Microbiome lodgers help protect tadpoles from climate change

Abstract

Most creatures are essentially mobile cities, inhabited by hundreds of species of friendly gut bacteria and microorganisms, which contribute to each animal's digestion and wellbeing. ‘Housing microbes in the gut can help animals perform better, like growing faster and reproducing more’, says Samantha Fontaine from the University of Pittsburgh, USA. In return for sanctuary, these internal microbial communities – known as gut microbiomes – also appear to provide protection for coldblooded (ectothermic) hosts from the damaging effects of high temperatures, which these species are experiencing increasingly as the planet warms. Having previously discovered that green frog (Lithobates clamitans) tadpoles struggle more with warmth when their gut microbiome is less diverse, Fontaine and Kevin Kohl (University of Pittsburgh) wanted to find out how the reduction in their microbial lodgers impacts the tadpoles’ ability to weather warm conditions.After collecting pairs of adult green frogs from the University of Pittsburgh's field station, Fontaine and Kohl returned to the lab where they induced a pair of adults to mate, before transferring the freshly laid frogspawn into sterile pondwater to develop into tadpoles. ‘Keeping the eggs in a sterilized environment allows us to better control the microbial environment the tadpoles are exposed to, so we can attribute any changes we see in their physiology later in life to the different water conditions’, says Fontaine. Then she transferred half of the tadpoles into an unsterilized pondwater mixture – teaming with microbial life – where the young amphibians could develop a strong gut microbiome, while their siblings remained unexposed to microbes in sterilised pondwater – developing a depleted microbiome – before allowing the animals to grow at a comfortable 22°C until 9 weeks old. Fontaine then tested their resilience to a heatwave by transferring tadpoles from both groups to warm water (32°C) for 1 day, before collecting the youngsters’ intestines, to find out which genes the two groups of tadpoles had activated during the warm spell, in addition to finding out how their gut microbiomes responded to the blast of warmth.Initially, when the duo compared gene expression patterns between the gut tissue of tadpoles carrying a more complex, natural, microbiome and those with a depleted microbiome before the heatwave, there was little difference between the two. The duo concluded that carrying any microbiome is better for the tadpoles’ general wellbeing than none at all. In addition, the heatwave impacted the gut tissue gene expression patterns of all of the tadpoles. However, the tadpoles with the depleted microbiome reacted most strongly, with the largest gene expression changes to the hot day. Instead of being protective, these massive increases in gut tissue gene expression appear to be detrimental to the youngsters’ health, possibly because the tadpoles with the depleted microbiome were under more stress.Moving on to compare the gene pools of the microbiomes, it was clear that at higher temperatures the tadpoles that were colonised with a diverse microbiome had a head start over those with a depleted microbiome; the more natural microbiome altered the prevalence of genes involved in amino acid and protein production, carbohydrate digestion and energy production, which seemed to provide their tadpole hosts with some protection from the heat. In contrast, the depleted microbiome of tadpoles from sterile pondwater didn't respond at all to the increased temperature, leaving the tadpole hosts poorly prepared as the mercury soared. The more diverse, natural microbiome was protecting the tadpoles from the damaging heatwave.In short, a tadpole's ability to withstand the heat is probably the sum of the tadpole and its microbial lodgers’ protective contributions, and Fontaine says, ‘As global temperatures continue to rise, it will be important to incorporate host–microbe interactions into our understanding of host responses to climate change’.