scholarly journals Epidermal galactose spurs chytrid virulence and predicts amphibian colonization

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Yu Wang ◽  
Elin Verbrugghe ◽  
Leander Meuris ◽  
Koen Chiers ◽  
Moira Kelly ◽  
...  
Keyword(s):  
Disease Ecology ◽  
Fungal Pathogens ◽  
Batrachochytrium Dendrobatidis ◽  
Host Susceptibility ◽  
Fungal Colonization ◽  
Amphibian Skin ◽  
Glycosylation Pattern ◽  
Amphibian Species ◽  
Juvenile Mortality ◽  
Galactose Content

AbstractThe chytrid fungal pathogens Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans cause the skin disease chytridiomycosis in amphibians, which is driving a substantial proportion of an entire vertebrate class to extinction. Mitigation of its impact is largely unsuccessful and requires a thorough understanding of the mechanisms underpinning the disease ecology. By identifying skin factors that mediate key events during the early interaction with B. salamandrivorans zoospores, we discovered a marker for host colonization. Amphibian skin associated beta-galactose mediated fungal chemotaxis and adhesion to the skin and initiated a virulent fungal response. Fungal colonization correlated with the skin glycosylation pattern, with cutaneous galactose content effectively predicting variation in host susceptibility to fungal colonization between amphibian species. Ontogenetic galactose patterns correlated with low level and asymptomatic infections in salamander larvae that were carried over through metamorphosis, resulting in juvenile mortality. Pronounced variation of galactose content within some, but not all species, may promote the selection for more colonization resistant host lineages, opening new avenues for disease mitigation.

scholarly journals Phylogenetic investigation of skin sloughing rates in frogs: relationships with skin characteristics and disease-driven declines

2019 ◽  
Vol 286 (1896) ◽  
pp. 20182378 ◽  
Author(s):  
Michel E. B. Ohmer ◽  
Rebecca L. Cramp ◽  
Craig R. White ◽  
Peter S. Harlow ◽  
Michael S. McFadden ◽  
...  
Keyword(s):  
Batrachochytrium Dendrobatidis ◽  
Phylogenetic Signal ◽  
Interspecific Variation ◽  
Phylogenetic Position ◽  
Turnover Rates ◽  
Amphibian Skin ◽  
Amphibian Species ◽  
Wide Range ◽  
Skin Morphology ◽  
And Function

Amphibian skin is highly variable in structure and function across anurans, and plays an important role in physiological homeostasis and immune defence. For example, skin sloughing has been shown to reduce pathogen loads on the skin, such as the lethal fungus Batrachochytrium dendrobatidis ( Bd ), but interspecific variation in sloughing frequency is largely unknown. Using phylogenetic linear mixed models, we assessed the relationship between skin turnover rate, skin morphology, ecological traits and overall evidence of Bd -driven declines. We examined skin sloughing rates in 21 frog species from three continents, as well as structural skin characteristics measured from preserved specimens. We found that sloughing rate varies significantly with phylogenetic group, but was not associated with evidence of Bd -driven declines, or other skin characteristics examined. This is the first comparison of sloughing rate across a wide range of amphibian species, and creates the first database of amphibian sloughing behaviour. Given the strong phylogenetic signal observed in sloughing rate, approximate sloughing rates of related species may be predicted based on phylogenetic position. While not related to available evidence of declines, understanding variation in sloughing rate may help explain differences in the severity of infection in genera with relatively slow skin turnover rates (e.g. Atelopus ).

scholarly journals Antifungal Bacteria on Woodland Salamander Skin Exhibit High Taxonomic Diversity and Geographic Variability

2017 ◽  
Vol 83 (9) ◽  
Author(s):  
Carly R. Muletz-Wolz ◽  
Graziella V. DiRenzo ◽  
Stephanie A. Yarwood ◽  
Evan H. Campbell Grant ◽  
Robert C. Fleischer ◽  
...  
Keyword(s):  
Fungal Pathogen ◽  
Batrachochytrium Dendrobatidis ◽  
Bacterial Species ◽  
Rrna Gene ◽  
Amphibian Skin ◽  
Amphibian Species ◽  
Protective Function ◽  
Content Type ◽  
Skin Bacteria ◽  
Salamander Species

