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Role of Antimicrobial Peptides in Amphibian Defense Against Trematode Infection

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Abstract

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.

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References

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bahar AA, Ren D (2013) Antimicrobial peptides. Pharmaceuticals 6: 1543–1575.

    Article  PubMed  PubMed Central  Google Scholar 

  • Batycka-Baran A, Maj J, Wolf R, Szepietowski JC (2014) The new insight into the role of antimicrobial proteins alarmins in the immunopathogeneis of Psoriais. Journal of Immunology Research 2014: 1–10.

    Article  Google Scholar 

  • Blaustein AR, Han BA, Relyea RA, Johnson PT, Buck JC, Gervasi SS, Kats LB (2011) The complexity of amphibian population declines: understanding the role of cofactors in driving amphibian losses. Annals of the New York Academy of Sciences 1223: 108–119.

    Article  PubMed  Google Scholar 

  • Beaver PC (1939) The morphology and life history of Psilostomum ondatrae Price 1931 (Trematoda: Psilostomatidae). Journal of Parasitology 25: 383–393.

    Article  Google Scholar 

  • Belden LK, Kiesecker JM (2005) Glucocorticosteroid hormone treatment of larval treefrogs increases infection by Alaria sp. trematode cercariae. Journal of Parasitology 9: 686–688.

    Article  Google Scholar 

  • Bovbjerg AM (1963) Development of the glands of the dermal plicae in Rana pipiens. Journal of Morphology 113: 231–243.

    Article  CAS  PubMed  Google Scholar 

  • Brogden KA, Ackermann M, McCray PB, Tack BF (2003) Antimicrobial peptides in animals and their role in host defenses. International Journal of Antimicrobial Agents 22: 465–478.

    Article  CAS  PubMed  Google Scholar 

  • Bulet P, Stöcklin R, Menin L (2004) Anti‐microbial peptides: from invertebrates to vertebrates. Immunological Reviews 198: 169–184.

    Article  CAS  PubMed  Google Scholar 

  • Carey C, Cohen N, Rollins-Smith L (1999) Amphibian declines: an immunological perspective. Developmental and Comparative Immunology 23: 459–472.

    Article  CAS  PubMed  Google Scholar 

  • Clark DP, Durell S, Maloy WL, Zasloff M (1994). Ranalexin: A novel antimicrobial peptide from bullfrog (Rana cateseiana) skin, structurally related to the bacterial antibiotic, polymixin. Journal of Biological Chemistry 269: 10849–10855.

    CAS  PubMed  Google 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.

    Article  Google Scholar 

  • Conlon JM (2008) Reflections on a systematic nomenclature for antimicrobial peptides from the skins of frogs of the family Ranidae. Peptides 29: 1815–1819.

    Article  CAS  PubMed  Google Scholar 

  • Densmore CL, Green DE (2007) Diseases of amphibians. Ilar Journal 48: 235–254.

    Article  CAS  PubMed  Google 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 

  • Gammill WM, Fites JS, Rollins-Smith LA (2012) Norepinephrine depletion of antimicrobial peptides from the skin glands of Xenopus laevis. Developmental and Comparative Immunology 37: 19–27.

    Article  CAS  PubMed  Google Scholar 

  • Ganz T (2003) The role of antimicrobial peptides in innate immunity. Integrative and Comparative Biology 43: 300–304.

    Article  CAS  PubMed  Google Scholar 

  • Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16: 183–190.

    Google Scholar 

  • Groner ML, Buck JC, Gervasi S, Blaustein AR, Reinert LK, Rollins-Smith LA, Bier ME, Hempel J, Relyea RA (2013) Larval exposure to predator cues alters immune function and response to a fungal pathogen in post-metamorphic wood frogs. Ecological Applications 23: 1443–1454.

    Article  PubMed  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.

    Article  CAS  PubMed  Google Scholar 

  • Holland MP, Skelly DK, Kashgarian M, Bolden SR, Harrison LM, Cappello M (2007) Echinostome infection in green frogs (Rana clamitans) is stage and age dependent. Journal of Zoology 271: 455–462.

    Article  Google Scholar 

  • Johnson PTJ, Lunde KB, Thurman EM, Ritchie EG, Wray SN, Sutherland DR, Blaustein AR (2002) Parasite (Ribeiroia ondatrae) infection linked to amphibian malformations in the western United States. Ecological Monographs 72: 151–168.

    Article  Google Scholar 

  • Johnson PTJ, Hartson RB (2009) All hosts are not equal: explaining differential patterns of malformations in an amphibian community. Journal of Animal Ecology 78: 191–201.

    Article  PubMed  Google Scholar 

  • Johnson PTJ, Kellermanns E, Bowerman J (2011) Critical windows of disease risk: amphibian pathology driven by developmental changes in host resistance and tolerance. Functional Ecology 25: 726–734.

    Article  Google Scholar 

  • Johnson PT, Rohr JR, Hoverman JT, Kellermanns E, Bowerman J, Lunde KB (2012) Living fast and dying of infection: host life history drives interspecific variation in infection and disease risk. Ecology Letters 15: 235–242.

    Article  PubMed  Google 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.

    Article  CAS  PubMed  Google Scholar 

  • Koprivnikar J, Marcogliese DJ, Rohr JR, Orlofske SA, Raffel TR, Johnson PTJ (2012) Macroparasite infections of amphibians: what can they tell us? EcoHealth 9: 342–360.

