ALBERT

Description: The amphibian-killing chytrid fungus Batrachochytrium dendrobatidis ( Bd ) is one of the most generalist pathogens known, capable of infecting hundreds of species globally and causing widespread population declines and extinctions. However, some host species are seemingly unaffected by Bd , tolerating or clearing infections without clinical signs of disease. Variation in host immune responses is commonly evoked for these resistant or tolerant species, yet to date, we have no direct comparison of amphibian species responses to infection at the level of gene expression. In this study, we challenged four Central American frog species that vary in Bd susceptibility, with a sympatric virulent strain of the pathogen. We compared skin and spleen orthologous gene expression using differential expression tests and coexpression gene network analyses. We found that resistant species have reduced skin inflammatory responses and increased expression of genes involved in skin integrity. In contrast, only highly susceptible species exhibited suppression of splenic T-cell genes. We conclude that resistance to chytridiomycosis may be related to a species’ ability to escape the immunosuppressive activity of the fungus. Moreover, our results indicate that within-species differences in splenic proteolytic enzyme gene expression may contribute to intraspecific variation in survival. This first comparison of amphibian functional immunogenomic architecture in response to Bd provides insights into key genetic mechanisms underlying variation in disease outcomes among amphibian species.

Description: The emergence of the disease chytridiomycosis caused by the chytrid fungus Batrachochytrium dendrobatidis ( Bd ) has been implicated in dramatic global amphibian declines. Although many species have undergone catastrophic declines and/or extinctions, others appear to be unaffected or persist at reduced frequencies after Bd outbreaks. The reasons behind this variance in disease outcomes are poorly understood: differences in host immune responses have been proposed, yet previous studies suggest a lack of robust immune responses to Bd in susceptible species. Here, we sequenced transcriptomes from clutch-mates of a highly susceptible amphibian, Atelopus zeteki , with different infection histories. We found significant changes in expression of numerous genes involved in innate and inflammatory responses in infected frogs despite high susceptibility to chytridiomycosis. We show evidence of acquired immune responses generated against Bd , including increased expression of immunoglobulins and major histocompatibility complex genes. In addition, fungal-killing genes had significantly greater expression in frogs previously exposed to Bd compared with Bd -naïve frogs, including chitinase and serine-type proteases. However, our results appear to confirm recent in vitro evidence of immune suppression by Bd , demonstrated by decreased expression of lymphocyte genes in the spleen of infected compared with control frogs. We propose susceptibility to chytridiomycosis is not due to lack of Bd -specific immune responses but instead is caused by failure of those responses to be effective. Ineffective immune pathway activation and timing of antibody production are discussed as potential mechanisms. However, in light of our findings, suppression of key immune responses by Bd is likely an important factor in the lethality of this fungus.

Description: For generalist pathogens, host species represent distinct selective environments, providing unique challenges for resource acquisition and defense from host immunity, potentially resulting in host-dependent differences in pathogen fitness. Gene expression modulation should be advantageous, responding optimally to a given host and mitigating the costs of generalism. Batrachochytrium dendrobatidis ( Bd ), a fungal pathogen of amphibians, shows variability in pathogenicity among isolates, and within-strain virulence changes rapidly during serial passages through artificial culture. For the first time, we characterize the transcriptomic profile of Bd in vivo , using laser-capture microdissection. Comparison of Bd transcriptomes (strain JEL423) in culture and in two hosts ( Atelopus zeteki and Hylomantis lemur ), reveals 〉2000 differentially expressed genes that likely include key Bd defense and host exploitation mechanisms. Variation in Bd transcriptomes from different amphibian hosts demonstrates shifts in pathogen resource allocation. Furthermore, expressed genotype variant frequencies of Bd populations differ between culture and amphibian skin, and among host species, revealing potential mechanisms underlying rapid changes in virulence and the possibility that amphibian community composition shapes Bd evolutionary trajectories. Our results provide new insights into how changes in gene expression and infecting population genotypes can be key to the success of a generalist fungal pathogen.

Description: 〈br /〉〈span class="detail_caption"〉Notes: 〈/span〉Becker, C Guilherme -- Rodriguez, David -- Zamudio, Kelly R -- New York, N.Y. -- Science. 2013 Apr 26;340(6131):428. doi: 10.1126/science.340.6131.428-a.〈br /〉〈span class="detail_caption"〉Record origin:〈/span〉 〈a href="http://www.ncbi.nlm.nih.gov/pubmed/23620033" target="_blank"〉PubMed〈/a〉

