Differentiating Batrachochytrium dendrobatidis and B. salamandrivorans in Amphibian Chytridiomycosis Using RNAScope®in situ Hybridization

Ossiboff, Robert J.; Towe, Anastasia E; Brown, Melissa Ann; Longo, Ana V.; Lips, Karen R.; Miller, Debra L.; Carter, Edward Davis; Gray, Matthew J.; Frasca, Salvatore

doi:10.3389/fvets.2019.00304

Cited by 14 publications

(14 citation statements)

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“…This significant keratin upregulation in coinfection could disrupt cutaneous function to an even greater degree, and warrants further testing. If similar responses are active in other susceptible salamander taxa, such as lungless plethodontids (Carter et al, 2019;Ossiboff et al, 2019), which rely heavily on cutaneous respiration and osmoregulation, coinfection could have particularly negative consequences on host survival.…”

Section: Discussionmentioning

confidence: 99%

“…Batrachochytrium, or with various combinations of lineages of Bd that differ in genotype (Jenkinson et al, 2018;Longo, Fleischer, & Lips, 2019;Ossiboff et al, 2019). Bd is widespread, and one or more lineages can be found on all continents inhabited by amphibians, including North America (O'Hanlon et al, 2018).…”

Section: Chytrid Coinfection Can Occur Between the Two Species Ofmentioning

confidence: 99%

“…However, pathogenic profiles of Bd and Bsal are distinct, with the former causing epidermal hyperplasia and hyperkeratosis, while the latter elicits macroscopic ulceration and necrosis that can reach the epithelial cells of dermal glands (Berger et al, 1998;Martel et al, 2013;Ossiboff et al, 2019;Voyles et al, 2009). In some host species, susceptibility to Bd appears to be related to compromised skin integrity, dysregulated innate immune processes, and T cell suppression (Ellison, Savage, et al, 2014;Ellison, Tunstall, et al, 2014;Fites et al, 2013;Grogan et al, 2018;McMahon et al, 2014;Rosenblum et al, 2009).…”

Section: Chytrid Coinfection Can Occur Between the Two Species Ofmentioning

confidence: 99%

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Incapacitating effects of fungal coinfection in a novel pathogen system

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As globalization lowers geographic barriers to movement, coinfection with novel and enzootic pathogens is increasingly likely. Novel and enzootic pathogens can interact synergistically or antagonistically, leading to increased or decreased disease severity. Here we examine host immune responses to coinfection with two closely related fungal pathogens: Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal). Both pathogens have had detrimental effects on amphibian populations, with Bd now largely enzootic, while Bsal is currently spreading and causing epizootics. Recent experimental work revealed that newts coinfected with Bd and Bsal had significantly higher mortality than those infected with either pathogen alone. Here we characterize host immunogenomic responses to chytrid coinfection relative to single infection. Across several classes of immune genes including pattern recognition receptors, cytokines, and MHC, coinfected host gene expression was weakly upregulated or comparable to that seen in single Bd infection, but significantly decreased when compared to Bsal infection. Combined with strong complement pathway downregulation and keratin upregulation, these results indicate that coinfection with Bd and Bsal compromises immune responses active against Bsal alone. As Bsal continues to invade naïve habitats where Bd is enzootic, coinfection will be increasingly common. If other Bd‐susceptible species in the region have similar responses, interactions between the two pathogens could cause severe population and community‐level declines.

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Section: Discussionmentioning

confidence: 99%

Section: Chytrid Coinfection Can Occur Between the Two Species Ofmentioning

confidence: 99%

Section: Chytrid Coinfection Can Occur Between the Two Species Ofmentioning

confidence: 99%

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Incapacitating effects of fungal coinfection in a novel pathogen system

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“…Lastly, swabbing frequency had no apparent effect on survival or Bsal loads. Although swabbing can remove zoospores (18), it likely does not remove all zoosporangia, which can extend deeper into the stratum corneum and stratum granulosum (34,35). In histological crosssections, we observed removal of epidermal layers, presumably from swabbing, and the presence of zoosporangia thereafter.…”

Section: Discussionmentioning

confidence: 83%

Experimental methodologies can affect pathogenicity ofBatrachochytrium salamandrivoransinfections

