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

2015 ◽  
Vol 282 (1805) ◽  
pp. 20142881 ◽  
Author(s):  
Matthew H. Becker ◽  
Jenifer B. Walke ◽  
Shawna Cikanek ◽  
Anna E. Savage ◽  
Nichole Mattheus ◽  
...  

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.

2018 ◽  
Vol 27 (Supplement) ◽  
pp. 81-90
Author(s):  
A.A. Cunningham

The unexplained decline of amphibian populations across the world was first recognised in the late 20th century. When investigated, most of these “enigmatic” declines have been shown to be due to one of two types of infectious disease: ranavirosis caused by infection with FV3-like ranavirus or with common midwife toad virus, or chytridiomycosis caused by infection with Batrachochytrium dendrobatidis or B. salamandrivorans. In all cases examined, infection has been via the human-mediated introduction of the pathogen to a species or population in which it has not naturally co-evolved. While ranaviruses and B. salamandrivorans have caused regionally localised amphibian population declines in Europe, the chytrid fungus, B. dendrobatidis, has caused catastrophic multi-species amphibian population declines and species extinctions globally. These diseases have already caused the loss of amphibian biodiversity, and over 40% of known amphibian species are threatened with extinction. If this biodiversity loss is to be halted, it is imperative that regulations are put in place – and enforced – to prevent the spread of known and yet-to-be discovered amphibian pathogens. Also, it is incumbent on those who keep or study amphibians to take measures to minimise the risk of disease spread, including from captive animals to those in the wild.


2019 ◽  
Vol 286 (1904) ◽  
pp. 20190833 ◽  
Author(s):  
Minjie Fu ◽  
Bruce Waldman

Many amphibian species around the world, except in Asia, suffer morbidity and mortality when infected by the emerging infectious pathogen Batrachochytrium dendrobatidis (Bd). A lineage of the amphibian chytrid fungus isolated from South Korean amphibians (BdAsia-1) is evolutionarily basal to recombinant global pandemic lineages (BdGPL) associated with worldwide amphibian population declines. In Asia, the Bd pathogen and its amphibian hosts have coevolved over 100 years or more. Thus, resilience of Asian amphibian populations to infection might result from attenuated virulence of endemic Bd lineages, evolved immunity to the pathogen or both. We compared susceptibilities of an Australasian amphibian, Litoria caerulea , known to lack resistance to BdGPL, with those of three Korean species, Bufo gargarizans , Bombina orientalis and Hyla japonica , after inoculation with BdAsia-1, BdGPL or a blank solution. Subjects became infected in all experimental treatments but Korean species rapidly cleared themselves of infection, regardless of Bd lineage. They survived with no apparent secondary effects. By contrast, L. caerulea , after infection by either BdAsia-1 or BdGPL, suffered deteriorating body condition and carried progressively higher Bd loads over time. Subsequently, most subjects died. Comparing their effects on L. caerulea , BdAsia-1 induced more rapid disease progression than BdGPL. The results suggest that genomic recombination with other lineages was not necessary for the ancestral Bd lineage to evolve hypervirulence over its long period of coevolution with amphibian hosts. The pathogen's virulence may have driven strong selection for immune responses in endemic Asian amphibian host species.


2017 ◽  
Vol 83 (9) ◽  
Author(s):  
Carly R. Muletz-Wolz ◽  
Graziella V. DiRenzo ◽  
Stephanie A. Yarwood ◽  
Evan H. Campbell Grant ◽  
Robert C. Fleischer ◽  
...  

