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1. Amphibian mast cells: barriers to deadly chytrid fungus infections

   https://doi.org/10.7554/eLife.92168.1  

   Hauser, Kelsey A; Hossainey, Muhammad_R H; Gentry, Lindsey K; Garvey, Christina N; Ranganathan, Netra; Yaparla, Amulya; Kalia, Namarta; Zelle, Mira; Jones, Elizabeth J; Duttargi, Anju N; et al (December 2023, E life Sciences)

   Global amphibian declines are largely driven by deadly disease outbreaks caused by the chytrid fungus, Batrachochytrium dendrobatidis (Bd). In the time since these disease outbreaks were first discovered, much has been learned about the roles of amphibian skin-produced antimicrobial components and skin microbiomes in controlling Bd. Yet almost nothing is known about the roles of skin-resident immune cells in anti-Bd defenses. Notably, mammalian mast cells reside within and serve as key immune sentinels in barrier tissues like the skin. Thus, they are critical to immune recognition of pathogens and to orchestrating the ensuing immune responses. Accordingly, we investigated the roles of Xenopus laevis frog mast cells during Bd infections. Our findings indicate that enrichment of X. laevis skin mast cells confers significant anti-Bd protection and ameliorates the inflammation-associated skin damage caused by Bd infection. Moreover, enriching X. laevis mast cells promotes greater mucin content within cutaneous mucus glands and protects frogs from Bd-mediated changes to their skin microbiomes. Together, this work underlines the importance of amphibian skin-resident immune cells in anti-Bd defenses and introduces a novel approach for investigating amphibian host-chytrid pathogen interactions. 

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2. Amphibian (Xenopus laevis) Macrophage Subsets Vary in Their Responses to the Chytrid Fungus Batrachochytrium dendrobatidis

   https://doi.org/10.3390/jof11040311  

   Yaparla, Amulya; Popovic, Milan; Hauser, Kelsey A; Rollins-Smith, Louise A; Grayfer, Leon (April 2025, Journal of Fungi)

   The chytrid fungus, Batrachochytrium dendrobatidis (Bd), infects amphibian skin, causing chytridiomycosis, which is a contributing cause of worldwide declines and extinctions of amphibians. Relatively little is known about the roles of amphibian skin-resident immune cells, such as macrophages, in these antifungal defenses. Across vertebrates, macrophage differentiation is controlled through the activation of colony-stimulating factor-1 (CSF1) receptor by CSF1 and interleukin-34 (IL34) cytokines. While the precise roles of these respective cytokines in macrophage development remain to be fully explored, our ongoing studies indicate that frog (Xenopus laevis) macrophages differentiated by recombinant forms of CSF1 and IL34 are functionally distinct. Accordingly, we explored the roles of X. laevis CSF1- and IL34-macrophages in anti-Bd defenses. Enriching cutaneous IL34-macrophages, but not CSF1-macrophages, resulted in significant anti-Bd protection. In vitro analysis of frog macrophage-Bd interactions indicated that both macrophage subsets phagocytosed Bd. However, IL34-macrophages cocultured with Bd exhibited greater pro-inflammatory gene expression, whereas CSF1-macrophages cocultured with Bd showed greater immunosuppressive gene expression profiles. Concurrently, Bd-cocultured with CSF1-macrophages, but not IL34-macrophages, possessed elevated expression of genes associated with immune evasion. This work marks a step forward in our understanding of the roles of frog macrophage subsets in antifungal defenses. 

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3. Host-associated helminth diversity and microbiome composition contribute to anti-pathogen defences in tropical frogs impacted by forest fragmentation

   https://doi.org/10.1098/rsos.240530  

   Neely, Wesley J; Souza, Kassia_M C; Martins, Renato A; Marshall, Vanessa M; Buttimer, Shannon M; Brito_de_Assis, Ananda; Medina, Daniel; Whetstone, Ross D; Lyra, Mariana L; Ribeiro, José Wagner; et al (June 2024, Royal Society Open Science)

   Habitat fragmentation can negatively impact wildlife populations by simplification of ecological interactions, but little is known about how these impacts extend to host-associated symbiotic communities. The symbiotic communities of amphibians play important roles in anti-pathogen defences, particularly against the amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd). In this study, we analyse the role of macroparasitic helminth communities in concert with microbial communities in defending the host against Bd infection within the context of forest fragmentation. We found that skin microbial and helminth communities are disrupted at fragmented habitats, while gut microbiomes appear more resilient to environmental change. We also detected potential protective roles of helminth diversity and anti-pathogen microbial function in limiting Bd infection. Microbial network analysis revealed strong patterns of structure in both skin and gut communities, with helminths playing central roles in these networks. We reveal consistent roles of microbial and helminth diversity in driving host–pathogen interactions and the potential implications of fragmentation on host fitness. 

