Diet- and salinity-induced modifications of the gut microbiota are associated with differential physiological responses to ranavirus infection in
            <i>Rana sylvatica</i>

Hughey, Myra C.; Warne, Robin; Dulmage, Alexa; Reeve, Robyn E.; Curtis, Grace H.; Whitfield, Kourtnie; Schock, Danna M.; Crespi, Erica

doi:10.1098/rstb.2022.0121

Cited by 7 publications

(4 citation statements)

References 92 publications

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“…This does not necessarily indicate that there is no relationship between ranavirus infection and changes in the skin microbiome. A recent study has found that the composition of the gut microbiome of Rana sylvatica may influence stress response to ranaviral infection (Hughey et al, 2023). Future studies focused on symptomatic animals or gut microbiomes may provide greater insights into the hostranavirus-microbiome relationship.…”

Section: The Presence Of Infectionmentioning

confidence: 99%

Family shapes microbiome differences in Oklahoma salamanders

Kirsch,

Smith,

Becker

et al. 2024

Front. Microbiomes

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IntroductionGiven the role of microbiomes in promoting host health and homeostasis, understanding the factors shaping skin microbial communities in wild vertebrates has become increasingly important in conservation. This goal is even more pressing for amphibians, for which the skin has multiple critical functions, and pathogens currently decimating populations are linked to significant changes in skin microbiomes. However, because microbiomes are also shaped by environmental and ecological influences, as well as by host phylogeny, it is important to quantify these contributions to microbiome structure in the presence of infection.MethodsTo understand the joint influence of these diverse factors shaping microbiomes, we used 16S rRNA sequencing to characterize the skin microbial communities of six salamander species (families Plethodontidae and Salamandridae) found in Oklahoma and contrasted the effects of infection status, phylogeny, host ecology, and host environment (i.e., climate) on skin microbiomes.ResultsDifferences at the level of host family were the main factor influencing microbiome diversity; however, we did not detect a substantial phylogenetic signal. Instead, host ecology and environment were more important in driving microbiome differences among species and genera. Salamanders that tested positive for the skin fungal parasite Batrachochytrium dendrobatidis (Bd) also had slightly less diverse microbiomes than Bd-free animals, but no such differences were associated with the systemic pathogen ranavirus (RV).DiscussionTogether, these results indicate a nuanced relationship between the number and type of microbes present on salamander skin and the factors influencing them. By developing a baseline assessment of the microbiome diversity and richness present on the skin of these focal species, this work also provides a foundation for monitoring and evaluating changes in skin microbiomes as populations continue to experience stressors and diseases.

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Section: The Presence Of Infectionmentioning

confidence: 99%

Family shapes microbiome differences in Oklahoma salamanders

Kirsch,

Smith,

Becker

et al. 2024

Front. Microbiomes

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“…For example, high-quality diets can improve the host's nutrient uptake and alter the metabolites used and produced by the host and its microbial communities [ 99 , 100 ]. In this theme issue, [ 101 ] investigates how increasing salinization in freshwaters by road de-icing salt runoff affects gut bacterial assembly, host physiology and responses to ranavirus exposure in larval wood frogs ( Rana sylvatica ). The authors found that elevating salinity and supplementing a basic larval diet with algae increased larval growth but also increased ranavirus loads.…”

Section: Amphibian Infectious Diseasesmentioning

confidence: 99%

“…However, larvae given algae did not exhibit elevated corticosterone levels, accelerated development or weight loss post-infection, whereas larvae fed a basic diet did. The authors suggest that algal supplementation may reduce stress responses to infection by regulating host metabolism and endocrine function [ 101 ].…”

Section: Amphibian Infectious Diseasesmentioning

confidence: 99%

Introduction to the special issue Amphibian immunity: stress, disease and ecoimmunology

Assis

Robert

Titon

2023

Phil. Trans. R. Soc. B

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Amphibian populations have been declining worldwide, with global climate changes and infectious diseases being among the primary causes of this scenario. Infectious diseases are among the primary drivers of amphibian declines, including ranavirosis and chytridiomycosis, which have gained more attention lately. While some amphibian populations are led to extinction, others are disease-resistant. Although the host's immune system plays a major role in disease resistance, little is known about the immune mechanisms underlying amphibian disease resistance and host–pathogen interactions. As ectotherms, amphibians are directly subjected to changes in temperature and rainfall, which modulate stress-related physiology, including immunity and pathogen physiology associated with diseases. In this sense, the contexts of stress, disease and ecoimmunology are essential for a better understanding of amphibian immunity. This issue brings details about the ontogeny of the amphibian immune system, including crucial aspects of innate and adaptive immunity and how ontogeny can influence amphibian disease resistance. In addition, the papers in the issue demonstrate an integrated view of the amphibian immune system associated with the influence of stress on immune–endocrine interactions. The collective body of research presented herein can provide valuable insights into the mechanisms underlying disease outcomes in natural populations, particularly in the context of changing environmental conditions. These findings may ultimately enhance our ability to forecast effective conservation strategies for amphibian populations. This article is part of the theme issue ‘Amphibian immunity: stress, disease and ecoimmunology’.

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“…For example, diet varies with amphibian life history stage and may in part contribute to differences in the microbiome observed between tadpoles and frogs, while microclimates may differ in their nutrient availability. Recent evidence indicates diet can mediate infection responses via shifts to the amphibian gut microbiome (Hughey et al, 2023), yet studies on the link between diet and the skin microbiome in amphibians are rare and limited to culturing methods (Antwis et al, 2014;Edwards et al, 2017), which underrepresents true microbial diversity.…”

mentioning

confidence: 99%

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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Diet- and salinity-induced modifications of the gut microbiota are associated with differential physiological responses to ranavirus infection in Rana sylvatica

Cited by 7 publications

References 92 publications

Family shapes microbiome differences in Oklahoma salamanders

Family shapes microbiome differences in Oklahoma salamanders

Introduction to the special issue Amphibian immunity: stress, disease and ecoimmunology

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

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