The pathogen<i>Batrachochytrium dendrobatidis</i>disturbs the frog skin microbiome during a natural epidemic and experimental infection

Jani, Andrea J.; Briggs, Cheryl J.

doi:10.1073/pnas.1412752111

Cited by 227 publications

(316 citation statements)

References 77 publications

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“…This suggests that A. zeteki microbial communities are at least somewhat resistant and/or resilient to invasion. This is contrary to a recent study that found the cutaneous bacterial community structure of Rana sierrae was affected by the presence of Bd and its density on the frog [57].…”

Section: Discussioncontrasting

confidence: 99%

“…These OTUs may have facilitated the colonization and growth of Bd or may have been opportunistic pathogens. In addition, the relative abundance of these OTUs may have increased because Bd was able to negatively affect the abundance of other OTUs [57]. Facilitation of Bd growth and colonization could occur either when symbiotic bacteria shift their metabolite profiles in a way that favours Bd [35] or by reducing the capability of other microbes to inhibit Bd.…”

Section: Discussionmentioning

confidence: 99%

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Composition of symbiotic bacteria predicts survival in Panamanian golden frogs infected with a lethal fungus

et al. 2015

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Symbiotic microbes can dramatically impact host health and fitness, and recent research in a diversity of systems suggests that different symbiont community structures may result in distinct outcomes for the host. In amphibians, some symbiotic skin bacteria produce metabolites that inhibit the growth of Batrachochytrium dendrobatidis (Bd), a cutaneous fungal pathogen that has caused many amphibian population declines and extinctions. Treatment with beneficial bacteria (probiotics) prevents Bd infection in some amphibian species and creates optimism for conservation of species that are highly susceptible to chytridiomycosis, the disease caused by Bd. In a laboratory experiment, we used Bd-inhibitory bacteria from Bd-tolerant Panamanian amphibians in a probiotic development trial with Panamanian golden frogs, Atelopus zeteki, a species currently surviving only in captive assurance colonies. Approximately 30% of infected golden frogs survived Bd exposure by either clearing infection or maintaining low Bd loads, but this was not associated with probiotic treatment. Survival was instead related to initial composition of the skin bacterial community and metabolites present on the skin. These results suggest a strong link between the structure of these symbiotic microbial communities and amphibian host health in the face of Bd exposure and also suggest a new approach for developing amphibian probiotics.

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Section: Discussioncontrasting

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Composition of symbiotic bacteria predicts survival in Panamanian golden frogs infected with a lethal fungus

et al. 2015

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“…Our knowledge of amphibian skin microbiomes is rapidly increasing (Jani and Briggs, 2014;Kueneman et al, 2014;Walke et al, 2014). Exploring skin bacterial communities across different amphibian developmental stages and the defensive functions those microbes play, particularly prior to the development of the adaptive immune function, is an important and understudied area.…”

Section: Discussionmentioning

confidence: 99%

“…Molecular methods for investigating microeukaryotes are just emerging, allowing us to further consider the role of nonbacterial microbes on the skin. In addition, there are few next-generation microbial data sets that compare Bd-positive and Bd-negative sites (Jani and Briggs, 2014). Within this study we begin to fill these knowledge gaps including describing A. boreas skin communities across developmental stages from Bd-positive and -negative sites across the host range in Colorado; surveying microeukaryotes from amphibians utilizing high throughput sequencing; and providing the first application of a cultureindependent database of known and expected Bd-inhibitory isolates.…”

Section: Discussionmentioning

confidence: 99%

Inhibitory bacteria reduce fungi on early life stages of endangered Colorado boreal toads (Anaxyrus boreas)

et al. 2015

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Increasingly, host-associated microbiota are recognized to mediate pathogen establishment, providing new ecological perspectives on health and disease. Amphibian skin-associated microbiota interact with the fungal pathogen, Batrachochytrium dendrobatidis (Bd), but little is known about microbial turnover during host development and associations with host immune function. We surveyed skin microbiota of Colorado's endangered boreal toads (Anaxyrus boreas), sampling 181 toads across four life stages (tadpoles, metamorphs, subadults and adults). Our goals were to (1) understand variation in microbial community structure among individuals and sites, (2) characterize shifts in communities during development and (3) examine the prevalence and abundance of known Bd-inhibitory bacteria. We used high-throughput 16S and 18S rRNA gene sequencing (Illumina MiSeq) to characterize bacteria and microeukaryotes, respectively. Life stage had the largest effect on the toad skin microbial community, and site and Bd presence also contributed. Proteobacteria dominated tadpole microbial communities, but were later replaced by Actinobacteria. Microeukaryotes on tadpoles were dominated by the classes Alveolata and Stramenopiles, while fungal groups replaced these groups after metamorphosis. Using a novel database of Bd-inhibitory bacteria, we found fewer Bd-inhibitory bacteria in post-metamorphic stages correlated with increased skin fungi, suggesting that bacteria have a strong role in early developmental stages and reduce skinassociated fungi.

