Manipulation of gut microbiota during critical developmental windows affect host physiological performance and disease susceptibility across ontogeny

Colonisation of gut microbiomes during early life can shape metabolism and immunity of adult animals. However, most data are derived from antibiotic‐treated or germ‐free laboratory mammals. Furthermore, few studies have explored how microbial colonization during critical windows influences a suite of other fitness‐related traits in wild animals. A recent study in the Journal of Animal Ecologytested whether hatching constitutes a critical development window for microbiome colonisation in wild-caught amphibians. Here, authors Robin Warne, Lucas Kirschman, and Lydia Zeglin present a summary of this work.

Our new study published in the Journal of Animal Ecology reveals the astounding and persistent effects that symbiotic gut bacteria can have on the development, growth, and health of their animal hosts. We found the bacterial community on the outside of eggs influences the microbiota that colonizes the guts of tadpoles as they hatch, and that differences in the bacteria during this initial colonization can have both positive and detrimental effects on the health of tadpoles as they grow into frogs.

Fig1

Wood frog tadpoles inoculated with differing bacterial communities at hatching exhibited differences in their gut microbiome that were associated with changes in development, growth, and metabolism. Changes in their gut microbiomes were also associated with differences in susceptibility to ranavirus (an emerging disease of amphibians) as well as variation in tail deformities. Tadpoles that were inoculated with random bacteria from the environment had more tail deformities (B) and were more susceptible to infection by ranavirus than tadpoles from other inoculation treatments.

In this experiment, we stripped the bacterial community on the eggs of wood frogs, and then inoculated them with microbes from differing sources, including from another species that differ in disease resistance and life history. We found tadpoles that received bacteria from the other species were more robust than controls, whereby they developed and grew faster, and trended towards being more resistant to a virus (ranavirus) that can be lethal to some amphibian tadpoles, especially wood frogs. By contrast, we found another group of tadpoles that were inoculated at hatching with random bacteria from the environment, were much less healthy. These tadpoles showed disrupted metabolic rates, high rates of tail deformities, and were more susceptible to the virus, which infects through the gut. These results suggest that variation in the types of symbiotic gut bacteria present at hatching influence the long-term health of their hosts.

The next step in our research is to explore the mechanisms by which gut bacteria influence their hosts. We think a likely way gut bacteria affect their hosts is via the metabolites or metabolic biproducts they produce, such as short chain fatty acids, essential nutrients like vitamins, and even hormone like compounds. These metabolites serve as energy substrates, essential nutrients, and potentially as signaling molecules that may directly influence their hosts through interfacing with hormone receptors in host tissues including the brain.

This experiment provides a great foundation for future experiments that explore these potential mechanisms, and these experiments could prove amphibians can be a valuable animal model for understanding microbiome effects on the health of hosts including in humans. This is because like our results in tadpoles, the mode of birth in humans (caesarian vs natural birth) can permanently shape the gut microbiome of adults, and have life-long effects on human health through affecting metabolic diseases and obesity.

This research could also inform conservation efforts of amphibians impacted by emerging diseases such as ranavirus and chytrid fungus, because researchers are exploring using bacterial inoculations and metabolites as a means to bioaugment amphibian resistance to such pathogens.

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