The adaptive microbiome hypothesis and immune interactions in amphibian mucus

Woodhams, Douglas C.; McCartney, Julia; Walke, Jenifer B.; Whetstone, Ross

doi:10.1016/j.dci.2023.104690

Cited by 18 publications

(17 citation statements)

References 312 publications

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“…Dermal swabs may provide additional insights into the health of salamanders beyond traditional hepatic metabolome profiling because of the chemical composition of the mucosal layer. The amphibian mucosal matrix is an intricate arrangement of protein-based mucins, lipids, carbohydrates, peptides, and other metabolites along with a diverse array of microbes (reviewed in Woodhams et al, 2023). Among the top impacted biological pathways identified from dermal swabs in the present study were alpha-linoleic and linoleic acid metabolism as well as fatty acid biosynthesis.…”

Section: Discussionmentioning

confidence: 76%

“…In addition to distinguishing metabolites and biological pathways of significance, the pesticides used in the present study were detected on the dermal swabs (Figure 4), suggesting that pesticides that amphibians have had recent contact with may also be identifiable using this nonlethal technique. Given that the amphibian dermal mucosa serves a myriad of functions ranging from water absorption and waterproofing to immunity (reviewed in Woodhams et al, 2023), expanding our toolkit to include mucosal sampling as a proxy for health profiling will aid conservation efforts and risk assessment.…”

Section: Discussionmentioning

confidence: 99%

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Validation of Salamander Dermal Mucus Swabs as a Novel, Nonlethal Approach for Amphibian Metabolomics and Glutathione Analysis Following Pesticide Exposure

Van Meter,

Glinski,

Wanat

et al. 2024

Enviro Toxic and Chemistry

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Evaluating biomarkers of stress in amphibians is critical to conservation, yet current techniques are often destructive and/or time‐consuming, which limits ease of use. In the present study, we validate the use of dermal swabs in spotted salamanders (Ambystoma maculatum) for biochemical profiling, as well as glutathione (GSH) stress response following pesticide exposure. Thirty‐three purchased spotted salamanders were acclimated to laboratory conditions at Washington College (Chestertown, MD, USA) for 4 weeks. Following acclimation, salamanders were randomly sorted into three groups for an 8‐h pesticide exposure on soil: control with no pesticide, 2,4‐dichlorophenoxyacetic acid (2,4‐D), or chlorpyrifos. Before and after exposure, mucus samples were obtained by gently rubbing a polyester‐tipped swab 50 times across the ventral and dorsal surfaces. Salamanders were humanely euthanized and dissected to remove the brain for acetylcholinesterase and liver for GSH and hepatic metabolome analyses, and a whole‐body tissue homogenate was used for pesticide quantification. Levels of GSH were present in lower quantities on dermal swabs relative to liver tissues for chlorpyrifos, 2,4‐D, and control treatments. However, 2,4‐D exposures demonstrated a large effect size increase for GSH levels in livers (Cohen's d = 0.925, p = 0.036). Other GSH increases were statistically insignificant, and effect sizes were characterized as small for 2,4‐D mucosal swabs (d = 0.36), medium for chlorpyrifos mucosal swabs (d = 0.713), and negligible for chlorpyrifos liver levels (d = 0.012). The metabolomics analyses indicated that the urea cycle, alanine, and glutamate metabolism biological pathways were perturbed by both sets of pesticide exposures. Obtaining mucus samples through dermal swabbing in amphibians is a viable technique for evaluating health in these imperiled taxa. Environ Toxicol Chem 2024;00:1–12. © 2024 SETAC

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Section: Discussionmentioning

confidence: 76%

Section: Discussionmentioning

confidence: 99%

Validation of Salamander Dermal Mucus Swabs as a Novel, Nonlethal Approach for Amphibian Metabolomics and Glutathione Analysis Following Pesticide Exposure

Van Meter,

Glinski,

Wanat

et al. 2024

Enviro Toxic and Chemistry

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“…and metabolism (Clugston & Blaner, 2014). One possible explanation for our findings is that limitations in dietary carotenoids may affect the normal secretion of innate immune compounds, such as defensins and lysozymes, that likely control the skin microbiota and promote homeostatisis (Colombo et al, 2015;Woodhams et al, 2023).…”