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“…In Rana sierrae, a high elevation species that has experienced significant Bd-driven declines in North America, Bd infection resulted in the disturbance of skin bacterial communities in both wild and captive amphibians (Jani & Briggs 2014). However, in populations in which Bd had become enzootic, skin bacterial populations appeared to remain relatively stable with changes in Bd infection intensity, although the sample size was too small to make conclusions (Jani & Briggs 2014). Skin bacterial community diversity has also been found to be lower in populations of a susceptible Panamanian frog species where Bd has become endemic (Rebollar et al 2016).…”

Section: How Does Sloughing Interact With Bd and The Frog Skin Microbmentioning

confidence: 99%

Interactions between amphibian skin sloughing and a cutaneous fungal disease: infection progression, immune defence, and phylogenetic patterns

Ohmer¹

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Worldwide, there has been an unprecedented rise in emerging infectious diseases of wildlife, and this has contributed to a widespread biodiversity crisis. Amphibian populations, in particular, are threatened by the fungal pathogen Batrachochytrium dendrobatidis (Bd), which in post-metamorphic animals only infects the skin, and causes the potentially lethal disease chytridiomycosis. Amphibians regularly slough their skin, and in doing so remove many skinassociated microbes. Thus, skin sloughing may play an important role in the pathogenesis of chytridiomycosis. To investigate this association, the influence of Bd infection on amphibian skin sloughing, and the role of sloughing in regulating infection, was examined. Furthermore, to better understand the variation in skin sloughing rates across species and ecological groups, and make inferences about the role of this process in susceptibility to this fungal disease, amphibian skin structure and function was investigated within a phylogenetic context. To determine the relationship between skin sloughing and disease progression (chapter 2), adult green tree frogs (Litoria caerulea) were exposed to an Australian Bd strain, and sloughing rates and infection load were monitored on a naturalistic cycling temperature regime (15 -23˚C).Sloughing rates were determined by filming frogs and infection intensity was monitored before and after sloughing with conventional swabbing and quantitative PCR. Sloughing rate was found to increase with Bd infection load in infected frogs, but sloughing itself did not affect Bd load on the ventral skin surface. Although a faster sloughing rate might be considered advantageous for Bdinfected animals, it does not appear to curb the progression of disease in susceptible species. In fact, sloughing may actually contribute to the loss of physiological homeostasis seen in terminally ill frogs by further inhibiting water and electrolyte transport across the skin.In some species less susceptible to chytridiomycosis, it has been demonstrated that Bd growth remains epibiotic, without penetrating the underlying epidermal layers. Therefore, sloughing may more effectively remove Bd zoospores in less susceptible species (chapter 3). To test this hypothesis, five Australian frog species, Lit. caerulea, Platyplectrum ornatum, Lechriodus fletcheri, Limnodynastes peronii, and Lim. tasmaniensis, were exposed to an Australian Bd strain, and their sloughing rates and infection loads monitored over time. Utilising an improved methodology to remove any artefacts from the swabbing itself, sloughing was found to reduce Bd load on the ventral skin surface, in all five species, despite wide ranging variation in susceptibility to Bd infection and subsequent disease. In less susceptible species, sloughing reduced Bd load up to 100%, leading to infection clearance. However, the drop in Bd load was only temporary in susceptible species, potentially due to the invasive growth of Bd in skin layers underlying the ii stratum corneum in these species. If less suscept...

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The pathogenBatrachochytrium dendrobatidisdisturbs the frog skin microbiome during a natural epidemic and experimental infection

Cited by 227 publications

References 77 publications

Composition of symbiotic bacteria predicts survival in Panamanian golden frogs infected with a lethal fungus

Composition of symbiotic bacteria predicts survival in Panamanian golden frogs infected with a lethal fungus

Inhibitory bacteria reduce fungi on early life stages of endangered Colorado boreal toads (Anaxyrus boreas)

Interactions between amphibian skin sloughing and a cutaneous fungal disease: infection progression, immune defence, and phylogenetic patterns

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