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4. When Defenses Fail: Atelopus zeteki Skin Secretions Increase Growth of the Pathogen Batrachochytrium dendrobatidis

   https://doi.org/10.1093/icb/icac060  

   Gass, Jordan; Voyles, Jamie (May 2022, Integrative and Comparative Biology)

   Abstract To combat the threat of emerging infectious diseases in wildlife, ecoimmunologists seek to understand the complex interactions among pathogens, their hosts, and their shared environments. The cutaneous fungal pathogen Batrachochytrium dendrobatidis (Bd), has led to the decline of innumerable amphibian species, including the Panamanian golden frog (Atelopus zeteki). Given that Bd can evade or dampen the acquired immune responses of some amphibians, nonspecific immune defenses are thought to be especially important for amphibian defenses against Bd. In particular, skin secretions constitute a vital component of amphibian innate immunity against skin infections, but their role in protecting A. zeteki from Bd is unknown. We investigated the importance of this innate immune component by reducing the skin secretions from A. zeteki and evaluating their effectiveness against Bd in vitro and in vivo. Following exposure to Bd in a controlled inoculation experiment, we compared key disease characteristics (e.g., changes in body condition, prevalence, pathogen loads, and survival) among groups of frogs that had their skin secretions reduced and control frogs that maintained their skin secretions. Surprisingly, we found that the skin secretions collected from A. zeteki increased Bd growth in vitro. This finding was further supported by infection and survival patterns in the in vivo experiment where frogs with reduced skin secretions tended to have lower pathogen loads and survive longer compared to frogs that maintained their secretions. These results suggest that the skin secretions of A. zeteki are not only ineffective at inhibiting Bd but may enhance Bd growth, possibly leading to greater severity of disease and higher mortality in this highly vulnerable species. These results differ from those of previous studies in other amphibian host species that suggest that skin secretions are a key defense in protecting amphibians from developing severe chytridiomycosis. Therefore, we suggest that the importance of immune components cannot be generalized across all amphibian species or over time. Moreover, the finding that skin secretions may be enhancing Bd growth emphasizes the importance of investigating these immune components in detail, especially for species that are a conservation priority. 

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5. Effects of temperature on the interaction between amphibian skin bacteria and Batrachochytrium dendrobatidis

   https://doi.org/10.3389/fmicb.2023.1253482  

   Robak, Matthew J; Saenz, Veronica; de_Cortie, Esmee; Richards-Zawacki, Corinne L (October 2023, Frontiers in Microbiology)

   Symbiotic relationships between animals and microbes are important for a range of functions, from digestion to protection from pathogens. However, the impact of temperature variation on these animal-microbe interactions remains poorly understood. Amphibians have experienced population declines and even extinctions on a global scale due to chytridiomycosis, a disease caused by chytrid fungi in the genusBatrachochytrium. Variation in susceptibility to this disease exists within and among host species. While the mechanisms generating differences in host susceptibility remain elusive, differences in immune system components, as well as variation in host and environmental temperatures, have been associated with this variation. The symbiotic cutaneous bacteria of amphibians are another potential cause for variation in susceptibility to chytridiomycosis, with some bacterial species producing antifungal metabolites that prevent the growth ofBd. The growth of bothBdand bacteria are affected by temperature, and thus we hypothesized that amphibian skin bacteria may be more effective at preventingBdgrowth at certain temperatures. To test this, we collected bacteria from the skins of frogs, harvested the metabolites they produced when grown at three different temperatures, and then grewBdin the presence of those metabolites under those same three temperatures in a three-by-three fully crossed design. We found that both the temperature at which cutaneous bacteria were grown (and metabolites produced) as well as the temperature at whichBdis grown can impact the ability of cutaneous bacteria to inhibit the growth ofBd. While some bacterial isolates showed the ability to inhibitBdgrowth across multiple temperature treatments, no isolate was found to be inhibitive across all combinations of bacterial incubation orBdchallenge temperatures, suggesting that temperature affects both the metabolites produced and the effectiveness of those metabolites against theBdpathogen. These findings move us closer to a mechanistic understanding of why chytridiomycosis outbreaks and related amphibian declines are often limited to certain climates and seasons. 

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