Synergistic inhibition of the lethal fungal pathogen batrachochytrium dendrobatidis: The combined effect of symbiotic bacterial metabolites and antimicrobial peptides of the frog rana muscosa

Journal of Chemical Ecology

Volumn 38, Issue 8, 2012, Pages 958-965

  Myers, Jillian M ^a   Ramsey, Jeremy P ^a   Blackman, Alison L ^a   Nichols, A Elizabeth ^a   Minbiole, Kevin P C ^b   Harris, Reid N ^a  

^a JAMES MADISON UNIVERSITY   (United States)

^b VILLANOVA UNIVERSITY   (United States)

Author keywords

2,4 diacetylphloroglucinol; Amphibian conservation; Antimicrobial peptides; Batrachochytrium dendrobatidis; Chytridiomycosis; Metabolites; Probiotic; Pseudomonas fluorescens; Synergy

Indexed keywords

2,4 DIACETYLPHLOROGLUCINOL; 2,4-DIACETYLPHLOROGLUCINOL; ANTIINFECTIVE AGENT; ANTIMICROBIAL CATIONIC PEPTIDE; DRUG DERIVATIVE; PHLOROGLUCINOL;

ALCOHOL; ANTIMICROBIAL ACTIVITY; BIOCHEMISTRY; CONCENTRATION (COMPOSITION); DISEASE RESISTANCE; FROG; FUNGAL DISEASE; FUNGUS; GROWTH REGULATOR; INHIBITION; METABOLITE; ORGANIC COMPOUND; PATHOGEN; PEPTIDE; SECRETION; SKIN; SPECIES CONSERVATION; SYNERGISM;

ANIMAL; ARTICLE; CHEMISTRY; CHYTRIDIOMYCETES; DRUG EFFECT; DRUG POTENTIATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; PSEUDOMONAS FLUORESCENS; RANIDAE; SKIN;

ANIMALS; ANTI-INFECTIVE AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; CHYTRIDIOMYCOTA; DRUG SYNERGISM; MICROBIAL SENSITIVITY TESTS; PHLOROGLUCINOL; PSEUDOMONAS FLUORESCENS; RANIDAE; SKIN;

AMPHIBIA; ANIMALIA; ANURA; BACTERIA (MICROORGANISMS); BATRACHOCHYTRIUM DENDROBATIDIS; PSEUDOMONAS FLUORESCENS; RANA MUSCOSA;

EID: 84870956150     PISSN: 00980331     EISSN: 15731561     Source Type: Journal    
DOI: 10.1007/s10886-012-0170-2     Document Type: Article

References (38)

