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Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression
Emerging fungal pathogens pose a greater threat to biodiversity than any other parasitic group, causing declines of many taxa, including bats, corals, bees, snakes and amphibians. Currently, there is little evidence that wild animals can acquire resistance to these pathogens. Batrachochytrium dendro...
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Published in: | Nature (London) 2014-07, Vol.511 (7508), p.224-227 |
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creator | McMahon, Taegan A Sears, Brittany F Venesky, Matthew D Bessler, Scott M Brown, Jenise M Deutsch, Kaitlin Halstead, Neal T Lentz, Garrett Tenouri, Nadia Young, Suzanne Civitello, David J Ortega, Nicole Fites, J Scott Reinert, Laura K Rollins-Smith, Louise A Raffel, Thomas R Rohr, Jason R |
description | Emerging fungal pathogens pose a greater threat to biodiversity than any other parasitic group, causing declines of many taxa, including bats, corals, bees, snakes and amphibians. Currently, there is little evidence that wild animals can acquire resistance to these pathogens. Batrachochytrium dendrobatidis is a pathogenic fungus implicated in the recent global decline of amphibians. Here we demonstrate that three species of amphibians can acquire behavioural or immunological resistance to B. dendrobatidis. Frogs learned to avoid the fungus after just one B. dendrobatidis exposure and temperature-induced clearance. In subsequent experiments in which B. dendrobatidis avoidance was prevented, the number of previous exposures was a negative predictor of B. dendrobatidis burden on frogs and B. dendrobatidis-induced mortality, and was a positive predictor of lymphocyte abundance and proliferation. These results suggest that amphibians can acquire immunity to B. dendrobatidis that overcomes pathogen-induced immunosuppression and increases their survival. Importantly, exposure to dead fungus induced a similar magnitude of acquired resistance as exposure to live fungus. Exposure of frogs to B. dendrobatidis antigens might offer a practical way to protect pathogen-naive amphibians and facilitate the reintroduction of amphibians to locations in the wild where B. dendrobatidis persists. Moreover, given the conserved nature of vertebrate immune responses to fungi and the fact that many animals are capable of learning to avoid natural enemies, these results offer hope that other wild animal taxa threatened by invasive fungi might be rescued by management approaches based on herd immunity. |
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Currently, there is little evidence that wild animals can acquire resistance to these pathogens. Batrachochytrium dendrobatidis is a pathogenic fungus implicated in the recent global decline of amphibians. Here we demonstrate that three species of amphibians can acquire behavioural or immunological resistance to B. dendrobatidis. Frogs learned to avoid the fungus after just one B. dendrobatidis exposure and temperature-induced clearance. In subsequent experiments in which B. dendrobatidis avoidance was prevented, the number of previous exposures was a negative predictor of B. dendrobatidis burden on frogs and B. dendrobatidis-induced mortality, and was a positive predictor of lymphocyte abundance and proliferation. These results suggest that amphibians can acquire immunity to B. dendrobatidis that overcomes pathogen-induced immunosuppression and increases their survival. Importantly, exposure to dead fungus induced a similar magnitude of acquired resistance as exposure to live fungus. Exposure of frogs to B. dendrobatidis antigens might offer a practical way to protect pathogen-naive amphibians and facilitate the reintroduction of amphibians to locations in the wild where B. dendrobatidis persists. Moreover, given the conserved nature of vertebrate immune responses to fungi and the fact that many animals are capable of learning to avoid natural enemies, these results offer hope that other wild animal taxa threatened by invasive fungi might be rescued by management approaches based on herd immunity.