Temperature-Dependent Effects of Cutaneous Bacteria on a Frog's Tolerance of Fungal Infection.

Matthew J Robak,Corinne L Richards-Zawacki

doi:10.3389/fmicb.2018.00410

Matthew J Robak, Corinne L Richards-Zawacki

Open Access

https://doi.org/10.3389/fmicb.2018.00410

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Abstract

Defense against pathogens is one of many benefits that bacteria provide to animal hosts. A clearer understanding of how changes in the environment affect the interactions between animals and their microbial benefactors is needed in order to predict the impact and dynamics of emerging animal diseases. Due to its dramatic effects on the physiology of animals and their pathogens, temperature may be a key variable modulating the level of protection that beneficial bacteria provide to their animal hosts. Here we investigate how temperature and the makeup of the skin microbial community affect the susceptibility of amphibian hosts to infection by Batrachochytrium dendrobatidis (Bd), one of two fungal pathogens known to cause the disease chytridiomycosis. To do this, we manipulated the skin bacterial communities of susceptible hosts, northern cricket frogs (Acris crepitans), prior to exposing these animals to Bd under two different ecologically relevant temperatures. Our manipulations included one treatment where antibiotics were used to reduce the skin bacterial community, one where the bacterial community was augmented with the antifungal bacterium, Stenotrophomonas maltophilia, and one in which the frog’s skin bacterial community was left intact. We predicted that frogs with reduced skin bacterial communities would be more susceptible (i.e., less resistant to and/or tolerant of Bd infection), and frogs with skin bacterial communities augmented with the known antifungal bacterium would be less susceptible to Bd infection and chytridiomycosis. However, we also predicted that this interaction would be temperature dependent. We found a strong effect of temperature but not of skin microbial treatment on the probability and intensity of infection in Bd-exposed frogs. Whether temperature affected survival; however, it differed among our skin microbial treatment groups, with animals having more S. maltophilia on their skin surviving longer at 14 but not at 26°C. Our results suggest that temperature was the predominant factor influencing Bd’s ability to colonize the host (i.e., resistance) but that the composition of the cutaneous bacterial community was important in modulating the host’s ability to survive (i.e., tolerate) a heavy Bd infection.

Highlights

That there exist mutualistic and even symbiotic relationships between animals and microbes has long been understood, yet it is only recently that we have come to appreciate how common and influential these relationships can be for ecological processes that play out across taxa and environments
We used a third generalized linear mixed models (GLMMs) to test whether temperature, bacterial treatment, or their interaction affected the probability that Batrachochytrium dendrobatidis (Bd)-exposed frogs became infected
This model used a binary logistic distribution and Stenotrophomonas maltophilia was detected on all frogs from all three bacterial manipulation groups and both temperatures throughout the experiment, with the exception of two frogs at 26◦C that each tested negative in one weekly sample: one frog from the “S. maltophilia added” group tested negative on day 41 and one from the “intact” bacteria group tested negative on day 55 (Supplementary Figures S2A,B)

Summary

Introduction

That there exist mutualistic and even symbiotic relationships between animals and microbes has long been understood, yet it is only recently that we have come to appreciate how common and influential these relationships can be for ecological processes that play out across taxa and environments (reviewed in McFallNgai et al, 2013). Temperature may be a key player in determining the health benefits that symbiotic microbes bestow upon their animal hosts, especially for ectotherms (Kohl and Yahn, 2016; Ferguson, 2017), though clear empirical examples appear to be limited to handful of invertebrates (Tianero et al, 2015; Ferguson, 2017) Amphibians are another taxon useful for investigating the effects of temperature on microbial symbioses, as several aspects of the amphibian immune system are known to function in a temperature-dependent manner (Maniero and Carey, 1997; Rollins-Smith and Woodhams, 2012) and the cutaneous bacteria of amphibians are known to be important to their defense against other skin microbes, including pathogenic fungi in the genus Batrachochytrium (Harris et al, 2009a)

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