diets contain high levels of plant cellulose (Fig.…”

Species-specific but not phylosymbiotic gut microbiomes of New Guinean passerine birds are shaped by diet and flight-associated gut modifications

“…R. Soc. B 288: 20210446 as microbiomes (when bacterial phylogeny is not considered) are secondarily influenced by host diet, which is consistent with previously documented flexible responses in gut communities to diet changes [17,19,22,26]. Individual dietary intake of wild New Guinean birds varies greatly within a species [32], suggesting broader dietary niches than often assumed (e.g.…”

“…These modifications could potentially affect the stability of avian gut microbial communities [10], because shorter gut retention leads to more fluctuating gut environments and potentially higher microbial turnover. Bird microbiomes are also highly variable between individuals of the same bird species [19][20][21] and tend to be malleable to dietary and environmental changes [19,[21][22][23][24][25][26]. Consequently, diet tends to affect gut microbiomes more than host phylogeny [17].…”

Gut microbiome composition, not alpha diversity, is associated with survival in a natural vertebrate population

“…Members of the order Clostridiales are abundant in the GM of many vertebrate taxa, including other insectivorous passerine species [97,98] and have previously been linked to an increase in immunological resistance to nest parasites in eastern bluebirds (Sialia sialis) [99]. A study on captive, juvenile ostriches (Struthio camelus), also showed that the abundance of ASVs in this order was reduced in the hindgut of diseased individuals that subsequently died, suggesting that they may be linked to host health and survival [10].…”

“…A study on captive, juvenile ostriches (Struthio camelus), also showed that the abundance of ASVs in this order was reduced in the hindgut of diseased individuals that subsequently died, suggesting that they may be linked to host health and survival [10]. Species in the order Clostridiales play a role in carbohydrate and protein fermentation (for example during the digestion of insect prey) as well as the degradation of toxic by-products from this process [97,100]. The short-chain fatty acids produced from fermentation can be directly absorbed across the intestinal wall and used as an energy source by the host [94].…”