</description><identifier>ISSN: 0028-0836</identifier><identifier>EISSN: 1476-4687</identifier><identifier>DOI: 10.1038/nature13491</identifier><identifier>PMID: 25008531</identifier><identifier>CODEN: NATUAS</identifier><language>eng</language><publisher>England: Nature Publishing Group</publisher><subject>Amphibians ; Amphibians - immunology ; Amphibians - microbiology ; Animal populations ; Animals ; Antigens, Fungal - immunology ; Cell Proliferation ; Chytridiomycota - immunology ; Diseases ; Experiments ; Frogs ; Fungi ; Fungi, Pathogenic ; Gene expression ; Generalized linear models ; Health aspects ; Immune response ; Immunology ; Infections ; Lymphocyte Count ; Lymphocytes ; Lymphocytes - cytology ; Mycoses - immunology ; Mycoses - prevention & control ; Peptides ; Physiological aspects ; Population Density ; Regulation ; Survival Analysis ; Toads ; Zoological research</subject><ispartof>Nature (London), 2014-07, Vol.511 (7508), p.224-227</ispartof><rights>COPYRIGHT 2014 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Jul 10, 2014</rights><rights>2014 Macmillan Publishers Limited. All rights reserved 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c611t-4608dc5e3889d0ac46492046d28c32e66b059132e505b275968ca24f80e971633</citedby><cites>FETCH-LOGICAL-c611t-4608dc5e3889d0ac46492046d28c32e66b059132e505b275968ca24f80e971633</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,315,786,790,891,27957,27958</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25008531$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>McMahon, Taegan A</creatorcontrib><creatorcontrib>Sears, Brittany F</creatorcontrib><creatorcontrib>Venesky, Matthew D</creatorcontrib><creatorcontrib>Bessler, Scott M</creatorcontrib><creatorcontrib>Brown, Jenise M</creatorcontrib><creatorcontrib>Deutsch, Kaitlin</creatorcontrib><creatorcontrib>Halstead, Neal T</creatorcontrib><creatorcontrib>Lentz, Garrett</creatorcontrib><creatorcontrib>Tenouri, Nadia</creatorcontrib><creatorcontrib>Young, Suzanne</creatorcontrib><creatorcontrib>Civitello, David J</creatorcontrib><creatorcontrib>Ortega, Nicole</creatorcontrib><creatorcontrib>Fites, J Scott</creatorcontrib><creatorcontrib>Reinert, Laura K</creatorcontrib><creatorcontrib>Rollins-Smith, Louise A</creatorcontrib><creatorcontrib>Raffel, Thomas R</creatorcontrib><creatorcontrib>Rohr, Jason R</creatorcontrib><title>Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression</title><title>Nature (London)</title><addtitle>Nature</addtitle><description>Emerging fungal pathogens pose a greater threat to biodiversity than any other parasitic group, causing declines of many taxa, including bats, corals, bees, snakes and amphibians. Currently, there is little evidence that wild animals can acquire resistance to these pathogens. Batrachochytrium dendrobatidis is a pathogenic fungus implicated in the recent global decline of amphibians. Here we demonstrate that three species of amphibians can acquire behavioural or immunological resistance to B. dendrobatidis. Frogs learned to avoid the fungus after just one B. dendrobatidis exposure and temperature-induced clearance. In subsequent experiments in which B. dendrobatidis avoidance was prevented, the number of previous exposures was a negative predictor of B. dendrobatidis burden on frogs and B. dendrobatidis-induced mortality, and was a positive predictor of lymphocyte abundance and proliferation. These results suggest that amphibians can acquire immunity to B. dendrobatidis that overcomes pathogen-induced immunosuppression and increases their survival. Importantly, exposure to dead fungus induced a similar magnitude of acquired resistance as exposure to live fungus. Exposure of frogs to B. dendrobatidis antigens might offer a practical way to protect pathogen-naive amphibians and facilitate the reintroduction of amphibians to locations in the wild where B. dendrobatidis persists. Moreover, given the conserved nature of vertebrate immune responses to fungi and the fact that many animals are capable of learning to avoid natural enemies, these results offer hope that other wild animal taxa threatened by invasive fungi might be rescued by management approaches based on herd immunity.</description><subject>Amphibians</subject><subject>Amphibians - immunology</subject><subject>Amphibians - microbiology</subject><subject>Animal populations</subject><subject>Animals</subject><subject>Antigens, Fungal - immunology</subject><subject>Cell Proliferation</subject><subject>Chytridiomycota - immunology</subject><subject>Diseases</subject><subject>Experiments</subject><subject>Frogs</subject><subject>Fungi</subject><subject>Fungi, Pathogenic</subject><subject>Gene expression</subject><subject>Generalized linear models</subject><subject>Health aspects</subject><subject>Immune response</subject><subject>Immunology</subject><subject>Infections</subject><subject>Lymphocyte Count</subject><subject>Lymphocytes</subject><subject>Lymphocytes - cytology</subject><subject>Mycoses - immunology</subject><subject>Mycoses - prevention & control</subject><subject>Peptides</subject><subject>Physiological aspects</subject><subject>Population Density</subject><subject>Regulation</subject><subject>Survival Analysis</subject><subject>Toads</subject><subject>Zoological