In sickness and in health: the dynamics of the fruit bat gut microbiota under a bacterial antigen challenge and its association with the immune response

Abstract

IntroductionInteractions between the gut microbiome (GM) and the immune system influence host health and fitness. However, few studies have investigated this link and GM dynamics during disease in wild species. Bats (Mammalia: Chiroptera) have an exceptional ability to cope with intracellular pathogens and a unique GM adapted to powered flight. Yet, the contribution of the GM to bat health, especially immunity, or how it is affected by disease, remains unknown.MethodsHere, we examined the dynamics of the Egyptian fruit bats’ (Rousettus aegyptiacus) GM during health and disease. We provoked an inflammatory response in bats using lipopolysaccharides (LPS), an endotoxin of Gram-negative bacteria. We then measured the inflammatory marker haptoglobin, a major acute phase protein in bats, and analyzed the GM (anal swabs) of control and challenged bats using high-throughput 16S rRNA sequencing, before the challenge, 24h and 48h post challenge.ResultsWe revealed that the antigen challenge causes a shift in the composition of the bat GM (e.g., Weissella, Escherichia, Streptococcus). This shift was significantly correlated with haptoglobin concentration, but more strongly with sampling time. Eleven bacterial sequences were correlated with haptoglobin concentration and nine were found to be potential predictors of the strength of the immune response, and implicit of infection severity, notably Weissella and Escherichia. The bat GM showed high resilience, regaining the colony’s group GM composition rapidly, as bats resumed foraging and social activities.ConclusionOur results demonstrate a tight link between bat immune response and changes in their GM, and emphasize the importance of integrating microbial ecology in ecoimmunological studies of wild species. The resilience of the GM may provide this species with an adaptive advantage to cope with infections and maintain colony health.

Different species of Chiroptera: Immune cells and molecules

“…In 2022 and 2023 Anne 65 and Tali et al 66 found that haptoglobin levels increased in Myotis myotis after stimulation by LPS, suggesting that haptoglobin is a major protein in bats during the acute inflammatory response period; Myotis myotis showed different haptoglobin hydroprotein levels in response to different stimuli, with haptoglobin levels decreasing after fungal infections and enzyme glycan attack resulting in a decrease of neutrophilic granulocytes were reduced; haptoglobin concentrations were also increased in LPS‐stimulated Rousettus aegyptiacus , possibly related to its own bacterial attack producing changes in gut microbial composition.…”

Advances in understanding bat infection dynamics across biological scales

“…Experimental studies have shown that GIT microbiota transplanted from great roundleaf bats ( Hipposideros armiger ) into antibiotic-treated mice altered immune cell levels and conferred greater resistance and survival to H1N1 influenza infection compared with control groups, indicating the GIT microbiome can interact with and change the host immune system [ 63 ]. Additionally, lipopolysaccharide injections in R. aegyptiacus induced significant and rapid (24–48 h) changes to the composition and diversity of gut microbial communities [ 64 ].…”