The Effects of Temperature on Animal Gut Microbiomes

Abstract

Temperature is a prominent abiotic environmental variable that drives the adaptive trajectories of animal lineages and structures the composition of animal communities. Global temperature regimes are expected to undergo rapid shifts in the next century, yet for many animal taxa we lack an understanding of the consequences of these predicted shifts for animal populations. In this review, we synthesize recent evidence that temperature variation shapes the composition and function of animal gut microbiomes, key regulators of host physiology, with potential consequences for host population responses to climate change. Several recent studies spanning a range of animal taxa, including Chordata, Arthropoda, and Mollusca, have reported repeatable associations between temperature and the community composition and function of the gut microbiome. In several cases, the same microbiome responses to temperature have been observed across distantly related animal taxa, suggesting the existence of conserved mechanisms underlying temperature-induced microbiome plasticity. Extreme temperatures can disrupt the stability of alpha-diversity within the gut microbiomes individual hosts and generate beta-diversity among microbiomes within host populations. Microbiome states resulting from extreme temperatures have been associated, and in some cases causally linked, with both beneficial and deleterious effects on host phenotypes. We propose routes by which temperature-induced changes in the gut microbiome may impact host fitness, including effects on colonization resistance in the gut, on host energy and nutrient assimilation, and on host life history traits. Cumulatively, available data indicate that disruption of the gut microbiome may be a mechanism by which changing temperatures will impact animal fitness in wild-living populations.

Effects of Thermal Stress on the Gut Microbiome of Juvenile Milkfish (Chanos chanos)

“…While the importance of the gut microbiome for the welfare and performance of fish is now widely acknowledged [19,20] and has been extensively studied for potential applications in aquaculture [13,17], there is a substantial lack of information concerning tropical aquaculture species, such as milkfish, and the influence of thermal stress on the gut microbiome and its interactions with the host [21]. With continuous anthropogenic greenhouse gas emissions, predicted shifts in global temperature regimes include a rapid warming of tropical ocean waters [22,23].…”

Alteration of gut microbiota with a broad-spectrum antibiotic does not impair maternal care in the European earwig

“…Independent of rifampicin, our data also reveal that both α - and β -diversity changed from pre-oviposition to egg hatching. This stage-specific pattern may result from the absence of food intake for about four weeks before gut sampling in females at egg hatching compared to before oviposition [60], and/or from the different rearing temperatures [61] and differences in female age [62] between the two life stages. Notwithstanding the drivers of this stage-specific effect, it is important to note that all the tested females were re-treated with rifampicin (or water) after egg hatching so that the resulting alteration of their gut microbiota reported at oviposition likely operated during their entire lifetime and could thus have affected all the traits measured after egg-hatching.…”

Do seasonal microbiome changes affect infection susceptibility, contributing to seasonal disease outbreaks?

“…[37,59,60] These changes do not always make a great deal of difference, as various taxa are capable of playing the same role in the physiology of the host, [36,61] but in some cases they may modify the microbiome's proper functionality. [51,62] Among the factors influencing the structure of a microbiome are antibiotics, [60,63] diet, [27,32,59,64,65] temperature, [28,66,67,68] humidity, [69,70] and even the host's production of vitamin D. [71,72] In humans, for example, treatment with vancomycin causes depletion of most components of a gut microbiome, such as Bacteroidetes, and is associated with increases in species of Proteobacteria linked with infectious processes. [63] Another factorone of the most important -is diet.…”

“…Currently, more and more emerging research shows that changes in temperature may constitute an important modulator of gut microbiome. [67] For instance research shows that rearing mice in temperatures mimicking summer heat weakens virus-specific adaptive immunity, although this can be partially restored by glucose or short-chain fatty acid supplementation, suggesting a role for diet and the microbiome in heat-mediated immune impairment. [26,100] Similarly, there is some evidence suggesting that low temperatures can influence the immunity of a host; this may be mediated by the microbiome.…”

“…Very likely, different parts of microbiomes will also prove relevant to seasonal outbreaks in different species; for instance, skin microbiomes appear to play an important role in amphibian immunology, [43,44] whereas in mammals gut microbiomes appear more relevant. [92,93] Furthermore, even though diet seems to be the most important modulator of microbiome structure, [27,32,59,64,65] microbiomes can also be shaped by other factors, such as antibiotics, [60,63] temperature, [28,66,67,68] humidity, [69,70] and even the host's production of vitamin D. [71,72] This suggests that seasonal outbreaks to which microbiomes may contribute may be triggered by seasonal changes in different external factors. In other words, the question of whether microbiomes contribute to outbreaks and, if so, which parts of microbiomes and which external factors producing changes in microbiomes are relevant are details that depend on the species in question and must be empirically investigated.…”