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.

scholarly journals Bioclimatic and anthropogenic variables shape the occurrence of Batrachochytrium dendrobatidis over a large latitudinal gradient

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Mario Alvarado-Rybak ◽  
Manuel Lepe-Lopez ◽  
Alexandra Peñafiel-Ricaurte ◽  
Andrés Valenzuela-Sánchez ◽  
Catalina Valdivia ◽  
...  
Keyword(s):  
Latitudinal Gradient ◽  
Batrachochytrium Dendrobatidis ◽  
Biodiversity Loss ◽  
Quantitative Real Time Pcr ◽  
Amphibian Skin ◽  
Amphibian Species ◽  
Risk Areas ◽  
Host Ecology ◽  
New Evidence ◽  
Central South

AbstractAmphibian chytridiomycosis, caused by the fungus Batrachochytrium dendrobatidis (Bd), has caused the greatest known loss of biodiversity due to an infectious disease. We used Bd infection data from quantitative real-time PCR (qPCR) assays of amphibian skin swabs collected across Chile during 2008–2018 to model Bd occurrence with the aim to determine bioclimatic and anthropogenic variables associated with Bd infection. Also, we used Bd presence/absence records to identify geographical Bd high-risk areas and compare Bd prevalence and infection loads between amphibian families, ecoregions, and host ecology. Data comprised 4155 Bd-specific qPCR assays from 162 locations across a latitudinal gradient of 3700 km (18º to 51ºS). Results showed a significant clustering of Bd associated with urban centres and anthropogenically highly disturbed ecosystems in central-south Chile. Both Bd prevalence and Bd infection loads were higher in aquatic than terrestrial amphibian species. Our model indicated positive associations of Bd prevalence with altitude, temperature, precipitation and human-modified landscapes. Also, we found that macroscale drivers, such as land use change and climate, shape the occurrence of Bd at the landscape level. Our study provides with new evidence that can improve the effectiveness of strategies to mitigate biodiversity loss due to amphibian chytridiomycosis.

scholarly journals Most of the Dominant Members of Amphibian Skin Bacterial Communities Can Be Readily Cultured

2015 ◽  
Vol 81 (19) ◽  
pp. 6589-6600 ◽  
Author(s):  
Jenifer B. Walke ◽  
Matthew H. Becker ◽  
Myra C. Hughey ◽  
Meredith C. Swartwout ◽  
Roderick V. Jensen ◽  
...  
Keyword(s):  
Bacterial Community ◽  
Batrachochytrium Dendrobatidis ◽  
Amplicon Sequencing ◽  
Reference Database ◽  
Rrna Gene ◽  
Amphibian Skin ◽  
Amphibian Species ◽  
Content Type ◽  
Average Percentage ◽  
Culture Independent

ABSTRACTCurrently, it is estimated that only 0.001% to 15% of bacteria in any given system can be cultured by use of commonly used techniques and media, yet culturing is critically important for investigations of bacterial function. Despite this situation, few studies have attempted to link culture-dependent and culture-independent data for a single system to better understand which members of the microbial community are readily cultured. In amphibians, some cutaneous bacterial symbionts can inhibit establishment and growth of the fungal pathogenBatrachochytrium dendrobatidis, and thus there is great interest in using these symbionts as probiotics for the conservation of amphibians threatened byB. dendrobatidis. The present study examined the portion of the culture-independent bacterial community (based on Illumina amplicon sequencing of the 16S rRNA gene) that was cultured with R2A low-nutrient agar and whether the cultured bacteria represented rare or dominant members of the community in the following four amphibian species: bullfrogs (Lithobates catesbeianus), eastern newts (Notophthalmus viridescens), spring peepers (Pseudacris crucifer), and American toads (Anaxyrus americanus). To determine which percentage of the community was cultured, we clustered Illumina sequences at 97% similarity, using the culture sequences as a reference database. For each amphibian species, we cultured, on average, 0.59% to 1.12% of each individual's bacterial community. However, the average percentage of bacteria that were culturable for each amphibian species was higher, with averages ranging from 2.81% to 7.47%. Furthermore, most of the dominant operational taxonomic units (OTUs), families, and phyla were represented in our cultures. These results open up new research avenues for understanding the functional roles of these dominant bacteria in host health.