ABSTRACT Diverse bacteria inhabit amphibian skin; some of those bacteria inhibit growth of the fungal pathogen Batrachochytrium dendrobatidis. Yet there has been no systematic survey of anti-B. dendrobatidis bacteria across localities, species, and elevations. This is important given geographic and taxonomic variations in amphibian susceptibility to B. dendrobatidis. Our collection sites were at locations within the Appalachian Mountains where previous sampling had indicated low B. dendrobatidis prevalence. We determined the numbers and identities of anti-B. dendrobatidis bacteria on 61 Plethodon salamanders (37 P. cinereus, 15 P. glutinosus, 9 P. cylindraceus) via culturing methods and 16S rRNA gene sequencing. We sampled co-occurring species at three localities and sampled P. cinereus along an elevational gradient (700 to 1,000 meters above sea level [masl]) at one locality. We identified 50 anti-B. dendrobatidis bacterial operational taxonomic units (OTUs) and found that the degree of B. dendrobatidis inhibition was not correlated with relatedness. Five anti-B. dendrobatidis bacterial strains occurred on multiple amphibian species at multiple localities, but none were shared among all species and localities. The prevalence of anti-B. dendrobatidis bacteria was higher at Shenandoah National Park (NP), VA, with 96% (25/26) of salamanders hosting at least one anti-B. dendrobatidis bacterial species compared to 50% (7/14) at Catoctin Mountain Park (MP), MD, and 38% (8/21) at Mt. Rogers National Recreation Area (NRA), VA. At the individual level, salamanders at Shenandoah NP had more anti-B. dendrobatidis bacteria per individual (μ = 3.3) than those at Catoctin MP (μ = 0.8) and at Mt. Rogers NRA (μ = 0.4). All salamanders tested negative for B. dendrobatidis. Anti-B. dendrobatidis bacterial species are diverse in central Appalachian Plethodon salamanders, and their distribution varied geographically. The antifungal bacterial species that we identified may play a protective role for these salamanders. IMPORTANCE Amphibians harbor skin bacteria that can kill an amphibian fungal pathogen, Batrachochytrium dendrobatidis. Some amphibians die from B. dendrobatidis infection, whereas others do not. The bacteria that can kill B. dendrobatidis, called anti-B. dendrobatidis bacteria, are thought to influence the B. dendrobatidis infection outcome for the amphibian. Yet how anti-B. dendrobatidis bacterial species vary among amphibian species and populations is unknown. We determined the distribution of anti-B. dendrobatidis bacterial species among three salamander species (n = 61) sampled at three localities. We identified 50 unique anti-B. dendrobatidis bacterial species and found that all of the tested salamanders were negative for B. dendrobatidis. Five anti-B. dendrobatidis bacterial species were commonly detected, suggesting a stable, functional association with these salamanders. The number of anti-B. dendrobatidis bacteria per individual varied among localities but not among co-occurring salamander species, demonstrating that environment is more influential than host factors in structuring the anti-B. dendrobatidis bacterial community. These anti-B. dendrobatidis bacteria may serve a protective function for their salamander hosts.


2021 ◽  
Author(s):  
Sara Meurling ◽  
Maria Cortazar-Chinarro ◽  
Mattias Siljestam ◽  
David Ahlen ◽  
Erik Agren ◽  
...  

Populations of the same species may differ in their sensitivity to pathogens but the factors behind this variation are poorly understood. Moreover, infections may cause sub-lethal fitness effects even in species resistant or tolerant to disease. The chytrid fungus Batrachochytrium dendrobatidis (Bd), is a generalist pathogen which has caused amphibian population declines worldwide. In many species, Bd infection causes the disease chytridiomycosis, often leading to high mortality. We investigated how geographical origin affects tolerance to Bd by exposing newly metamorphosed individuals of two North European amphibians (moor frog Rana arvalis, common toad Bufo bufo) from two latitudinal regions to two different BdGPL strains. Bd exposure strongly lowered survival in B. bufo, and in both species survival was lower in the northern region, this difference being much stronger in B. bufo. Northern individuals were smaller in both species, and the survival difference between the regions was size-mediated with smaller individuals being more sensitive to Bd. In both species, Bd exposure led to sub-lethal effects in terms of reduced growth suggesting that even individuals surviving the infection may have reduced fitness mediated by smaller body size. Bd strain affected size-dependent mortality differently in the two regions. We discuss the possible mechanisms how body size and geographical origin can contribute to the present results.


2018 ◽  
Author(s):  
Thomas L. Marshall ◽  
Carlos R. Baca ◽  
Decio T. Correa ◽  
Michael R. J. Forstner ◽  
Dittmar Hahn ◽  
...  

