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The pathogenic fungusBatrachochytrium dendrobatidis(Bd)is associated with drastic global amphibian declines. Prophylactic exposure to killed zoospores and the soluble chemicals they produce (Bdmetabolites) can induce acquired resistance toBdin adult Cuban treefrogsOsteopilus septentrionalis. Here, we exposed metamorphic frogs of a second species, the Pacific chorus frogPseudacris regilla, to one of 2 prophylactic treatments prior to liveBdexposures: killedBdzoospores with metabolites, killed zoospores alone, or a water control. Prior exposure to killedBdzoospores with metabolites reducedBdinfection intensity in metamorphic Pacific chorus frogs by 60.4% compared to control frogs. Interestingly,Bdintensity in metamorphs previously exposed to killed zoospores alone did not differ in magnitude relative to the control metamorphs, nor to those treated with killed zoospores plus metabolites. Previous work indicated thatBdmetabolites alone can induce acquired resistance in tadpoles, and so these findings together indicate that it is possible that the solubleBdmetabolites may contain immunomodulatory components that drive this resistance phenotype. Our results expand the generality of this prophylaxis work by identifying a second amphibian species (Pacific chorus frog) and an additional amphibian life stage (metamorphic frog) that can acquire resistance toBdafter metabolite exposure. This work increases hopes that aBd-metabolite prophylaxis might be widely effective across amphibian species and life stages.
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Asymmetric cross-strain protection for amphibians exposed to a fungal-metabolite prophylactic treatment
Chytridiomycosis, an infectious disease of amphibians caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), poses an imminent conservation threat. The global spread of Bd has led to mass mortality events in many amphibian species, resulting in at least 90 species' extinctions to date. Exposure to Bd metabolites (i.e. non-infectious antigenic chemicals released by Bd) partially protects frogs during subsequent challenges with live Bd, suggesting its use as a prophylactic treatment and potential vaccine. However, we do not know whether Bd metabolite exposure protects against strains beyond the one used for treatment. To address this knowledge gap, we conducted a 3 × 2 experiment where we exposed adult Cuban treefrogs, Osteopilus septentrionalis , to one of three treatments (Bd metabolites from California-isolated strain JEL-270, Panamá-isolated strain JEL-419, or an artificial spring water control) and then challenged individuals with live Bd from either strain. We found that exposure to Bd metabolites from the California-isolated strain significantly reduced Bd loads of frogs challenged with the live Panamá-isolated strain, but no other treatments were found to confer protective effects. These findings demonstrate asymmetric cross-protection of a Bd metabolite prophylaxis and suggest that work investigating multiple, diverse strains is urgently needed.
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- PAR ID:
- 10294044
- Date Published:
- Journal Name:
- Biology Letters
- Volume:
- 17
- Issue:
- 8
- ISSN:
- 1744-957X
- Page Range / eLocation ID:
- 20210207
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Batrachochytrium dendrobatidis(Bd), an aquatic pathogenic fungus, is responsible for the decline of hundreds of amphibian species worldwide and negatively impacts biodiversity globally. Prophylactic exposure to the metabolites produced by Bd can provide protection for naïve tree frogs and reduce subsequent Bd infection intensity.Here, we used a response surface design crossing Bd metabolite prophylaxis concentration and exposure duration to determine how these factors modulate prophylactic protection against Bd in Pacific chorus frog (Pseudacris regilla) tadpoles (5 × 5 surface design) and metamorphs (3 × 3 surface design). We exposed individuals every weekday to one of five Bd metabolite concentrations or a water control for 1–5 weeks, after which all animals were challenged with live Bd to evaluate their susceptibility.Exposure to the Bd metabolite prophylaxis reduced Bd load and prevalence compared to the control for both the tadpoles and metamorphs. Increasing Bd metabolite prophylaxis concentration did not confer additional protection for either life stage, but increasing duration of exposure did benefit metamorphs by decreasing Bd prevalence but not Bd load.On average, control tadpoles and metamorphs had 66.2% and 99.4% higher Bd loads, respectively, than tadpoles and metamorphs exposed to any Bd metabolite prophylaxis.Additionally, Bd metabolite prophylaxis reduced Bd prevalence relative to controls in both tadpoles (20.5% vs. 56.3%, respectively) and metamorphs (21.9% vs. 87.5%, respectively).Synthesis and applications: The efficacy of short‐term exposures of relatively low concentrations of Bd metabolites at reducing Bd infections suggests that this approach has the potential to be scaled up to field use to aid in disease mitigation and conservation. Our results, combined with additional research on Bd metabolite prophylaxis for other amphibian species, suggest that this strategy may represent a broadly useful tool to protect at‐risk amphibian populations.more » « less
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Abstract To combat the loss of species due to emerging infectious diseases, scientists must incorporate ecological parameters, such as temperature and humidity, to understand how the environment affects host–pathogen interactions. The fungal disease chytridiomycosis is a compelling case study to investigate the role of both temperature and humidity on infectious disease, as both the fungal pathogen (Batrachochytrium dendrobatidis, Bd) and the host (amphibians) are heavily influenced by these abiotic factors. We performed two experiments to investigate the importance of relative humidity and temperature on frog immunity (production of antimicrobial skin secretions) and disease development in captive golden frogs (Atelopus zeteki) of Panama. We found that the quantity of skin secretions significantly decreased over time in frogs moved from low to medium and high relative humidity treatments. FollowingBdexposure, frogs in high temperature (26–27 °C) and high relative humidity (80–90%) had lower pathogen loads and survived significantly longer than frogs kept in all other treatment conditions, including high temperature and low relative humidity. These results suggest that high relative humidity may be an important, although less understood, mediator ofBdinfection and the survival of golden frogs. Because the environment can drastically alter disease dynamics, understanding how temperature and humidity influence chytridiomycosis outcomes in golden frogs may be essential for the success of the reintroduction of captive frogs.more » « less
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Abstract Batrachochytrium dendrobatidis(Bd) has been associated with massive amphibian population declines worldwide. Wildlife vaccination campaigns have proven effective for mitigating damage from other pathogens, and there is evidence that adult frogs can acquire resistance to Bd when exposed to killed Bd zoospores and the metabolites they produced.Here, we investigated whether Cuban treefrogs tadpolesOsteopilus septentrionaliscan gain protection from Bd through exposure to a prophylaxis treatment composed of killed zoospores or soluble Bd metabolites. We used a 2 × 2 factorial design, crossing the presence or absence of killed zoospores with the presence or absence of Bd metabolites. All hosts were subsequently exposed to live Bd to evaluate susceptibility.Exposure to killed zoospores did not induce a protective response. However, tadpoles exposed to Bd metabolites had significantly lower Bd intensity and prevalence than tadpoles that were not exposed to metabolites.The metabolites Bd produce pose no risk of Bd infection and therefore make an epidemiologically safe prophylaxis treatment, protecting tadpoles against Bd. This work provides a promising potential for protecting amphibians in the wild as a disease management strategy for controlling Bd‐associated declines.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rsbl.2021.0207
