Interactions between amphibians' symbiotic bacteria cause the production of emergent anti-fungal metabolites

Frontiers in Microbiology

Volumn 5, Issue AUG, 2014, Pages

  Loudon, Andrew H ^a   Holland, Jessica A ^a   Umile, Thomas P ^b   Burzynski, Elizabeth A ^b   Minbiole, Kevin P C ^b   Harris, Reid N ^a  

^a JAMES MADISON UNIVERSITY   (United States)

^b VILLANOVA UNIVERSITY   (United States)

Author keywords

Amphibians; Anti fungal metabolites; Batrachochytrium dendrobatidis; Emergent metabolites; Host associated microbial communities; Interspecific competition; Symbiotic bacteria; Synergy

Indexed keywords

TRYPTOPHOL;

AMPHIBIA; ANALYSIS OF VARIANCE; ARTICLE; BATRACHOCHYTRIUM DENDROBATIDIS; CHYTRIDIOMYCOSIS; COMPARATIVE STUDY; CONTROLLED STUDY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IC50; JANTHINOBACTERIUM; KNOWLEDGE; MASS SPECTROMETRY; METABOLIC REGULATION; MICROBIAL COMMUNITY; NONHUMAN; OPTICAL DENSITY; POLYMERASE CHAIN REACTION; PROTON NUCLEAR MAGNETIC RESONANCE; SYMBIOSIS;

EID: 84987781483     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00441     Document Type: Article

References (33)