    Article  PubMed  Google Scholar 

  • LaFonte BE, Johnson PTJ (2013) Experimental infection dynamics: using immunosuprression and in vivo parasites tracking to understand host resistance in an amphibian–trematode system. The Journal of Experimental Biology 216: 3700–3708.

    Article  PubMed  Google Scholar 

  • Levy O (1996) Antibiotic proteins of polymorphonuclear leukocytes. European Journal of Haematology 56: 263–277.

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Xiang Q, Zhang Q, Huang Y, Su Z (2012) Overview on the recent study of antimicrobial peptides: origins, functions, relative mechanisms and application. Peptides 37: 207–215.

    Article  CAS  PubMed  Google Scholar 

  • Nicolas P, Mor A (1995) Peptides as weapons against microorganisms in the chemical defense system of vertebrates. Annual Reviews in Microbiology 49: 277–304.

    Article  CAS  Google Scholar 

  • Paull SH, Johnson PTJ (2014) Experimental warming drives a seasonal shift in the timing of host‐parasite dynamics with consequences for disease risk. Ecology Letters 17:445–453.

    Article  PubMed  Google Scholar 

  • Pask JD, Woodhams DC, Rollins‐Smith LA (2012) The ebb and flow of antimicrobial skin peptides defends northern leopard frogs (Rana pipiens) against chytridiomycosis. Global Change Biology 18: 1231–1238.

    Article  Google Scholar 

  • Pinto EG, Pimenta DC, Antoniazzi MM, Jared C, Tempone AG (2013) Antimicrobial peptides isolated from Phyllomedusa nordestina (Amphibia) alter the permeability of plasma membrane of Leishmania and Trypanosoma cruzi. Experimental Parasitology 135: 655–660.

    Article  CAS  PubMed  Google Scholar 

  • Pretzel J, Mohring F, Rahlfs S, Becker K (2013) Antiparasitic peptides. Yellow Biotechnology I: 157–192.

    CAS  Google Scholar 

  • Raffel TR, Lloyd-Smith JO, Sessions SK, Hudson PJ, Rohr JR (2011) Does the early frog catch the worm? Disentangling potential drivers of a parasite age-intensity relationship in tadpoles. Oecologia 165: 1031–1042.

    Article  PubMed  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richgels KL, Hoverman JT, Johnson PT (2013) Evaluating the role of regional and local processes in structuring a larval trematode metacommunity of Helisoma trivolvis. Ecography 36: 854–863.

    Article  Google Scholar 

  • Rinaldi AC (2002) Antimicrobial peptides from amphibian skin: an expanding scenario: Commentary. Current Opinion in Chemical Biology 6: 799–804.

    Article  CAS  PubMed  Google Scholar 

  • Rollins-Smith LA 1998. Metamorphosis and the amphibian immune system. Immunological Reviews 166: 221–230.

    Article  CAS  PubMed  Google Scholar 

  • Rollins-Smith LA, Reinert LK, Miera V, Conlon JM. 2002. Antimicrobial peptide defenses of the Tarahumara frog, Rana tarahumarae. Biochemical and biophysical research communications 297: 361–367.

    Article  CAS  PubMed  Google Scholar 

  • Rollins-Smith LA, Reinert LK, O’Leary CJ, Houston LE, Woodhams DC (2005) Antimicrobial peptide defenses in amphibian skin. Integrative and Comparative Biology 45: 137–142.

    Article  CAS  PubMed  Google 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 92–143

    Google Scholar 

  • Rohr JR, Raffel TR, Hall CA (2010) Developmental variation in resistance and tolerance in a multi‐host–parasite system. Functional Ecology 24: 1110–1121.

    Article  Google 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 

  • Schotthoefer AM, Cole RA, Beasley VR (2003) Relationship of tadpole stage to location of echinostome cercariae encystment and the consequences for tadpole survival. Journal of Parasitology 89: 475–482.

    Article  PubMed  Google Scholar 

  • Sears BF, Schlunk AD, Rohr JR (2012) Do parasitic trematode cercariae demonstrate a preference for susceptible host species? PLoS one 7: e51012.

    Article  CAS  PubMed  PubMed Central  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Todd BD (2007) Parasites lost? An overlooked hypothesis for the evolution of alternative reproductive strategies in amphibians. The American Naturalist 170: 793–799.

    Article  PubMed  Google Scholar 

  • Woodhams DC, Ardipradja K, Alford RA, Marantelli G, Reinert LK, Rollins-Smith LA (2007) Resistance to chytridiomycosis varies among amphibian species and is correlated with skin peptide defense. Animal Conservation 10: 409–417.

    Article  Google Scholar 

  • Yeaman MR, Yount NY (2003) Mechanisms of antimicrobial peptide action and resistance. Pharmacological Reviews 55: 27–55.

    Article  CAS  PubMed  Google Scholar 

  • Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415: 389–95.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

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.

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Correspondence to Dana M. Calhoun.

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Calhoun, D.M., Woodhams, D., Howard, C. et al. Role of Antimicrobial Peptides in Amphibian Defense Against Trematode Infection. EcoHealth 13, 383–391 (2016). https://doi.org/10.1007/s10393-016-1102-3

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  • DOI: https://doi.org/10.1007/s10393-016-1102-3

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