1. BERG, G., GROSCH, R., and SCHERWINSKI, K. 2007. Risikofolgeabschätzung für den Einsatz mikrobieller Antagonisten: Gibtes Effekte auf Nichtzielorganismen? Gesunde Pflanzen 59:107-117.
2. BERGER, L., SPEARE, R., DASZAK, P., GREEN, D. E., CUNNINGHAM, A. A., GOGGIN, C. L., SLOCOMBE, R., RAGAN, M. A., HYATT, A. D., MCDONALD, K. R., HINES, H. B., LIPS, K. R., MARANTELLI, G., and PARKES, H. 1998. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc. Natl. Acad. Sci. U. S. A. 95:9031-9036.
3. BERGER, L., HYATT, A. D., SPEARE, R., and LONGCORE, J. E. 2005. Life cycle stages of the amphibian chytrid Batrachochytrium dendrobatidis. Dis. Aquat. Org. 68:51-63.
4. BRIGGS, C. J., VREDENBURG, V. T., KNAPP, R. A., and RACHOWICZ, L. J. 2005. Investigating the population-level effects of chytridiomycosis: An emerging infectious disease of amphibians. Ecology 86:3149-3159.
5. BRUCKER, R. M., HARRIS, R. N., SCHWANTES, C. R., GALLAHER, T. N., FLAHERTY, D. C., LAM, B. A., and MINBIOLE, K. P. C. 2008a. Amphibian chemical defense: Antifungal metabolites of the microsymbiont Janthinobacterium lividum on the salamander Plethodon cinereus. J. Chem. Ecol. 34:1422-1429.
6. BRUCKER, R. M., BAYLOR, C. M., WALTERS, R. L., LAUER, A., HARRIS, R. N., and MINBIOLE, K. P. C. 2008b. The identification of 2,4-diacetylphloroglucinol as an antifungal metabolite produced by cutaneous bacteria of the salamander Plethodon cinereus. J. Chem. Ecol. 34:39-43.
7. CASSONE, M. and OTVOS JR, L. 2010. Synergy among antibacterial peptides and between peptides and small-molecule antibiotics. Expert Rev. Anti-Infect. Ther. 8:703-716.
8. COLLINS, J. P. and STORFER, A. 2003. Global amphibian declines: Sorting the hypotheses. Divers. Distrib. 9:89-98.
9. CONLON, J. M., KOLODZIEJEK, J., and NOWOTNY, N. 2004. Antimicrobial peptides from ranid frogs: Taxonomic and phylogenetic markers and a potential source of new therapeutic agents. Biochim. Biophys. Acta 1696:1-14.
10. CONLON, J. M., WOODHAMS, D. C., RAZAA, H., COQUET, L., LEPRINCE, J., JOUENNE, T., VAUDRY, H., and ROLLINS-SMITH, L. A. 2007. Peptides with differential cytolytic activity from skin secretions of the Lemur leaf frog Hylomantis lemur (Hylidae: Phyllomedusinae). Toxicon 50:498-506.
11. DALY, J. W. 1995. The chemistry of poisons in amphibian skin. Proc. Natl. Acad. Sci. U. S. A. 92:9-13.
12. HARRIS, R. N., JAMES, T. Y., LAUER, A., SIMON, M. A., and PATEL, A. 2006. Amphibian pathogen Batrachochytrium dendrobatidis is inhibited by the cutaneous bacteria of amphibian species. EcoHealth 3:53-56.
13. HARRIS, R. N., LAUER, A., SIMON, M. A., BANNING, J. L., and ALFORD, R. A. 2009a. Addition of antifungal skin bacteria to salamanders ameliorates the effects of chytridiomycosis. Dis. Aquat. Org. 83:11-16.
14. HARRIS, R. N., BRUCKER, R. M., WALKE, J. B., BECKER, M. H., SCHWANTES, C. R., FLAHERTY, D. C., LAM, B. A., WOODHAMS, D. C., BRIGGS, C. J., VREDENBURG, V. T., and MINBIOLE, K. P. 2009b. Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. ISME J. 3:818-824.
15. HOFFMAN, M., ET AL. 2010. The impact of conservation on the status of the world's vertebrates. Science 330:1503-1509.
16. KILPATRICK, A., BRIGGS, C., and DASZAK, P. 2010. The ecology and impact of chytridiomycosis: An emerging disease of amphibians. Trends Ecol. Evol. 25:109-118.
17. LAM, B. A., WALKE, J. B., VREDENBURG, V. T., and HARRIS, R. N. 2010. Proportion of individuals with anti-Batrachochytrium dendrobatidis skin bacteria is associated with population persistence in the frog Rana muscosa. Biol. Conserv. 143:529-531.
18. LAUER, A., SIMON, M. A., BANNING, J. L., and Re E., DUNCAN, K., and HARRIS, R. N. 2007. Common cutaneous bacteria from the eastern red-backed salamander can inhibit pathogenic fungi. Copeia 2007:630-640.
19. LAUER, A., SIMON, M. A., BANNING, J. L., LAM, B., and HARRIS, R. N. 2008. Diversity of cutaneous bacteria with antifungal activity isolated from female four-toed salamanders. ISME J. 2:145-157.
20. LIPS, K. R., BREM, F., BRENES, R., REEVE, J. D., ALFORD, R. A., VOYLES, J., CAREY, C., LIVO, L., PESSIER, A. P., and COLLINS, J. P. 2006. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc. Natl. Acad. Sci. U. S. A. 103:3165-3170.
