Gut microbiota of invasive bullfrog tadpoles responds more rapidly to temperature than a noninvasive congener

Abstract

Environmental temperature can alter the composition, diversity, and function of ectothermic vertebrate gut microbial communities, which may result in negative consequences for host physiology, or conversely, increase phenotypic plasticity and persistence in harsh conditions. The magnitude of either of these effects will depend on the length of time animals are exposed to extreme temperatures, and how quickly the composition and function of the gut microbiota can respond to temperature change. However, the temporal effects of temperature on gut microbiota are currently unknown. Here, we investigated the length of time required for increased temperature to alter the composition of gut bacterial communities in tadpoles of two frog species, the green frog, Lithobates clamitans, and its congener, the globally invasive American bullfrog, L. catesbeianus. We also explored the potential functional consequences of these changes by comparing predicted metagenomic profiles across temperature treatments at the last experimental time point. Bullfrog‐associated microbial communities were more plastic than those of the green frog. Specifically, bullfrog communities were altered by increased temperature within hours, while green frog communities took multiple days to exhibit significant changes. Further, over ten times more bullfrog bacterial functional pathways were temperature‐dependent compared to the green frog. These results support our hypothesis that bullfrog gut microbial communities would respond more rapidly to temperature change, potentially bolstering their ability to exploit novel environments. More broadly, we have revealed that even short‐term increases in environmental temperature, expected to occur frequently under global climate change, can alter the gut microbiota of ectothermic vertebrates.

The gut bacteria of an invasive amphibian respond to the dual challenges of range-expansion and parasite attack

“…Environmental temperature can alter microbial taxonomic community and predicted microbial function, resulting in increased phenotypic plasticity and persistence in harsh conditions (Fontaine & Kohl, 2020b). For example, gut microbiota of invasion bullfrog tadpoles responds more rapidly to environmental temperature than noninvasion green frogs (Fontaine & Kohl, 2020b). Environmental temperature alters the digestive performance and gut microbiota of red-backed salamanders ( Plethodon cinereus : Fontaine, Novarro, & Kohl, 2018) and in a study of western clawed frogs ( Xenopus tropicalis ) the authors observed a higher prevalence of Verrucomicrobia in the gut of frogs inhabiting a warmer environment, and an opposite pattern in Proteobacteria (J.…”

“…It is interesting that even though environmental isothermality and lungworm infection intensity are not significantly different between range-core and invasion-front toads, environmental isothermality and occurrence of lungworms are significantly associated with the microbial taxonomic community and predicted microbial function. Environmental temperature can alter microbial taxonomic community and predicted microbial function, resulting in increased phenotypic plasticity and persistence in harsh conditions (Fontaine & Kohl, 2020b). For example, gut microbiota of invasion bullfrog tadpoles responds more rapidly to environmental temperature than noninvasion green frogs (Fontaine & Kohl, 2020b).…”

“…Environmental temperature can alter microbial taxonomic community and predicted microbial function, resulting in increased phenotypic plasticity and persistence in harsh conditions (Fontaine & Kohl, 2020b). For example, gut microbiota of invasion bullfrog tadpoles responds more rapidly to environmental temperature than noninvasion green frogs (Fontaine & Kohl, 2020b).…”

“…The invasive species has much higher abundance of the order Bacteroidales , with the genera Bacillariophyta and Clostridium being significantly more abundant in native than invasive fish (Ye, Amberg, Chapman, Gaikowski, & Liu, 2014). It is not clear how the observed differences in gut bacteria contribute to invasiveness, especially the comparison of gut microbiota regarding host invasiveness has only been conducted in two different species (Fontaine & Kohl, 2020a; Qu et al, 2020). Research on gut microbiota variation between populations with different invasion characters in the same species would help to elucidate such patterns.…”

Holo-Omics: Integrated Host-Microbiota Multi-omics for Basic and Applied Biological Research

“…One potential application is to measure the impact of microorganisms in vertebrate adaptation and improve predictions from anthropogenic disturbances, such as climate change and habitat destruction, on species distributions. It has been proposed that metagenomes could confer enhanced adaptive capacity to their hosts ( Alberdi et al., 2016 ), potentially enabling rapid adaptation to changing environmental conditions ( Fontaine and Kohl, 2020 ). The adaptive capacity of hosts and their associated microbiota through linking specific host genotypes with metagenomes has been demonstrated with regard to toxicity resilience ( Macke et al., 2017 ), heat tolerance ( Moran and Yun, 2015 ), drought and desiccation ( Cernava et al., 2019 ), disease resistance ( Rosshart et al., 2017 ), and nutrient acquisition ( Falcinelli et al., 2015 ).…”