Microbiome mediation of animal life histories via metabolites and insulin‐like signalling

Abstract

The regulatory pathways by which gut microbiota potentially shape host life histories remain largely untested, however, a constellation of research suggests that gut bacteria likely have significant effects on their hosts via metabolites. In this article we review known and hypothesized pathways by which gut microbiota influence host life histories through interfacing with the neuroendocrine system, with a focus on the insulin‐like growth factor (IGF) signalling pathway. Bacterially derived metabolites including short‐chain fatty acids (SCFAs), polyamines, and peptides likely impact host life histories as metabolic substrates, essential nutrients, and via molecular signalling with well‐studied neuroendocrine pathways. The hypothalamus–pituitary axis and insulin‐like signalling (ILS) pathways are central regulatory networks for development, growth, reproductive maturity, reproduction, and senescence and are likely targets for tests of how gut bacterial metabolites shape host life histories. SCFAs in particular, as metabolites derived from bacterial fermentation, are implicated as significant microbiome signalling molecules shown to interface with the ILS pathway as well as to bind to receptors on neuroendocrine and peripheral nervous tissues. For example, experimental increases of SCFA production have been shown to affect IGF‐1 levels in circulation and are associated with robust development, growth, reproduction, and delayed senescence. Finally, emerging ‐omics approaches are providing integrative ways to test and detail the potential diverse ways in which gut microbiota interact with their hosts and the likely important roles they play in shaping host life‐history responses to varied environmental conditions.

Heat Tolerance is Affected by the Gut Microbiota in a Vertebrate Ectotherm

“…Compared to GF larvae, NI larvae had a lower, although not statistically significant, relative abundance of Firmicutes and Bacteroidota, two phyla associated with SCFA-production (den Besten et al, 2013;Warne and Dallas, 2022). This could account for our observed CT max pattern.…”

“…One potential mechanism through which M. hirudinis could promote heat tolerance is through upregulation of antioxidants as a byproduct of acetate production (Gonzalez-Bosch et al, 2021;Warne and Dallas, 2022). Heat stress is associated with an increased production of reactive oxygen species (ROS) in vertebrates that induce oxidative damage which negatively affect cellular function, host survival, and can limit host CT max (reviewed in Ritchie and Friesen, 2022).…”

“…The host microbiota represents a complex biological community consisting of bacteria, fungi, and viruses that has received increased focus over recent decades as its highly influential role on host physiology has become elucidated (Kohl and Carey, 2016; McFall-Ngai et al, 2013; Warne and Dallas, 2022). Resultantly, how the host microbiota responds to changes in environmental variables that are intimately tied to organismal biology, such as temperature, are of great interest.…”

Diet- and salinity-induced modifications of the gut microbiota are associated with differential physiological responses to ranavirus infection in Rana sylvatica

“…in particular, which are generally considered to be very effective at extracting energy from foods [68]. Firmicutes are thought to mediate resource allocation of hosts by increasing the production of insulin-like growth factor in the liver via increased short-chain fatty acid mobilization, which promotes growth and fat deposition in diverse animals [15,20]. Consistent with these effects of greater Firmicutes abundance, we show increased growth and fat storage with algal supplementation in wood frog larvae.…”

“…Extensive cross-talk between the gut microbiota and host occurs through metabolite secretion and signalling [8,9], forming a relationship that primes the immune system early on and lasts throughout an organism's life [10][11][12][13]. Bacterially produced short-chain fatty acids are integral to this communication, and their influence extends from the gut to the neuroendocrine and immune systems, where they help modulate diverse host processes such as nutrient uptake, fat storage, mucus production and inflammatory responses [14][15][16]. Host-associated microbial communities, therefore, have the potential to affect © 2023 The Author(s) Published by the Royal Society.…”