1. Becker, M. H., Brucker, R. M., Schwantes, C. R., Harris, R. N., and Minbiole, K. P. C. (2009). The bacterially produced metabolite violacein is associated with survival of amphibians infected with a lethal fungus. Appl. Environ. Microbiol. 75, 6635-6638. doi: 10.1128/AEM.01294-09
2. Becker, M. H., and Harris, R. N. (2010). Cutaneous bacteria of the redback salamander prevent morbidity associated with a lethal disease. PLoS ONE 5:e10957. doi: 10.1371/journal.pone.0010957
3. Becker, M. H., Harris, R. N., Minbiole, K. P., Schwantes, C. R., Rollins-Smith, L. A., Reinert, L. K., et al. (2011). Towards a better understanding of the use of probiotics for preventing chytridiomycosis in Panamanian golden frogs. Ecohealth 8, 501-506. doi: 10.1007/s10393-012-0743-0
4. Bell, S. C., Alford, R. A., Garland, S., Padilla, G., and Thomas, A. D. (2013). Screening bacterial metabolites for inhibitory effects against Batrachochytrium dendrobatidis using a spectrophotometric assay. Dis. Aquat. Org. 103, 77-85. doi: 10.3354/dao02560
5. Bletz, M. C., Loudon, A. H., Becker, M. H., Bell, S. C., Woodhams, D. C., Minbiole, K. P. C. M., et al. (2013). Mitigating amphibian chytridiomycosis with bioaugmentation: characteristics of effective probiotics and strategies for their selection and use. Ecol. Lett. 16, 807-820. doi: 10.1111/ele.12099
6. Brucker, R. M., Baylor, C. M., Walters, R. L., Lauer, A., Harris, R. N., and Minbiole, K. P. C. (2008a). 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. doi: 10.1007/s10886-007-9352-8
7. Brucker, R. M., Harris, R. N., Schwantes, C. R., Gallaher, T. N., Flaherty, D. C., Lam, B. A., et al. (2008b). Amphibian chemical defense: antifungal metabolites of the microsymbiont Janthinobacterium lividum on the salamander Plethodon cinereus. J. Chem. Ecol. 34, 1422-1429. doi: 10.1007/s10886-008-9555-7
8. De Boer, W., Wagenaar, A. M., Klein Gunnewiek, P. J. A., and Van Veen, J. A. (2007). In vitro suppression of fungi caused by combinations of apparently non-antagonistic soil bacteria. FEMS Microbiol. Ecol. 59, 177-185. doi: 10.1111/j.1574-6941.2006.00197.x
9. Ghannoum, M. A., and Rice, L. B. (1999). Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clin. Microbiol. Rev. 12, 501-517.
10. Guzmán-López, O., Trigos, A., Fernández, F. J., de Jesús Yañez-Morales, M., and Saucedo-Castaneda, G. (2007). Tyrosol and tryptophol produced by Ceratocystis adiposa. World J. Microbiol. Biotechnol. 23, 1473-1477. doi: 10.1007/s11274-007-9392-9
11. Harris, R. N., Brucker, R. M., Walke, J. B., Becker, M. H., Schwantes, C. R., Flaherty, D. C., et al. (2009b). Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. ISME j. 3, 818-824. doi: 10.1038/ismej.2009.27
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. doi: 10.1007/s10393-005-0009-1
13. Harris, R. N., Lauer, A., Simon, M. A., Banning, J. L. M., and Alford, R. A. (2009a). Addition of antifungal skin bacteria to salamanders ameliorates the effects of chytridiomycosis. Dis. Aquat. Org. 83, 11-16. doi: 10.3354/dao02004
14. Hoffmann, M., Hilton-Taylor, C., Angulo, A., Böhm, M., Brooks, T. M., Butchart, S. H., et al. (2010). The impact of conservation on the status of the world's vertebrates. Science 330, 1503-1509. doi: 10.1126/science.1194442
15. Kilpatrick, A. M., Briggs, C. J., and Daszak, P. (2010). The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends Ecol. Evol. 25, 190-118. doi: 10.1016/j.tree.2009.07.011
16. Kueneman, J. G., Parfrey, L. W., Woodhams, D. C., Archer, H. M., Knight, R., and McKenzie, V. J. (2013). The amphibian skin-associated microbiome across species, space and life history stages. Mol. Ecol. 23, 1238-1250. doi: 10.1111/mec.12510
17. Lauer, A., Simon, M. A., Banning, J. L., Andre, E., Duncan, K., and Harris, R. N. (2007). Common cutaneous bacteria from the eastern red-backed salamander can inhibit pathogenic fungi. Copeia 3, 630-640. doi: 10.1643/0045-8511(2007)2007[630:CCBFTE]2.0.CO;2
18. Lawley, T. D., Clare, S., Walker, A. W., Stares, M. D., Connor, T. R., Raisen, C., et al. (2012). Targeted restoration of the intestinal microbiota with a simple, defined bacteriotherapy resolves relapsing Clostridium difficile disease in mice. PLoS Pathog. 8:e1002995. doi: 10.1371/journal.ppat.1002995
19. Lingappa, B. T., Prasad, M., Lingappa, Y., Hunt, D. F., and Biemann, K. (1969). Phenethyl alcohol and tryptophol: autoantibiotics produced by the fungus Candida albicans. Science 163, 192-194. doi: 10.1126/science.163.3863.192
20. Loudon, A. H., Woodhams, D. C., Parfrey, L. W., Archer, H., Knight, R., McKenzie, V., et al. (2013). Microbial community dynamics and effect of environmental microbial reservoirs on red-backed salamanders (Plethodon cinereus). ISME J. 8, 830-840. doi: 10.1038/ismej.2013.200
21. McKenzie, V. J., Bowers, R. M., Fierer, N., Knight, R., and Lauber, C. L. (2011). Co-habiting amphibian species harbor unique skin bacterial communities in wild populations. ISME J. 6, 588-596. doi: 10.1038/ismej.2011.129
22. Myers, J. M., Ramsey, J. P., Blackman, A. L., Nichols, A. E., Minbiole, K. P. C., and Harris, R. N. (2012). Synergistic inhibition of the lethal fungal pathogen Batrachochytrium dendrobatidis: the combined effects of symbiotic bacteria metabolites and antimicrobial peptides of the frog Rana muscosa. J. Chem. Ecol. 8, 958-965. doi: 10.1007/s10886-012-0170-2
23. Rey, P., Leucart, S., Desilets, H., Bélanger, R. R., Larue, J. P., and Tirilly, Y. (2001). Production of indole-3-acetic acid and tryptophol by Pythium ultimum and Pythium group F: possible role in pathogenesis. Eur. J. Plant Pathol. 107, 895-904. doi: 10.1023/A:1013187922191
24. Rosazza, J. P., Juhl, R., and Davis, P. (1973). Tryptophol formation by Zygosaccharomyces priorianus. Appl. Microbiol. 26, 98-105.
25. Scheuring, I., and Yu, D. W. (2012). How to assemble a beneficial microbiome in three easy steps. Ecol. Lett. 11, 1300-1307. doi: 10.1111/j.1461-0248.2012.01853.x
26. Stuart, S. N., Chanson, J. S., Cox, N. A., Young, B. E., Rodrigues, A. S. L., Fischman, D. L., et al. (2004). Status and trends of amphibian declines and extinction worldwide. Science 306, 1783-1786. doi: 10.1126/science.1103538
27. Sugawara, F., and Strobel, G. A. (1987). Tryptophola phytotoxin produced by Drechslera nodulosum. Phytochemistry 26, 1349-1351. doi: 10.1016/S0031-9422(00)81810-5
28. Umile, T. P., McLaughlin, P. J., Johnson, K. R., Honarvar, S., Blackman, A. L., Burzynski, E. A., et al. (2014). Nonlethal amphibian skin swabbing of cutaneous natural products for HPLC fingerprinting. Anal. Methods 6, 3277-3284. doi: 10.1039/c4ay00566j
29. Vredenburg, V. T., Briggs, C. J., and Harris, R. N. (2011). "Host-pathogen dynamics of amphibian chytridiomycosis: the role of the skin microbiome in health and disease". in Fungal Diseases: An Emerging Challenge to Human, Animal, and Plant Health, eds L. Olsen, E. Choffnes, D. A. Relman, and L. Pray (Washington, DC: The National Academies Press), 342-355.
30. Wake, D. B., and Vredenburg, V. T. (2008). Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proc. Nat. Acad. Sci. U.S.A. 105 (Suppl. 1), 11466-11473. doi: 10.1073/pnas.0801921105
31. Walke, J. B., Becker, M. H., Loftus, S. C., House, L. L., Cormier, G., Jensen, R. V., et al. (2014). Amphibian skin may select for rare environmental microbes. ISME J. doi: 10.1038/ismej.2014.77. [Epub ahead of print].
32. Woodhams, D. C., Brandt, H., Baumgartner, S., Kielgast, J., Küpfer, E., Tobler, U., et al. (2014). Interacting symbionts and immunity in the amphibian skin mucosome predict disease risk and probiotic effectiveness. PLoS ONE 9:e96375. doi: 10.1371/journal.pone.0096375
33. Woodhams, D. C., Vredenburg, V. T., Simon, M. A., Billheimer, D., Shakhtour, B., Shyr, Y., et al. (2007). Symbiotic bacteria contribute to innate immune defenses of the threatened mountain yellow-legged frog, Rana muscosa. Biol. Conserv. 138, 390-398. doi: 10.1016/j.biocon.2007.05.004