Description: Emerging infectious diseases are reducing biodiversity on a global scale. Recently, the emergence of the chytrid fungus Batrachochytrium salamandrivorans resulted in rapid declines in populations of European fire salamanders. Here, we screened more than 5000 amphibians from across four continents and combined experimental assessment of pathogenicity with phylogenetic methods to estimate the threat that this infection poses to amphibian diversity. Results show that B. salamandrivorans is restricted to, but highly pathogenic for, salamanders and newts (Urodela). The pathogen likely originated and remained in coexistence with a clade of salamander hosts for millions of years in Asia. As a result of globalization and lack of biosecurity, it has recently been introduced into naive European amphibian populations, where it is currently causing biodiversity loss.〈br /〉〈span class="detail_caption"〉Notes: 〈/span〉Martel, A -- Blooi, M -- Adriaensen, C -- Van Rooij, P -- Beukema, W -- Fisher, M C -- Farrer, R A -- Schmidt, B R -- Tobler, U -- Goka, K -- Lips, K R -- Muletz, C -- Zamudio, K R -- Bosch, J -- Lotters, S -- Wombwell, E -- Garner, T W J -- Cunningham, A A -- Spitzen-van der Sluijs, A -- Salvidio, S -- Ducatelle, R -- Nishikawa, K -- Nguyen, T T -- Kolby, J E -- Van Bocxlaer, I -- Bossuyt, F -- Pasmans, F -- Wellcome Trust/United Kingdom -- New York, N.Y. -- Science. 2014 Oct 31;346(6209):630-1. doi: 10.1126/science.1258268.〈br /〉〈span class="detail_caption"〉Author address: 〈/span〉Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium. an.martel@ugent.be. ; Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium. Centre for Research and Conservation, Royal Zoological Society of Antwerp, Koningin Astridplein 26, Antwerp, Belgium. ; Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium. ; CIBIO/InBIO, Centro de Investigacao em Biodiversidade e Recursos Geneticos da Universidade do Porto, Instituto de Ciencias Agrarias de Vairao, Rua Padre Armando Quintas, Vairao, Portugal. ; Department of Infectious Disease Epidemiology, Imperial College London, Norfolk Place, London W2 1PG, UK. ; Genome Sequencing and Analysis Program, The Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA. ; Koordinationsstelle fur amphibien- und reptilienschutz in der Schweiz (KARCH), Passage Maximilien-de-Meuron 6, 2000 Neuchatel, Switzerland. Institut fur Evolutionsbiologie und Umweltwissenschaften, Universitat Zurich. Winterthurerstrasse 190, 8057 Zurich, Switzerland. ; Invasive Alien Species Research Team, National Institute for Environment Studies, 16-2 Onogawa, Tsukuba, Ibaraki 305-8506, Japan. ; Department of Biology, University of Maryland, College Park, MD 20742, USA. ; Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY 14853, USA. ; Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones cientificas (CSIC), Jose Gutierrez Abascal 2, 28006 Madrid, Spain. ; Biogeography Department, Trier University, 54286 Trier, Germany. ; Durrell Institute of Conservation and Ecology, University of Kent, Kent CT2 7NR, UK. Institute of Zoology, Zoological Society of London, London NW1 4RY, UK. ; Institute of Zoology, Zoological Society of London, London NW1 4RY, UK. ; Reptile, Amphibian and Fish Conservation the Netherlands (RAVON), Post Office Box 1413, 6501 BK Nijmegen, Netherlands. ; Department of Earth Science, Environmental and Life (Di.S.T.A.V.), University of Genova, Corso Europa 26, I-16132 Genova, Italy. ; Graduate School of Human and Environmental Studies, Kyoto University, Yoshida Nihonmatsu-cho, Sakyo-ku, Kyoto 606-8501, Japan. ; Vietnam National Museum of Nature, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Cau Giay, Hanoi, Vietnam. ; James Cook University, One Health Research Group, School of Public Health, Tropical Medicine and Rehabilitation Sciences, Townsville, Queensland, Australia. ; Amphibian Evolution Lab, Biology Department, Vrije Universiteit Brussel, Pleinlaan 2, 1050 Brussels, Belgium.〈br /〉〈span class="detail_caption"〉Record origin:〈/span〉 〈a href="http://www.ncbi.nlm.nih.gov/pubmed/25359973" target="_blank"〉PubMed〈/a〉

Description: Almost 30 y ago, the field of intraspecific phylogeography laid the foundation for spatially explicit and genealogically informed studies of population divergence. With new methods and markers, the focus in phylogeography shifted to previously unrecognized geographic genetic variation, thus reducing the attention paid to phenotypic variation in those same diverging...

Description: Habitat loss and disease are main drivers of global amphibian declines, yet the interaction between them remains largely unexplored. Here we show that paradoxically, habitat loss is negatively associated with occurrence, prevalence, and infection intensity of the chytrid fungus Batrachochytrium dendrobatidis (Bd) in amphibian populations in the tropics. At a large spatial scale, increased habitat loss predicted lower disease risk in amphibian populations across Costa Rica and eastern Australia, even after jointly considering the effect of potential biotic and abiotic correlates. Lower host-species richness and suboptimal microclimates for Bd in disturbed habitats are potential mechanisms underlying this pattern. Furthermore, we found that anthropogenic deforestation practices biased to lowlands and natural vegetation remaining in inaccessible highlands explain increased Bd occurrence at higher elevations. At a smaller spatial scale, holding constant elevation, latitude, and macroclimate, we also found a negative relationship between habitat loss, and both Bd prevalence and infection intensity in frog populations in two landscapes of the Brazilian Atlantic Forest. Our results indicate that amphibians will be disproportionately affected by emerging diseases in pristine environments, and that, paradoxically, disturbed habitats may act as shelters from disease, but only for the very few species that can tolerate deforestation. Thus, tropical amphibian faunas are threatened both by destruction of natural habitats as well as increased disease in pristine forests. To curb further extinctions and develop effective mitigation and restoration programs we must look to interactions between habitat loss and disease, the two main factors at the root of global amphibian declines.