A central goal of population and community ecology is to understand factors that lead to the emergence of infectious diseases in wildlife.  Our research has identified individual and population-level variation in susceptibility to a cutaneous fungal infection in three species of amphibians.  We are investigating the role of beneficial cutaneous bacteria in generating this variation and in protecting individuals from a lethal fungal pathogen.

    Amphibian skin is attacked by a fungal pathogen, Batrachochytrium dendrobatidis, which is a chytrid fungus.  This disease has caused widespread population declines and apparent extinctions in areas of the world, such as Australia and the Americas.  Our hypothesis is that study of the ecological context of emerging infectious diseases, such as chytridiomycosis, is crucial in understanding and eventually controlling the disease.  The ecological context is the interaction of the dispersing zoospore of B. dendrobatidis and the resident anti-chytrid microbiota on amphibian skin.

    Our research has shown that the skin of healthy amphibians (salamander Plethodon cinereus) is populated by resident bacteria and that a number of cutaneous bacterial species have anti-chytrid properties.  The dispersing zoospores of the pathogen will likely interact with the amphibian’s cutaneous bacterial microbiota and may be inhibited by it.  In the laboratory, our research has shown that “bio-augmentation” of beneficial bacteria followed by exposure to the chytrid pathogen can speed clearance time of the chytrid infection in P. cinereus.  From field data, a comparison was made of the skin  microbiota of populations of the frog Rana muscosa that are coexisting with the pathogen with those that decline once the pathogen arrives.  A significantly higher proportion of individuals in the persisting population had at least one species of anti-chytrid bacteria on the skin.

    We are testing the efficacy of the application of anti-chytrid bacteria to the skin of the threatened anuran species Rana muscosa that is negatively affected by B. dendrobatidis.  Our hypothesis is that application of bacteria will have a protective effect against the negative effects of B. dendrobatidis.  We are also studying:  (1)  the effects of stress on individual amphibian’s cutaneous microbiota and susceptibility to chytridiomycosis, (2) the role of horizontal and vertical transmission of skin bacteria on amphibians’ cutaneous microbiota, (3) the effect of microbial community composition on horizontal and vertical transmission and on amphibian disease susceptibility, (4) antibiotics produced by skin bacteria.  The potential discovery of antifungal molecules opens the door to a novel chemotherapeutic that could be applicable not only to amphibian conservation but to human medicine.

At JMU, I collaborate with Dr. Kevin Minbiole, who is in the Department of Chemistry and Biochemistry.  Work in his laboratory has shown that antifungal metabolites found on amphibian skins and produced by amphibians’ skin microbes are often in high enough concentration to inhibit fungal zoospores.

I am collaborating with Dr. Lisa Belden at Virginia Tech on the role of beneficial microbes in preventing disease.

Our research is currently funded by the National Science Foundation and supported by the USDA Forest Service.

References

Lam*, B. A., J. B. Walke, V. T. Vredenburg, R. N. Harris. Proportion of individuals with anti-Batrachochytrium dendrobatidis skin bacteria is associated with population persistence in the frog Rana muscosa. Biological Conservation, in press.

Becker, M. H., R. M. Brucker, C. R. Schwantes, R. N. Harris, K.P.C. Minbiole. 2009. The bacterially-produced metabolite violacein is associated with survival in amphibians infected with a lethal disease. Applied and Environmental Microbiology 75:6635-6638.

Harris, R. N., R. M. Brucker, J. B. Walke, M. H. Becker, C. R. Schwantes*, D. C Flaherty*, B. A. Lam, D. C. Woodhams, C. J. Briggs, V. T. Vredenburg, K. P. C. Minbiole.  2009. Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. ISME Journal 3:818-824.

Harris, R. N., A. Lauer, M. A. Simon, J. L. Banning*, R. A. Alford.  2009. Addition of antifungal skin bacteria to salamanders ameliorates the effects of chytridiomycosis. Diseases of Aquatic Organisms 83:11-16.

Banning*, J. L., A. L. Weddle*, G. W. Wahl III*, M. A. Simon, A. Lauer, R. L. Walters*, and R. N. Harris. 2008. Antifungal skin bacteria, embryonic survival, and communal nesting in four-toed salamanders, Hemidactylium scutatum. Oecologia 156:423–429

Brucker*, R. M., C. M. Baylor*, R. L. Walters*, A. Lauer, R. N. Harris, and K. P. C. Minbiole. 2008. The identification of 2,4-diacetylphloroglucinol as an antifungal metabolite produced by cutaneous bacteria of the salamander Plethodon cinereus. Journal of Chemical Ecology 34:39-43.

Brucker*, R. M., R. N. Harris, C. R. Schwantes*, T. N. Gallaher, D. C. Flaherty*, B. A. Lam*, K. P. C. Minbiole. 2008. Amphibian chemical defense: antifungal metabolites of the microsymbiont Janthinobacterium lividum on the salamander Plethodon cinereus. Journal of Chemical Ecology 34:1422-1429.

Lauer, A., M. A. Simon, J. L. Banning*, B. Lam*, and R. N. Harris. 2008. Diversity of cutaneous bacteria with antifungal activity isolated from female four-toed salamanders.  The ISME Journal 2: 145–157.

Belden, L. K., and R. N. Harris. 2007. Infectious diseases in wildlife:  the community ecology context. Frontiers in Ecology and Environment 5:533-539.

Lauer, A., M. A. Simon, J. L. Banning*, E. André*, K. Duncan*, and R.  N. Harris.  2007. Common cutaneous bacteria from the eastern red-backed salamander can inhibit pathogenic fungi. Copeia, 2007: 630-640.

Woodhams, D. C., V. T. Vredenburg, M. J. Stice, M. A. Simon, D. Billheimer, B. Shakhtour, Y. Shyr, C. J. Briggs, L. A. Rollins-Smith, and R. N. Harris. 2007. Symbiotic bacteria contribute to innate immune defenses of the threatened mountain yellow-legged frog, Rana muscosa.  Biological Conservation, 138: 390-398.

Woodhams, D. C., L. A. Rollins-Smith, R. A. Alford, M. A. Simon & R. N. Harris. 2007. Response - Innate immune defenses of amphibian skin: antimicrobial peptides and more. Animal Conservation 10: 425–428

Harris, R. N., T. Y. James, A. Lauer, M. A. Simon, A. Patel*. 2006. The amphibian pathogen Batrachochytrium dendrobatidis is inhibited by the cutaneous bacteria of amphibian species.  EcoHealth 3:53-56.

*undergraduate or masters student co-author