Gene expression varies within and between enzootic and epizootic lineages of Batrachochytrium dendrobatidis (Bd) in the Americas

McDonald, Cait A.; Ellison, Amy; Toledo, Luı́s Felipe; James, Timothy Y.; Zamudio, Kelly R.

doi:10.1016/j.funbio.2019.10.008

Cited by 19 publications

(25 citation statements)

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“…S2). We uncovered a similar general expression pattern among Bd samples grown in vitro , which included two different Bd lineages ( Bd GPL and Bd Brazil) (33), as these points clustered at one end of the PC1 (Fig. 2).…”

Section: Resultsmentioning

confidence: 72%

“…Chytridiomycosis threatens amphibian populations worldwide, however, disease risk varies greatly depending on a myriad of factors, including Bd lineage (12,13,16,24). While several studies have characterized the infection response of different amphibian species (21,(28)(29)(30)(31)(32)(33)(34)(35), our work contributes to identify Bd's functional machinery driving invasion and disease dynamics in a wide amphibian host range. In this study, we provide a framework to integrate available transcriptome data to further explore pathogen functional genomics during host-pathogen interactions.…”

Section: Discussionmentioning

confidence: 99%

“…Infected amphibian skin and in culture transcriptome data. We selected RNA-Seq data from Bd in culture studies (21,22,31,33) and amphibian infection trials (21,22,(28)(29)(30)32,(34)(35)(36)(37) and generated new infection transcriptome data for two amphibian species (see Table S1 for NCBI Short Read Archive accession codes and further information about transcriptome files). Data selection was made based on sequencing strategy (Illumina sequencing technology), experiment day, sequencing coverage, and number of biological replicates.…”

Section: Methodsmentioning

confidence: 99%

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

Torres‐Sánchez

Villate

McGrath-Blaser

et al. 2021

Preprint

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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.

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Section: Resultsmentioning

confidence: 72%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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

Torres‐Sánchez

Villate

McGrath-Blaser

et al. 2021

Preprint

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“…It acts locally at the mucosal epithelium to limit damage from inflammation by inhibiting proteolytic enzyme activity, and has particular efficacy against serine proteases (Vandooren et al, 2018). Serine- type peptidases are notably expanded in the Bd genome, are expressed by both Bd- Brazil and Bd-GPL lineages, and may be key to the transition to pathogenicity within the Batrachochytrium genus (Joneson et al, 2011; McDonald et al, 2019). Shared early upregulation of a serine protease inhibitor by frogs could indicate a general response combatting nonspecific Bd colonization of the skin epithelium.…”

Section: Discussionmentioning

confidence: 99%

Host immune responses to enzootic and invasive pathogen lineages vary in magnitude, timing, and efficacy

McDonald

Becker

Lambertini

et al. 2021

Preprint

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Infectious diseases of wildlife continue to pose a threat to biodiversity worldwide, yet pathogens are far from monolithic in virulence. Within the same pathogen species, virulence can vary considerably depending on strain or lineage, in turn eliciting variable host responses. One pathogen that has caused extensive biodiversity loss is the amphibian-killing fungus, Batrachochytrium dendrobatidis (Bd), which is comprised of a globally widespread hypervirulent lineage (Bd-GPL), and multiple geographically restricted lineages. Whereas host immunogenomic responses to Bd-GPL have been characterized in a number of amphibian species, immunogenomic responses to geographically-restricted, enzootic Bd lineages are unknown. To examine lineage-specific host immune responses to Bd, we exposed a species of pumpkin toadlet, Brachycephalus pitanga, which is endemic to Brazil's Southern Atlantic Forest, to either the Bd-GPL or the enzootic Bd-Asia-2/Brazil (hereafter Bd-Brazil) lineage. We quantified functional immunogenomic responses over the course of infection using differential gene expression tests and coexpression network analyses. Host immune responses varied significantly with Bd lineage. Toadlet responses to Bd-Brazil were weak at early infection (26 genes differentially expressed), peaked by mid-stage infection (435 genes) and were nearly fully resolved by late-stage disease (9 genes). In contrast, responses to Bd-GPL were magnified and delayed; toadlets differentially expressed 97 genes early, 86 genes at mid-stage infection, and 728 genes by late-stage infection. Given that infection intensity did not vary between mid- and late-stage disease, this suggests that pumpkin toadlets may be at least partially tolerant to the geographically-restricted Bd-Brazil lineage. In contrast, mortality was higher in Bd-GPL-infected toadlets, suggesting that late-stage immune activation against Bd-GPL was not protective and was consistent with immune dysregulation previously observed in other species. Our results demonstrate that both the timing of immune response and the particular immune pathways activated are specific to Bd lineage. Within regions where multiple Bd lineages co-occur, and given continued global Bd movement, these differential host responses may influence not only individual disease outcome, but transmission dynamics at the population and community levels.

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“…Comparative genomics of chytrids has enabled the identification of gene families associated with pathogenicity and evidence of divergent infection strategies of Bd and Bsal [63]. Meanwhile, transcriptomics has revealed how host responses to infection vary depending on the host species but also the lineage of fungus infecting [64,65], and that the fungus itself exhibits host-specific gene expression [66]. Further emphasising how -omics reveals the extreme complexity of fungal host-pathogen systems, recent research has shown that environmental conditions such as temperature also mediate the transcriptional host response to infection [67].…”

Section: -Omics and Fungal Pathogen Outbreaks In Wildlifementioning

confidence: 99%

Cross-Disciplinary Genomics Approaches to Studying Emerging Fungal Infections

Ghosh

Brookes

Edwards

et al. 2020

Life

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Emerging fungal pathogens pose a serious, global and growing threat to food supply systems, wild ecosystems, and human health. However, historic chronic underinvestment in their research has resulted in a limited understanding of their epidemiology relative to bacterial and viral pathogens. Therefore, the untargeted nature of genomics and, more widely, -omics approaches is particularly attractive in addressing the threats posed by and illuminating the biology of these pathogens. Typically, research into plant, human and wildlife mycoses have been largely separated, with limited dialogue between disciplines. However, many serious mycoses facing the world today have common traits irrespective of host species, such as plastic genomes; wide host ranges; large population sizes and an ability to persist outside the host. These commonalities mean that -omics approaches that have been productively applied in one sphere and may also provide important insights in others, where these approaches may have historically been underutilised. In this review, we consider the advances made with genomics approaches in the fields of plant pathology, human medicine and wildlife health and the progress made in linking genomes to other -omics datatypes and sets; we identify the current barriers to linking -omics approaches and how these are being underutilised in each field; and we consider how and which -omics methodologies it is most crucial to build capacity for in the near future.

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Gene expression varies within and between enzootic and epizootic lineages of Batrachochytrium dendrobatidis (Bd) in the Americas

Cited by 19 publications

References 58 publications

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

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

Host immune responses to enzootic and invasive pathogen lineages vary in magnitude, timing, and efficacy

Cross-Disciplinary Genomics Approaches to Studying Emerging Fungal Infections

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