research</subject><issn>0028-0836</issn><issn>1476-4687</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><recordid>eNp10s2L1DAYB-AgijuunrxL0YsiXZMmTdKLMAx-LCwKuiKeQiZ9O5ulTTpJM-h_b0bXdUYqPaQkT375ehF6TPAZwVS-cnpKAQhlDbmDFoQJXjIuxV20wLiSJZaUn6AHMV5jjGsi2H10UtUYy5qSBfq2HMYru7baxUKbbbIBigDRxkk7A8Xki97uoNCuLVrQbdElt0mx8DsIxg_WbX716L6ww5Ccj2kc8_RovXuI7nW6j_Dopj1FX96-uVy9Ly8-vjtfLS9KwwmZ8laxbE0NVMqmxdowzpoKM95W0tAKOF_juiH5r8b1uhJ1w6XRFeskhkYQTukpev07d0zrAVoDbgq6V2Owgw4_lNdWHY84e6U2fqdYXkpIkgOe3wQEv00QJzXYaKDvtQOfoiI1Y4JKxptMn_1Dr30KLh9vr3i-30qKvyrfCyjrOp_XNftQtaSCY0EJZlmVM2oDDvImvYPO5u4j_3TGm9Fu1SE6m0H5a2GwZjb1xdGEbCb4Pm10ilGdf_50bF_-3y4vv64-zGoTfIwButsnIVjtC1cdFG7WTw5f8db-qVT6E5IA5Tc</recordid><startdate>20140710</startdate><enddate>20140710</enddate><creator>McMahon, Taegan A</creator><creator>Sears, Brittany F</creator><creator>Venesky, Matthew D</creator><creator>Bessler, Scott M</creator><creator>Brown, Jenise M</creator><creator>Deutsch, Kaitlin</creator><creator>Halstead, Neal T</creator><creator>Lentz, Garrett</creator><creator>Tenouri, Nadia</creator><creator>Young, Suzanne</creator><creator>Civitello, David J</creator><creator>Ortega, Nicole</creator><creator>Fites, J Scott</creator><creator>Reinert, Laura K</creator><creator>Rollins-Smith, Louise A</creator><creator>Raffel, Thomas R</creator><creator>Rohr, Jason R</creator><general>Nature Publishing Group</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>ATWCN</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>7T5</scope><scope>7TG</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88G</scope><scope>88I</scope><scope>8AF</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BEC</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>BKSAR</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M2O</scope><scope>M2P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>MBDVC</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PCBAR</scope><scope>PDBOC</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PSYQQ</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>Q9U</scope><scope>R05</scope><scope>RC3</scope><scope>S0X</scope><scope>SOI</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20140710</creationdate><title>Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression</title><author>McMahon, Taegan A ; Sears, Brittany F ; Venesky, Matthew D ; Bessler, Scott M ; Brown, Jenise M ; Deutsch, Kaitlin ; Halstead, Neal T ; Lentz, Garrett ; Tenouri, Nadia ; Young, Suzanne ; Civitello, David J ; Ortega, Nicole ; Fites, J Scott ; Reinert, Laura K ; Rollins-Smith, Louise A ; Raffel, Thomas R ; Rohr, Jason R</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c611t-4608dc5e3889d0ac46492046d28c32e66b059132e505b275968ca24f80e971633</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Amphibians</topic><topic>Amphibians - 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Currently, there is little evidence that wild animals can acquire resistance to these pathogens. Batrachochytrium dendrobatidis is a pathogenic fungus implicated in the recent global decline of amphibians. Here we demonstrate that three species of amphibians can acquire behavioural or immunological resistance to B. dendrobatidis. Frogs learned to avoid the fungus after just one B. dendrobatidis exposure and temperature-induced clearance. In subsequent experiments in which B. dendrobatidis avoidance was prevented, the number of previous exposures was a negative predictor of B. dendrobatidis burden on frogs and B. dendrobatidis-induced mortality, and was a positive predictor of lymphocyte abundance and proliferation. These results suggest that amphibians can acquire immunity to B. dendrobatidis that overcomes pathogen-induced immunosuppression and increases their survival. Importantly, exposure to dead fungus induced a similar magnitude of acquired resistance as exposure to live fungus. Exposure of frogs to B. dendrobatidis antigens might offer a practical way to protect pathogen-naive amphibians and facilitate the reintroduction of amphibians to locations in the wild where B. dendrobatidis persists. Moreover, given the conserved nature of vertebrate immune responses to fungi and the fact that many animals are capable of learning to avoid natural enemies, these results offer hope that other wild animal taxa threatened by invasive fungi might be rescued by management approaches based on herd immunity.</abstract><cop>England</cop><pub>Nature Publishing Group</pub><pmid>25008531</pmid><doi>10.1038/nature13491</doi><tpages>4</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Amphibians Amphibians - immunology Amphibians - microbiology Animal populations Animals Antigens, Fungal - immunology Cell Proliferation Chytridiomycota - immunology Diseases Experiments Frogs Fungi Fungi, Pathogenic Gene expression Generalized linear models Health aspects Immune response Immunology Infections Lymphocyte Count Lymphocytes Lymphocytes - cytology Mycoses - immunology Mycoses - prevention & control Peptides Physiological aspects Population Density Regulation Survival Analysis Toads Zoological research |
title | Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression |
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