scholarly journals Development and worldwide use of a non-lethal and minimal population-level impact protocols for the isolation of chytrids from amphibians

2018 ◽  
Author(s):  
Matthew C. Fisher ◽  
Pria Ghosh ◽  
Jennifer M. G. Shelton ◽  
Kieran Bates ◽  
Lola Brookes ◽  
...  
Keyword(s):  
Fungal Pathogens ◽  
Batrachochytrium Dendrobatidis ◽  
Population Level ◽  
Ability To Work ◽  
Amphibian Species ◽  
Sterile Culture ◽  
Important Group ◽  
Fungal Isolates ◽  
Emerging Fungal Pathogens

ABSTRACTParasitic chytrid fungi have emerged as a significant threat to amphibian species worldwide, necessitating the development of techniques to isolate these pathogens into sterile culture for research purposes. However, early methods of isolating chytrids from their hosts relied on killing amphibians. We modified a pre-existing protocol for isolating chytrids from infected animals to use toe clips and biopsies from toe webbing rather than euthanizing hosts, and distributed the protocol to interested researchers worldwide as part of the BiodivERsA project RACE – here called the RML protocol. In tandem, we developed a lethal procedure for isolating chytrids from tadpole mouthparts. Reviewing a database of use a decade after their inception, we find that these methods have been widely applied across at least 5 continents, 23 countries and in 62 amphibian species, and have been successfully used to isolate chytrids in remote field locations. Isolation of chytrids by the non-lethal RML protocol occured in 18% of attempts with 207 fungal isolates and three species of chytrid being recovered. Isolation of chytrids from tadpoles occured in 43% of attempts with 334 fungal isolates of one species (Batrachochytrium dendrobatidis) being recovered. Together, these methods have resulted in a significant reduction and refinement of our use of threatened amphibian species and have improved our ability to work with this important group of emerging fungal pathogens.

Panzootic chytrid fungus exploits diverse amphibian host environments through plastic infection strategies

2021 ◽  
Author(s):  
María Torres-Sánchez ◽  
Jennifer Villate ◽  
Sarah McGrath-Blaser ◽  
Ana V Longo
Keyword(s):  
Gene Expression ◽  
Batrachochytrium Dendrobatidis ◽  
Gene Duplications ◽  
Amphibian Skin ◽  
Amphibian Species ◽  
Pathogenic Genes ◽  
Host Pathogen ◽  
Single Host ◽  
History Of ◽  
Phylogenetic Framework

While many pathogens are limited to a single host, others can jump from host to host, which likely contributes to the emergence of infectious diseases. Despite this threat to biodiversity, traits associated with overcoming eco-evolutionary barriers to achieve host niche expansions are not well understood. Here, we examined the case of Batrachochytrium dendrobatidis (Bd), a multi-host pathogen that infects the skin of hundreds of amphibian species worldwide. To uncover functional machinery driving multi-host invasion, we analyzed Bd transcriptomic landscapes across 14 amphibian hosts and inferred the origin and evolutionary history of pathogenic genes under a phylogenetic framework comprising 12 other early-divergent zoosporic fungi. Our results not only revealed a conserved basal genetic machinery, but also highlighted the ability of Bd to display plastic infection strategies when challenged under suboptimal host environments. We found that genes related to amphibian skin exploitation have arisen mainly via gene duplications. We argue that plastic gene expression can drive variation in Bd lifecycles with different mode and tempo of development. Our findings support the idea that host skin environments exert contrasting selective pressures, such that gene expression plasticity constitutes one of the evolutionary keys leading to the success of this panzootic multi-host pathogen.