21. MINTEER, B. A. and COLLINS, J. P. 2008. From environmental to ecological ethics: Toward a practical ethics for ecologists and conservationists. Sci. Eng. Ethics 14:483-501.
22. PASK, J. D., WOODHAMS, D. C., and ROLLINS SMITH, L. A. 2012. The ebb and flow of antimicrobial skin peptides defends northern leopard frogs (Rana pipiens) against chytridiomycosis. Glob. Chang. Biol. 18:1231-1238.
23. RAMSEY, J. P., REINERT, L. K., HARPER, L. K., WOODHAMS, D. C., and ROLLINS-SMITH, L. A. 2010. Immune defenses against Batrachochytrium dendrobatidis, a fungus linked to global amphibian declines, in the South African clawed frog, Xenopus laevis. Infect. Immun. 78:3981-3992.
24. ROLLINS-SMITH, L. A. 2009. The role of amphibian antimicrobial peptides in protection of amphibians from pathogens linked to global amphibian declines. Biochim. Biophys. Acta 1788:1593-1599.
25. ROLLINS-SMITH, L. A. and CONLON, J. M. 2005. Antimicrobial peptide defenses against chytridiomycosis, an emerging infectious disease of amphibian populations. Dev. Comp. Immunol. 29:589-598.
26. ROLLINS-SMITH, L. A., CAREY, C., LONGCORE, J., DOERSAM, J. K., BOUTTE, A., BRUZGAL, J. E., and CONLON, J. M. 2002. Activity of antimicrobial skin peptides from ranid frogs against Batrachochytrium dendrobatidis, the chytrid fungus associated with global amphibian declines. Dev. Comp. Immunol. 26:471-479.
27. ROLLINS-SMITH, L. A., WOODHAMS, D. C., REINERT, L. K., VREDENBURG, V. T., BRIGGS, C. J., NIELSEN, P. F., and CONLON, J. M. 2006. Antimicrobial peptide defenses of the mountain yellow-legged frog (Rana muscosa). Dev. Comp. Immunol. 30:831-842.
28. SCHERWINSKI, K., GROSCH, R., and BERG, G. 2008. Effect of bacterial antagonists on lettuce: Active biocontrol of Rhizoctonia solani and negligible, short-term effects on nontarget microorganisms. FEMS Microbiol. Ecol. 64:106-116.
29. SIMMACO, M., MIGNOGNA, G., and BARRA, D. 1998. Antimicrobial peptides from amphibian skin: What do they tell us? Biopolymers 47:435-450.
30. SIMON, S. N., CHANCON, J. S., COX, N. A., YOUNG, B. E., RODRIGUES, A. S. L., FISCHMAN, D. L., and WALLER, R. W. 2004. Status and trends of amphibian declines and extinctions worldwide. Science 306:1783-1786.
31. VREDENBURG, V. T., BRIGGS, C. J., and HARRIS, R. 2011. Hostpathogen dynamics of amphibian chytridiomycosis: The role of the skin microbiome in health and disease, pp. 342-355, in L. Olsen, E. R. Choffnes, D. A. Relman, and L. Pray (eds.), Fungal Diseases: An Emerging Threat to Human, Animal, and Plant Health. The National Academies Press, Washington, D. C.
32. WELDON, C., DU PREEZ, L. H., HYATT, A. D., MULLER, R., and SPEARE, R. 2004. Origin of the amphibian chytrid fungus. Emerg. Infect. Dis. 10:2100-2105.
33. WOODHAMS, D. C., VOYLES, J., LIPS, K. R., CAREY, C., and ROLLINSSMITH, L. A. 2005. Predicted disease susceptibility in a Panamanian amphibian assemblage based on skin peptide defenses. J. Wildl. Dis. 42:207-218.
34. WOODHAMS, D. C., ROLLINS-SMITH, L. A., CAREY, C., REINERT, L., TYLER, M. J., and ALFORD, R. 2006. Population trends associated with antimicrobial peptide defenses against chytridiomycosis in Australian frogs. Oecologia 46:531-540.
35. WOODHAMS, D. C., ARDIPRADJA, K., ALFORD, R. A., MARANTELLI, G., REINERT, L. K., and ROLLINS-SMITH, L. A. 2007a. Resistance to chytridiomycosis varies by amphibian species and is correlated with skin peptide defenses. Anim. Conserv. 10:409-417.
36. WOODHAMS, D. C., ROLLINS-SMITH, L. A., ALFORD, R. A., SIMON, M. A., and HARRIS, R. N. 2007b. Response - Innate immune defenses of amphibian skin: antimicrobial peptides and more. Anim. Conserv. 10:425-428.
37. WOODHAMS, D. C., VREDENBURG, V. T., STICE, M. J., SIMON, M. A., BILLHEIMER, D., SHAKHTOUR, B., SHYR, Y., BRIGGS, C. J., ROLLINS-SMITH, L. A., and HARRIS, R. N. 2007c. Symbiotic bacteria contribute to innate immune defenses of the threatened mountain yellow-legged frog, Rana muscosa. Biol. Conserv. 138:390-398.
38. ZASLOFF, M. 2002. Antimicrobial peptides of multicellular organisms. Nature 415:389-395.