ABSTRACTChytridiomycosis, an emerging infectious disease caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), has caused amphibian population declines worldwide. Bd was first described in the 1990s and there are still geographic gaps in the genetic analysis of this globally distributed pathogen. Relatively few genetic studies have focused on regions where Bd exhibits low virulence, potentially creating a bias in our current knowledge of the pathogen’s genetic diversity. Disease-associated declines have not been recorded in Texas (USA), yet Bd has been detected on amphibians in the state. These strains have not been isolated and characterized genetically; therefore, we isolated, cultured, and genotyped Bd from central Texas and compared isolates to a panel of previously genotyped strains distributed across the Western Hemisphere. We also isolated other chytrids not known to infect amphibians from east Texas. To identify larval amphibian hosts, we sequenced part of the COI gene. Among 37 Bd isolates from Texas, we detected 19 unique multi-locus genotypes, but found no genetic structure associated with host species, Texas localities, or across North America. Isolates from central Texas exhibit high diversity and genetically cluster with Bd-GPL isolates from the western U.S. that have caused amphibian population declines. This study genetically characterizes isolates of Bd from the south central U.S. and adds to the global knowledge of Bd genotypes.


Author(s):  
Debra Patla ◽  
Charles Peterson

Declines and extinctions of many populations of amphibians have been noted worldwide in recent years (Corn and Fogelman 1984, Beiswenger 1986, McAllister and Leonard 1990, Wake and Morowitz 1990, Wake 1991, Adler 1992). Habitat modifications due to human activities may contribute to many of these declines. Habitat may be destroyed overtly, or it may be fragmented. Fragmentation results in reduced area, a differential loss of important habitat components, and increased isolation of populations (Wyman 1990). The persistence of amphibians in areas where modifications short of total habitat destruction occur depends on the preservation of essential habitat components and landscape connectivity that allows individual animals access to breeding, foraging, and wintering sites (Sinsch 1989). Long-term persistence also may rely on the immigration of individuals from other populations (Pechmann et al. 1991, Sjogren 1991). Our efforts to conserve amphibian species and to establish methods of sustainable resource use depend on our understanding of habitat fragmentation and knowledge of the behavioral and population responses to different types of habitat modifications (Gibbons 1988, Groom and Schumaker 1993). Few studies have addressed these types of questions. Notable exceptions include some studies on the effects of logging (Corn and Bury 1989) and acidification (Wyman and Hawksley-Lescault 1988, Harte and Hoffman 1989, Corn and Vertucci 1992). In Europe, researchers and wildlife conservationists are investigating the impacts of roads on amphibians and attempting to find solutions to fragmentation and mortality effects (Langton 1989), but this concern has not yet received noticeable attention in North America. We lack studies evaluating the relative importance and integration of foraging areas, hibernacula, breeding sites, areas occupied pre- and post-breeding, and dispersal routes connecting these areas. With these kinds of information, researchers and land managers will acquire the ability to better analyze, predict, and mitigate the effects of habitat modifications that are sources of amphibian population declines.


2016 ◽  
Vol 283 (1839) ◽  
pp. 20161553 ◽  
Author(s):  
Jordan G. Kueneman ◽  
Douglas C. Woodhams ◽  
Reid Harris ◽  
Holly M. Archer ◽  
Rob Knight ◽  
...  

Host-associated microbiomes perform many beneficial functions including resisting pathogens and training the immune system. Here, we show that amphibians developing in captivity lose substantial skin bacterial diversity, primarily due to reduced ongoing input from environmental sources. We combined studies of wild and captive amphibians with a database of over 1 000 strains that allows us to examine antifungal function of the skin microbiome. We tracked skin bacterial communities of 62 endangered boreal toads, Anaxyrus boreas , across 18 time points, four probiotic treatments, and two exposures to the lethal fungal pathogen Batrachochytrium dendrobatidis ( Bd ) in captivity, and compared these to 33 samples collected from wild populations at the same life stage. As the amphibians in captivity lost the Bd -inhibitory bacteria through time, the proportion of individuals exposed to Bd that became infected rose from 33% to 100% in subsequent exposures. Inoculations of the Bd -inhibitory probiotic Janthinobacterium lividum resulted in a 40% increase in survival during the second Bd challenge, indicating that the effect of microbiome depletion was reversible by restoring Bd -inhibitory bacteria. Taken together, this study highlights the functional role of ongoing environmental inputs of skin-associated bacteria in mitigating a devastating amphibian pathogen, and that long-term captivity decreases this defensive function.