scholarly journals The Effect of Aquatic and Terrestrial Environmental Factors on the Interaction Between Grand Teton Boreal Toads and a Lethal Fungal Pathogen

2008 ◽  
Vol 31 ◽  
pp. 125-131
Author(s):  
Peter Murphy ◽  
Sophie St-Hilaire ◽  
Charles Peterson
Keyword(s):  
Fungal Pathogen ◽  
Batrachochytrium Dendrobatidis ◽  
Chytrid Fungus ◽  
Population Declines ◽  
Amphibian Skin ◽  
Amphibian Species ◽  
American Bullfrog ◽  
The North ◽  
S 100 ◽  
Boreal Toads

Batrachochytrium dendrobatidis (Bd), the chytrid fungus which infects keratinized amphibian skin and causes the lethal disease chytridiomycosis, has been linked to population declines and extinctions worldwide (Lips et al. 2006). Amphibians infected with Bd may suffer a variety of outcomes. Individuals of some species have been killed by :S 100 Bd zoospores, while other species, such as the North American bullfrog Rana catesbiana, are highly resistant (Daszak et al. 2004). Within an amphibian species, populations may also respond differently to Bd, with some declining et al. remaining stable (Kriger and Hero 2006). Divergent outcomes among species and populations with respect to Bd may arise from at least three factors, or their interaction.

scholarly journals Fungal infection, decline and persistence in the only obligate troglodytic Neotropical salamander

PeerJ ◽  
2020 ◽  
Vol 8 ◽  
pp. e9763
Author(s):  
Mizraim Olivares-Miranda ◽  
Vance T. Vredenburg ◽  
Julio C. García-Sánchez ◽  
Allison Q. Byrne ◽  
Erica B. Rosenblum ◽  
...  
Keyword(s):  
Batrachochytrium Dendrobatidis ◽  
Infection Intensity ◽  
Sampling Technique ◽  
Sympatric Species ◽  
Amphibian Declines ◽  
Small Range ◽  
Museum Specimens ◽  
Amphibian Species ◽  
Extant Population ◽  
Epidemic Wave

The fungal pathogen Batrachochytrium dendrobatidis (Bd) is implicated in global mass die-offs and declines in amphibians. In Mesoamerica, the Bd epidemic wave hypothesis is supported by detection of Bd in historic museum specimens collected over the last century, yet the timing and impact of the early stages of the wave remain poorly understood. Chiropterotriton magnipes, the only obligate troglodytic Neotropical salamander, was abundant in its small range in the decade following its description in 1965, but subsequently disappeared from known localities and was not seen for 34 years. Its decline is roughly coincident with that of other populations of Neotropical salamanders associated with the invasion and spread of Bd. To determine the presence and infection intensity of Bd on C. magnipes and sympatric amphibian species (which are also Bd hosts), we used a noninvasive sampling technique and qPCR assay to detect Bd on museum specimens of C. magnipes collected from 1952 to 2012, and from extant populations of C. magnipes and sympatric species of amphibians. We also tested for the presence of the recently discovered Batrachochytrium salamandivorans (Bsal), another fungal chytridiomycete pathogen of salamanders, using a similar technique specific for Bsal. We did not detect Bd in populations of C. magnipes before 1969, while Bd was detected at low to moderate prevalence just prior to and during declines. This pattern is consistent with Bd-caused epizootics followed by host declines and extirpations described in other hosts. We did not detect Bsal in any extant population of C. magnipes. We obtained one of the earliest positive records of the fungus to date in Latin America, providing additional historical evidence consistent with the Bd epidemic wave hypothesis. Genotyping results show that at least one population is currently infected with the Global Panzootic Lineage of Bd, but our genotyping of the historical positive samples was unsuccessful. The lack of large samples from some years and the difficulty in genotyping historical Bd samples illustrate some of the difficulties inherent in assigning causality to historical amphibian declines. These data also provide an important historical baseline for actions to preserve the few known remaining populations of C. magnipes.

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