Inhibitory Bacterial Diversity and Mucosome Function Differentiate Susceptibility of Appalachian Salamanders to Chytrid Fungal Infection

Jiménez, Randall R.; Carfagno, Amy; Linhoff, Luke; Gratwicke, Brian; Woodhams, Douglas C.; Chafran, Liana S.; Bletz, Molly C.; Bishop, Barney; Muletz‐Wolz, Carly R.

doi:10.1128/aem.01818-21

Cited by 32 publications

(31 citation statements)

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“…These differences could be explained by differences in skin mucus composition, immune response, or gene expression before and after metamorphosis as it has been proposed that mucus chemical composition (e.g., production of antimicrobial peptides) play a critical role in shaping the skin microbiota as well as in defense against pathogens [ 30 , 54 , 55 ]. Antimicrobial peptide repertory of the skin changes through development in some frog species [ 56 ], and some bacteria can induce the synthesis of specific antimicrobial peptides [ 51 ].…”

Section: Discussionmentioning

confidence: 99%

“…Observations in several amphibian species indicate that certain bacteria with properties such as biofilm formation [ 82 ] or putative inhibitory ability [ 55 ] are positively or negatively corelated with a decrease of Bd prevalence. Thus, we expect that bacteria with negative correlations to infection intensity could be important in the defense against Bd in A. altamirani .…”

Section: Discussionmentioning

confidence: 99%

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The skin microbiota of the axolotl Ambystoma altamirani is highly influenced by metamorphosis and seasonality but not by pathogen infection

et al. 2022

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Background Microbiomes have been increasingly recognized as major contributors to host health and survival. In amphibians, bacterial members of the skin microbiota protect their hosts by inhibiting the growth of the fungal pathogen Batrachochytrium dendrobatidis (Bd). Even though several studies describe the influence of biotic and abiotic factors over the skin microbiota, it remains unclear how these symbiotic bacterial communities vary across time and development. This is particularly relevant for species that undergo metamorphosis as it has been shown that host physiology and ecology drastically influence diversity of the skin microbiome. Results We found that the skin bacterial communities of the axolotl A. altamirani are largely influenced by the metamorphic status of the host and by seasonal variation of abiotic factors such as temperature, pH, dissolved oxygen and conductivity. Despite high Bd prevalence in these samples, the bacterial diversity of the skin microbiota did not differ between infected and non-infected axolotls, although relative abundance of particular bacteria were correlated with Bd infection intensity. Conclusions Our work shows that metamorphosis is a crucial process that shapes skin bacterial communities and that axolotls under different developmental stages respond differently to environmental seasonal variations. Moreover, this study greatly contributes to a better understanding of the factors that shape amphibian skin microbiota, especially in a largely underexplored group like axolotls (Mexican Ambystoma species).

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

The skin microbiota of the axolotl Ambystoma altamirani is highly influenced by metamorphosis and seasonality but not by pathogen infection

et al. 2022

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“…Open Sci. 10: 220810 [141], our results suggest that despite containing many putative anti-Bd skin microbes, the pre-existing skin microbiome is not a key factor accounting for control of Bd infection in hellbenders.…”

Section: Microbiome Response To Experimental Vaccination and Challengementioning

confidence: 77%

Immune priming prior to pathogen exposure sheds light on the relationship between host, microbiome and pathogen in disease

