Environmental temperature alters the digestive performance and gut microbiota of a terrestrial amphibian

Abstract

Environmental temperature and gut microbial communities can both have profound impacts on the digestive performance of ectothermic vertebrates. Additionally, the diversity, composition and function of gut microbial communities themselves are influenced by temperature. It is typically assumed that the temperature-dependent nature of ectotherm digestive performance is due to factors such as host physiological changes and adaptation to local climatic conditions. However, it is also possible that temperature-induced alterations to gut microbiota may influence the relationship between temperature and digestion. To explore the connections between these three factors, we compared digestive performance and gut microbial community diversity and composition in red-backed salamanders housed at three experimental temperatures: 10, 15 and 20°C. We also investigated associations between specific bacterial taxa and temperature or salamander digestive performance. We found that salamander digestive performance was greatest at 15°C, while gut microbial diversity was reduced at 20°C. Further, gut microbial community composition differed among the three temperature treatments. The relative abundance of 25 bacterial genera was dependent on temperature, with high temperatures being associated with reductions in the relative abundance of disease-resistant bacteria and increases in pathogenic taxa. The relative abundance of four bacterial genera was correlated with salamander energy assimilation, two of which are known to digest chitin, a main component of the red-backed salamander diet. These findings suggest that gut microbiota may mediate the relationship between temperature and digestion in ectotherms. We discuss how global climate change may impact ectotherms by altering host-microbe interactions.

The Effects of Temperature on Animal Gut Microbiomes

“…A similar effect has also been observed in tadpoles (Lithobates pipiens), which displayed decreases in relative abundances of Firmicutes at 28 • C relative to at 18 • C (Kohl and Yahn, 2016). The gut microbiotas of Salamanders (Plethodon cinereus) were also found to display progressive decreases in the relative abundances of genera within the Firmicutes (e.g., Anaerotrucus) at 10, 15, and 20 • C (Fontaine et al, 2018). In addition, laying hens exposed to heat stress have been shown to exhibit significant decreases in the relative abundance of Firmicutes within the fecal microbiota (Zhu et al, 2019).…”

“…In mammals, Firmicutes and Bacteroidetes dominate, whereas Proteobacteria comprise a larger fraction of the gut microbiota in many birds, reptiles, and fish. Recent studies have assayed the gut microbiota of labreared or enclosure-reared vertebrates at different temperatures (Tajima et al, 2007;Chevalier et al, 2015;Kohl and Yahn, 2016;Bestion et al, 2017;Fontaine et al, 2018;Zhu et al, 2019). Despite the differences in composition among the gut microbiotas of vertebrate lineages, several general trends in responses of the gut microbiota to temperature variation have been observed across host species.…”

Bighorn sheep gut microbiomes associate with genetic and spatial structure across a metapopulation

“…Host diet is a primary environmental driver of microbiome variation in controlled laboratory studies 13,14 and humans 3 , and several studies in wild mammals have also demonstrated microbiome variation across spatial and seasonal ranges of nutritional variation. Other environmental factors that may interact with diet to influence the microbiome include altitude 20,21 and climate 22 . Host factors, such as genetic variation, have been shown to play a role in filtering particular microbes from the environment, thereby influencing the composition and relative abundances of resident microbial communities 23,24 .…”

Interaction of behavior and physiology of anurans in response to thermal and hydric stress: an approach to understand the vulnerability of anurans to climate change

“…Staying in the PBT range optimizes multiple physiological functions (e.g. locomotion, digestion, development, reproduction) (Licht, 1965;Stevenson et al, 1985;Hertz et al, 1993;Navas and Bevier, 2001;Angilletta et al, 2002;Tracy et al, 2010;Berger et al, 2011;Fontaine et al, 2018). Heath's model also argues that when the environmental temperatures increase and the Tb of these organisms exceed their PBT range, they may present another type of behavioral response called "all-or-none".…”

“…The PBT optimizes multiple physiological functions (Licht, 1965;Heath, 1970;Stevenson, 1985;Hertz et al, 1993;Angilletta et al, 2002;Tracy et al, 2010), including locomotor performance (Bennet, 1990;Navas et al, 1999;Stevenson et al, 1985;Deere and Chown, 2006), feeding rates and digestive efficiency (Kingslover and Woods, 1997;Wang et al, 2002;McConnachie and Alexander, 2004;Fontaine et al, 2018), rates of development and growth (Berger et al, 2011) and reproduction (Navas and Bevier, 2001;Symes et al, 2017). However, when environmental conditions force the animal to an increase in Tb exceeding its PBT range, individuals may need to quickly retract from a thermally stressful situation to avoid prompt mortality.…”