Does the frog microbiome recover from disease-induced disturbance?

Effects of an infectious disease on the microbiome can outlast the infection itself. Clearing frogs of infection did not lead to recovery of the microbiome.

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From disease outbreaks to earthquakes, fires, and storms, disturbances are prominent  features of ecological systems. Some types of disturbance may be increasing in frequency due to human activities. Understanding if and how biological systems recover or “bounce back” from disturbances is critical for predicting and managing their effects.

Disturbances occur at all spatial scales. For the microbes that live in or on animals, the animal host represents the ecosystem, and events such as host illness represent disturbances. As such, pathogen infection can lead to changes in the microbiome. However, we know little about microbiome resilience to disease: Can a microbiome recover after the host clears the infection, and how long does recovery take?

A yellow-legged frog basks at the side of a lake. Photo credit: Andrea Jani

The mountain yellow-legged frog, Rana muscosa, is threatened with extinction, and one of its greatest threats is a fungal pathogen called Batrachochytrium dendrobatidis (Bd for short)1,2. Bd infects the skin of amphibians and causes the potentially lethal disease chytridiomycosis. Bd also interacts with the skin microbiome. Under certain conditions, bacteria isolated from amphibian skin can prevent or slow down Bd growth3–5. Disease-resistant and -susceptible frog populations harbor different microbial communities6. On the flip side, Bd infection disturbs the microbiome and leads to changes in the relative abundances of various types of bacteria7. We set out to test if the skin microbiome can recover its initial state after it has been disturbed by Bd.

A frog that died during an outbreak of Bd in the wild. Photo credit: Andrea Jani

We infected mountain yellow-legged frogs with Bd, then cleared their infections by treating them with anti-fungal drugs. We tracked the microbiome to measure the effect of Bd. We then tested if clearing the frogs of infection allowed the microbiome to return to its original (pre-infection) state (i.e., to recover). As expected, Bd infection altered microbiome composition (i.e., the abundances of different types of bacteria in the microbiome). Treating the frogs with anti-fungal drugs cleared their Bd infections. However, the frogs’ microbiomes did not return to their original state. In other words, resilience was low. (Resilience is a rate of recovery, analogous to the speed at which a rubber band snaps back after being stretched.)

An important unanswered question is whether the microbiome disturbance we observed is detrimental to the frog. Changes in the composition of a microbiome do not always affect functional capacity. In some cases, functional redundancy among bacterial “species” provides some insurance against functional loss. In addition, changes in response to disturbance might even be adaptive, selecting for a more resilient microbiome. Hopefully, future research will shed light on the effects of disturbance and resilience on microbiome function.   

 Scientists and wildlife managers are working furiously to find ways to save the mountain yellow-legged frog from extinction. In fact, the experimental infections in our study did double duty, contributing to an effort to boost immune responses to Bd by infecting and then clearing the frogs. By studying how this affected the microbiome, we hope to improve tools for conserving these frogs and other amphibians threatened by this fungal disease.

Read the full article here: https://doi.org/10.1038/s41396-020-00875-w

 BIBLIOGRAPHY

  1. Rachowicz, L. J. et al. Emerging infectious disease as a proximate cause of amphibian mass mortality. Ecology 87, 1671–1683 (2006).
  2. Vredenburg, V. T., Knapp, R. A., Tunstall, T. S. & Briggs, C. J. Dynamics of an emerging disease drive large-scale amphibian population extinctions. PNAS 107, 9689–9694 (2010).
  3. Harris, R. N. et al. Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. The ISME Journal 3, 818–824 (2009).
  4. Woodhams, D. C. et al. Treatment of amphibians infected with chytrid fungus: learning from failed trials with itraconazole, antimicrobial peptides, bacteria, and heat therapy. Dis Aquat Organ 98, 11–25 (2012).
  5. Piovia-Scott, J. et al. Greater Species Richness of Bacterial Skin Symbionts Better Suppresses the Amphibian Fungal Pathogen Batrachochytrium Dendrobatidis. Microbial Ecology 74, 217–226 (2017).
  6. Jani, A. J., Knapp, R. A. & Briggs, C. J. Epidemic and endemic pathogen dynamics correspond to distinct host population microbiomes at a landscape scale. Proceedings of the Royal Society B-Biological Sciences 284, 20170944 (2017).
  7. Jani, A. J. & Briggs, C. J. The pathogen Batrachochytrium dendrobatidis disturbs the frog skin microbiome during a natural epidemic and experimental infection. PNAS 111, E5049–E5058 (2014).

 

Andrea Jani

Assistant Researcher, University of Hawaii at Manoa

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