Section: T T T T T T T T T T T T T T T T T T T T T T T T T T T T Cu Cumentioning

confidence: 92%

Dietary carotenoid supplementation has long‐term and community‐wide effects on the amphibian skin microbiome

Risely,

Byrne,

Hoye

et al. 2023

Molecular Ecology

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The amphibian skin microbiome plays a crucial role in host immunity and pathogen defence, yet we know little about the environmental drivers of skin microbial variation across host individuals. Inter‐individual variation in the availability of micro‐nutrients such as dietary carotenoids, which are involved in amphibian immunity, may be one factor that influences skin microbial assembly across different life history stages. We compared the effect of four carotenoid supplementation regimes during different life stages on the adult skin microbiome using a captive population of the critically endangered southern corroboree frog, Pseudophryne corroboree. We applied 16S rRNA sequencing paired with joint‐species distribution models to examine the effect of supplementation on taxon abundances. We found that carotenoid supplementation had subtle yet taxonomically widespread effects on the skin microbiome, even 4.5 years post supplementation. Supplementation during any life‐history stage tended to have a positive effect on the number of bacterial taxa detected, although explanatory power was low. Some genera were sensitive to supplementation pre‐metamorphosis, but most demonstrated either additive or dominant effects, whereby supplementation during one life history stage had intermediate or similar effects, respectively, to supplementation across life. Carotenoid supplementation increased abundances of taxa belonging to lactic acid bacteria, including Lactococcus and Enterococcus, a group of bacteria that have previously been linked to protection against the amphibian fungal pathogen Batrachochytrium dendrobatidis (Bd). While the fitness benefits of these microbial shifts require further study, these results suggest a fundamental relationship between nutrition and the amphibian skin microbiome which may be critical to amphibian health and the development of novel conservation strategies.

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“…Another contributor to immune function is the host-associated microbiome, which, combined with the innate immune system, provides a defensive mechanism against pathogen colonization and growth [30][31][32][33] . In line with work on the microbiomes of other organisms, classifying protective aspects of the amphibian microbiome is complex and often conflicting between host species and study systems [34][35][36] .…”

mentioning

confidence: 99%

“…These include bacteria isolated from amphibian skin capable of inhibiting colonization and growth of the amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd) [40][41][42][43] , a globally distributed pathogen of great conservation concern for amphibians 8,44,45 . The outcome of pathogen infection may, therefore, be determined by adaptive shifts in the microbiome through enrichment with key anti-pathogen members, bolstering immune defenses 33,41,43,[46][47][48] .…”

mentioning

confidence: 99%

Linking microbiome and stress hormone responses in wild tropical treefrogs across continuous and fragmented forests

Neely,

Martins,

Mendonça da Silva

et al. 2023

Commun Biol

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The amphibian skin microbiome is an important component of anti-pathogen defense, but the impact of environmental change on the link between microbiome composition and host stress remains unclear. In this study, we used radiotelemetry and host translocation to track microbiome composition and function, pathogen infection, and host stress over time across natural movement paths for the forest-associated treefrog, Boana faber. We found a negative correlation between cortisol levels and putative microbiome function for frogs translocated to forest fragments, indicating strong integration of host stress response and anti-pathogen potential of the microbiome. Additionally, we observed a capacity for resilience (resistance to structural change and functional loss) in the amphibian skin microbiome, with maintenance of putative pathogen-inhibitory function despite major temporal shifts in microbiome composition. Although microbiome community composition did not return to baseline during the study period, the rate of microbiome change indicated that forest fragmentation had more pronounced effects on microbiome composition than translocation alone. Our findings reveal associations between stress hormones and host microbiome defenses, with implications for resilience of amphibians and their associated microbes facing accelerated tropical deforestation.

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The adaptive microbiome hypothesis and immune interactions in amphibian mucus

Cited by 18 publications

References 312 publications

Validation of Salamander Dermal Mucus Swabs as a Novel, Nonlethal Approach for Amphibian Metabolomics and Glutathione Analysis Following Pesticide Exposure

Validation of Salamander Dermal Mucus Swabs as a Novel, Nonlethal Approach for Amphibian Metabolomics and Glutathione Analysis Following Pesticide Exposure

Dietary carotenoid supplementation has long‐term and community‐wide effects on the amphibian skin microbiome

Linking microbiome and stress hormone responses in wild tropical treefrogs across continuous and fragmented forests

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