et al. 2023

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Dynamic interactions between host, pathogen and host-associated microbiome dictate infection outcomes. Pathogens including Batrachochytrium dendrobatidis (Bd) threaten global biodiversity, but conservation efforts are hindered by limited understanding of amphibian host, Bd and microbiome interactions. We conducted a vaccination and infection experiment using Eastern hellbender salamanders ( Cryptobranchus alleganiensis alleganiensis ) challenged with Bd to observe infection, skin microbial communities and gene expression of host skin, pathogen and microbiome throughout the experiment. Most animals survived high Bd loads regardless of their vaccination status and vaccination did not affect pathogen load, but host gene expression differed based on vaccination. Oral vaccination (exposure to killed Bd) stimulated immune gene upregulation while topically and sham-vaccinated animals did not significantly upregulate immune genes. In early infection, topically vaccinated animals upregulated immune genes but orally and sham-vaccinated animals downregulated immune genes. Bd increased pathogenicity-associated gene expression in late infection when Bd loads were highest. The microbiome was altered by Bd, but there was no correlation between anti-Bd microbe abundance or richness and pathogen burden. Our observations suggest that hellbenders initially generate a vigorous immune response to Bd, which is ineffective at controlling disease and is subsequently modulated. Interactions with antifungal skin microbiota did not influence disease progression.

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“…Our use of microbiome read counts to test for a relationship between Bd -inhibitory bacteria and Bd produced comparable results to studies which used quantitative PCR to detect and quantify the abundance of Bd . For example, Jiménez et al (2022) found that Bd infection intensity significantly decreased on the skin of the eastern newt ( Notophthalmus viridescens ) as the relative abundance of putative Bd -inhibitory bacteria increased. Similarly, Flechas et al (2019) found lower Bd infection prevalence within post-metamorphic life stages which also had high relative abundances of Bd -inhibitory bacteria in two frog species.…”

Section: Discussionmentioning

confidence: 99%

Spatiotemporal and ontogenetic variation, microbial selection, and predicted Bd-inhibitory function in the skin-associated microbiome of a Rocky Mountain amphibian

2022

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Host-associated microbiomes play important roles in host health and pathogen defense. In amphibians, the skin-associated microbiota can contribute to innate immunity with potential implications for disease management. Few studies have examined season-long temporal variation in the amphibian skin-associated microbiome, and the interactions between bacteria and fungi on amphibian skin remain poorly understood. We characterize season-long temporal variation in the skin-associated microbiome of the western tiger salamander (Ambystoma mavortium) for both bacteria and fungi between sites and across salamander life stages. Two hundred seven skin-associated microbiome samples were collected from salamanders at two Rocky Mountain lakes throughout the summer and fall of 2018, and 127 additional microbiome samples were collected from lake water and lake substrate. We used 16S rRNA and ITS amplicon sequencing with Bayesian Dirichlet-multinomial regression to estimate the relative abundances of bacterial and fungal taxa, test for differential abundance, examine microbial selection, and derive alpha diversity. We predicted the ability of bacterial communities to inhibit the amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd), a cutaneous fungal pathogen, using stochastic character mapping and a database of Bd-inhibitory bacterial isolates. For both bacteria and fungi, we observed variation in community composition through time, between sites, and with salamander age and life stage. We further found that temporal trends in community composition were specific to each combination of salamander age, life stage, and lake. We found salamander skin to be selective for microbes, with many taxa disproportionately represented relative to the environment. Salamander skin appeared to select for predicted Bd-inhibitory bacteria, and we found a negative relationship between the relative abundances of predicted Bd-inhibitory bacteria and Bd. We hope these findings will assist in the conservation of amphibian species threatened by chytridiomycosis and other emerging diseases.

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Inhibitory Bacterial Diversity and Mucosome Function Differentiate Susceptibility of Appalachian Salamanders to Chytrid Fungal Infection

Abstract: How host mucosal defenses interact, and influence disease outcome is critical in understanding host defenses against pathogens. A more detailed understanding is needed of the interactions between the host and the functioning of its mucosal defenses in pathogen defense.

Cited by 32 publications

References 85 publications

The skin microbiota of the axolotl Ambystoma altamirani is highly influenced by metamorphosis and seasonality but not by pathogen infection

The skin microbiota of the axolotl Ambystoma altamirani is highly influenced by metamorphosis and seasonality but not by pathogen infection

Immune priming prior to pathogen exposure sheds light on the relationship between host, microbiome and pathogen in disease

Spatiotemporal and ontogenetic variation, microbial selection, and predicted Bd-inhibitory function in the skin-associated microbiome of a Rocky Mountain amphibian

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