2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Jaime Bosch ◽  
Camino Monsalve-Carcaño ◽  
Stephen J. Price ◽  
Jon Bielby

AbstractUnderstanding the occurrence and consequence of co-infections can be useful in designing disease management interventions. Amphibians are the most highly threatened vertebrates, and emerging pathogens are a serious threat to their conservation. The amphibian chytrid fungus and the viruses of the Ranavirus genus are already widely distributed, causing disease outbreaks and population declines worldwide. However, we lack information about the occurrence and consequences of coinfection with these pathogens across age-classes of amphibian hosts. Here, we analyze the occurrence of infection of the amphibian chytrid fungus and ranaviruses during one season in two susceptible amphibian species at two different locations at which outbreaks have occurred. We found that the co-occurrence of both pathogens in a particular host is not common except in highly susceptible life-stages, and that single infections are the most common situation. Moreover, we found that the occurrence of one pathogen in a particular host did not predict the occurrence of the other. We attribute these results to the niches in which both pathogens proliferate in amphibian hosts.


Molecules ◽  
2020 ◽  
Vol 25 (22) ◽  
pp. 5436
Author(s):  
Katelyn A. M. McMillan ◽  
Melanie R. Power Coombs

Host defense peptides (HDPs) are a group of antimicrobial peptides (AMPs) that are crucial components of the innate immune system of many different organisms. These small peptides actively kill microbes and prevent infection. Despite the presence of AMPs in the amphibian immune system, populations of these organisms are in decline globally. Magainin is an AMP derived from the African clawed frog (Xenopus laevis) and has displayed potent antimicrobial effects against a wide variety of microbes. Included in this group of microbes are known pathogens of the African clawed frog and other amphibian species. Arguably, the most deleterious amphibious pathogen is Batrachochytrium dendrobatidis, a chytrid fungus. Investigating the mechanism of action of magainin can help understand how to effectively fight off infection. By understanding amphibian AMPs’ role in the frog, a potential conservation strategy can be developed for other species of amphibians that are susceptible to infections, such as the North American green frog (Rana clamitans). Considering that population declines of these organisms are occurring globally, this effort is crucial to protect not only these organisms but the ecosystems they inhabit as well.


2021 ◽  
Vol 8 ◽  
Author(s):  
Mae Cowgill ◽  
Andrew G. Zink ◽  
Wesley Sparagon ◽  
Tiffany A. Yap ◽  
Hasan Sulaeman ◽  
...  

The emerging fungal pathogen, Batrachochytrium dendrobatidis (Bd), which can cause a fatal disease called chytridiomycosis, is implicated in the collapse of hundreds of host amphibian species. We describe chytridiomycosis dynamics in two co-occurring terrestrial salamander species, the Santa Lucia Mountains slender salamander, Batrachoseps luciae, and the arboreal salamander, Aneides lugubris. We (1) conduct a retrospective Bd-infection survey of specimens collected over the last century, (2) estimate present-day Bd infections in wild populations, (3) use generalized linear models (GLM) to identify biotic and abiotic correlates of infection risk, (4) investigate susceptibility of hosts exposed to Bd in laboratory trials, and (5) examine the ability of host skin bacteria to inhibit Bd in culture. Our historical survey of 2,866 specimens revealed that for most of the early 20th century (~1920–1969), Bd was not detected in either species. By the 1990s the proportion of infected specimens was 29 and 17% (B. luciae and A. lugubris, respectively), and in the 2010s it was 10 and 17%. This was similar to the number of infected samples from contemporary populations (2014–2015) at 10 and 18%. We found that both hosts experience signs of chytridiomycosis and suffered high Bd-caused mortality (88 and 71% for B. luciae and A. lugubris, respectively). Our GLM revealed that Bd-infection probability was positively correlated with intraspecific group size and proximity to heterospecifics but not to abiotic factors such as precipitation, minimum temperature, maximum temperature, mean temperature, and elevation, or to the size of the hosts. Finally, we found that both host species contain symbiotic skin-bacteria that inhibit growth of Bd in laboratory trials. Our results provide new evidence consistent with other studies showing a relatively recent Bd invasion of amphibian host populations in western North America and suggest that the spread of the pathogen may be enabled both through conspecific and heterospecific host interactions. Our results suggest that wildlife disease studies should assess host-pathogen dynamics that consider the interactions and effects of multiple hosts, as well as the historical context of pathogen invasion, establishment, and epizootic to enzootic transitions to better understand and predict disease dynamics.


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