Role of Antimicrobial Peptides in Amphibian Defense Against Trematode Infection
Antimicrobial peptides (AMPs) contribute to the immune defenses of many vertebrates, including amphibians. As larvae, amphibians are often exposed to the infectious stages of trematode parasites, many of which must penetrate the host’s skin, potentially interacting with host AMPs. We tested the effects of the natural AMPs repertoires on both the survival of trematode infectious stages as well as their ability to infect larval amphibians. All five trematode species exhibited decreased survival of cercariae in response to higher concentrations of adult bullfrog AMPs, but no effect when exposed to AMPs from larval bullfrogs. Similarly, the use of norepinephrine to remove AMPs from larval bullfrogs, Pacific chorus frogs, and gray treefrogs had only weak (gray treefrogs) or non-significant (other tested species) effects on infection success by Ribeiroia ondatrae. We nonetheless observed strong differences in parasite infection as a function of both host stage (first- versus second-year bullfrogs) and host species (Pacific chorus frogs versus gray treefrogs) that were apparently unrelated to AMPs. Taken together, our results suggest that AMPs do not play a significant role in defending larval amphibians against trematode cercariae, but that they could be one mechanism helping to prevent infection of post-metamorphic amphibians, particularly for highly aquatic species.
Keywordsdisease ecology wildlife immunology antimicrobial peptides trematodes
We thank Travis McDevitt-Galles, Jay Bowerman, and Chris Smith for collecting the snails and amphibians used in this study. We also thank Christina Garcia, Katherine Hardy, and Abigail Kimball for assisting with animal husbandry. Finally, we thank two anonymous reviewers for their comments on the manuscript. This research was supported by funding from the National Science Foundation (DEB-0841758), the National Institutes of Health (NIH-KK1408), and the David and Lucile Packard Foundation.
- Apidianakis Y, Mindrinos MN, Wenzhong X, Lau GW, Baldini RL, Davis RW, Rahme LG (2005) Profiling early infection responses: Pseudomonas aeruginosa eludes host defense by suppressing antimicrobial peptide gene expression. Proceedings of the National Academy of Sciences of the United States of America 102: 2573–2578.CrossRefPubMedPubMedCentralGoogle Scholar
- Chivers DP, Wisenden BD, Hindman CJ, Michalak TA, Kusch RC, Kaminskyj SG, Jack KL, Ferrari MC, Pollock RJ, Halbgewachs CF, Pollock MS, Alemadi S, James CT, Savaloja RK, Goater CP, Corwin A, Mirza RS, Kiesecker JM, Brown GE, Adrian JC Jr, Krone PH, Blaustein AR, Mathis A. (2007) Epidermal ‘alarm substance’ cells of fishes maintained by non-alarm functions: possible defense against pathogens, parasites and UVB radiation. Proceedings of the Royal Society of London B: Biological Sciences. 274: 2611–2619.CrossRefGoogle Scholar
- Fox J (2002) Cox proportional-hazards regression for survival data. An R and S-PLUS companion to applied regression, Sage Publications: London, pp. 1–18.Google Scholar
- Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16: 183–190.Google Scholar
- Holden WM, Reinert LK, Hanlon SM, Parris MJ, Rollins-Smith LA (2015) Development of antimicrobial peptide defenses of southern leopard frogs, Rana sphenocephala, against the pathogenic chytrid fungus, Batrachochytrium dendrobatidis. Developmental and Comparative Immunology 48: 65–75.CrossRefPubMedGoogle Scholar
- Katzenback BA, Holden HA, Falardeau J, Childers C, Hadj-Moussa H, Avis TJ, Storey KB (2014) Regulation of the Rana sylvatica brevinin-1SY antimicrobial peptide during development and in dorsal and ventral skin in response to freezing, anoxia and dehydration. Journal of Experimental Biology 217: 1392–1401.CrossRefPubMedGoogle Scholar
- Pretzel J, Mohring F, Rahlfs S, Becker K (2013) Antiparasitic peptides. Yellow Biotechnology I: 157–192.Google Scholar
- Ramsey JP, Reinert LK, Harper LK, Woodhams DC, Rollins-Smith LA (2010) Immune defenses against Batrachochytrium dendrobatidis, a fungus linked to global amphibian declines, in the South African clawed frog, Xenopus laevis. Infection and Immunity 78: 3981–3992.CrossRefPubMedPubMedCentralGoogle Scholar
- Rollins-Smith LA, Woodhams DC (2011) Amphibian immunity: Staying in tune with the environment. In: Ecoimmunology, Demas GE, Nelson RJ (editors), New York: Oxford University Press, pp 92–143Google Scholar
- Schell SC (1970) How to know the trematodes. Dubuque, Iowa: Wm. C. Brown Company Publishers.Google Scholar
- Schell SC (1985) Handbook of trematodes of North America North of Mexico. University Press of Idaho, Moscow.Google Scholar
- Tennessen JA, Woodhams DC, Chaurand P, Reinert LK, Billheimer D, Shyr Y, Caprioli RM, Blouin MS, Rollins-Smith LA (2009) Variations in the expressed antimicrobial peptide repertoire of Northern leopard frog (Rana pipiens) populations suggest intraspecies differences in resistance to pathogens. Developmental and Comparative Immunology 33: 1247–1257.CrossRefPubMedPubMedCentralGoogle Scholar