Kumar¹,

Malagon²,

Carter³

et al. 2020

Preprint

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25Controlled experiments are one approach to understanding the pathogenicity of etiologic agents 26 to susceptible hosts. The recently discovered fungal pathogen, Batrachochytrium 27 salamandrivorans (Bsal), has resulted in a surge of experimental investigations because of its 28 potential to impact global salamander biodiversity. However, variation in experimental 29 methodologies could thwart knowledge advancement by introducing confounding factors that 30 make comparisons difficult among studies. Thus, our objective was to evaluate if variation in 31 experimental methods changed inferences made on the pathogenicity of Bsal. We tested whether 32 passage duration of Bsal culture, exposure method of the host to Bsal (water bath vs. skin 33 inoculation), Bsal culturing method (liquid vs. plated), host husbandry conditions (aquatic vs. 34 terrestrial), and skin swabbing frequency influenced diseased-induced mortality in a susceptible 35 host species, the eastern newt (Notophthalmus viridescens). We found that disease-induced 36 mortality was faster for eastern newts when exposed to a low passage isolate, when newts were 37 housed in terrestrial environments, and if exposure to zoospores occurred via water bath. We did 38 not detect differences in disease-induced mortality between culturing methods or swabbing 39 frequencies. Our results illustrate the need to standardize methods among Bsal experiments; we 40 provide suggestions for future experiments in the context of hypothesis testing. 41 42 43 44 4 45 46Batrachochytrium salamandrivorans (Bsal) is an emerging fungal pathogen of global 47 conservation concern(1-3). Bsal has been identified as the causal agent in recent near extirpations 48 of wild fire salamanders (Salamandra salamandra) in Belgium and the Netherlands(4, 5), and 49 has been detected in live amphibians in captivity and moving through international trade(6-8). 50Controlled experiments where hosts are exposed to Bsal under standardized conditions suggest 51 that the pathogen has a broad host range, including several salamander and anuran families (4, 9). 52A central tenet to understanding Bsal invasion threat is estimating host susceptibility to infection, 53 and whether host infection progresses to clinical disease hence its pathogenicity (10). 54One approach to estimating pathogenicity of etiologic agents is using exposure 55 experiments(11, 12). However, variation in pathogen culturing methods, host husbandry 56 conditions, and pathogen exposure methods could result in different inferences made on 57 pathogenicity (13). For example, Martel et al. (9) inferred that the eastern newt (Notophthalmus 58 viridescens) was hyper-sensitive to Bsal infection, because 100% of individuals exposed to 59 5x10 3 zoospores died within 34 days. Longo et al. (14) reported ca. 50% mortality of eastern 60 newts exposed to the same dose of Bsal over 18 weeks, with some individuals clearing the 61 pathogen and surviving to the end of the experiment. Several explanations were offered for the 62 difference in findi...

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“…Lastly, swabbing frequency had no apparent effect on survival or Bsal loads. Although swabbing can remove zoospores [18], it likely does not remove all zoosporangia, which can extend deeper into the stratum corneum and stratum granulosum [35,36]. In histological cross-sections, we observed removal of epidermal layers, presumably from swabbing, and the presence of zoosporangia thereafter.…”

Section: Plos Onementioning

confidence: 82%

Experimental methodologies can affect pathogenicity of Batrachochytrium salamandrivorans infections

et al. 2020

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Controlled experiments are one approach to understanding the pathogenicity of etiologic agents to susceptible hosts. The recently discovered fungal pathogen, Batrachochytrium salamandrivorans (Bsal), has resulted in a surge of experimental investigations because of its potential to impact global salamander biodiversity. However, variation in experimental methodologies could thwart knowledge advancement by introducing confounding factors that make comparisons difficult among studies. Thus, our objective was to evaluate if variation in experimental methods changed inferences made on the pathogenicity of Bsal. We tested whether passage duration of Bsal culture, exposure method of the host to Bsal (water bath vs. skin inoculation), Bsal culturing method (liquid vs. plated), host husbandry conditions (aquatic vs. terrestrial), and skin swabbing frequency influenced diseased-induced mortality in a susceptible host species, the eastern newt (Notophthalmus viridescens). We found that disease-induced mortality was faster for eastern newts when exposed to a low passage isolate, when newts were housed in terrestrial environments, and if exposure to zoospores occurred via water bath. We did not detect differences in disease-induced mortality between culturing methods or swabbing frequencies. Our results illustrate the need to standardize methods among Bsal experiments. We provide suggestions for future Bsal experiments in the context of hypothesis testing and discuss the ecological implications of our results.

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Differentiating Batrachochytrium dendrobatidis and B. salamandrivorans in Amphibian Chytridiomycosis Using RNAScope®in situ Hybridization

Cited by 14 publications

References 32 publications

Incapacitating effects of fungal coinfection in a novel pathogen system

Incapacitating effects of fungal coinfection in a novel pathogen system

Experimental methodologies can affect pathogenicity ofBatrachochytrium salamandrivoransinfections

Experimental methodologies can affect pathogenicity of Batrachochytrium salamandrivorans infections

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