Infectious pathogens can disrupt the microbiome in addition to directly affecting the host. Impacts of disease may be dependent on the ability of the microbiome to recover from such disturbance, yet remarkably little is known about microbiome recovery after disease, particularly in nonhuman animals. We assessed the resilience of the amphibian skin microbial community after disturbance by the pathogen,
- NSF-PAR ID:
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- The ISME Journal
- Page Range / eLocation ID:
- p. 1628-1640
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
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.more » « less
Host-associated microbial communities can influence physiological processes of macroorganisms, including contributing to infectious disease resistance. For instance, some bacteria that live on amphibian skin produce antifungal compounds that inhibit two lethal fungal pathogens, Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal). Therefore, differences in microbiome composition among host species or populations within a species can contribute to variation in susceptibility to Bd/Bsal. This study applies 16S rRNA sequencing to characterize the skin bacterial microbiomes of three widespread terrestrial salamander genera native to the western United States. Using a metacommunity structure analysis, we identified dispersal barriers for these influential bacteria between salamander families and localities. We also analysed the effects of habitat characteristics such as percent natural cover and temperature seasonality on the microbiome. We found that certain environmental variables may influence the skin microbial communities of some salamander genera more strongly than others. Each salamander family had a somewhat distinct community of putative anti-Bd skin bacteria, suggesting that salamanders may select for a functional assembly of cutaneous symbionts that could differ in its ability to protect these amphibians from disease. Our observations raise the need to consider host identity and environmental heterogeneity during the selection of probiotics to treat wildlife diseases.
The amphibian skin microbiome has been the focus of numerous studies because of the protective effects that some bacteria provide against the pathogenic fungus
Batrachochytrium dendrobatidis, which has caused a global panzootic among amphibians. However, the mechanisms driving community structure and function in the amphibian skin microbiome are still poorly understood, and longitudinal analyses of the skin microbiome have not yet been conducted in wild populations. In this study, we investigate longitudinal patterns in the skin microbiome of 19 individually marked adult frogs from two wild populations of the endangered Sierra Nevada yellow-legged frog ( Rana sierrae), sampled over the course of 2 years. We found that individuals with low bacterial diversity (dominated by order Burkhorderiales) had significantly more stable bacterial communities than those with higher diversity. Amplicon sequence variants (ASVs) with high relative abundance were significantly less transient than those with low relative abundance, and ASVs with intermediate-level relative abundances experienced the greatest volatility over time. Based on these results, we suggest that efforts to develop probiotic treatments to combat B. dendrobatidisshould focus on bacteria that are found at high relative abundances in some members of a population, as these strains are more likely to persist and remain stable in the long term.
Variation in the structure of host-associated microbial communities has been correlated with the occurrence and severity of disease in diverse host taxa, suggesting a key role of the microbiome in pathogen defense. However, whether these correlations are typically a cause or consequence of pathogen exposure remains an open question, and requires experimental approaches to disentangle. In amphibians, infection by the fungal pathogen Batrachochytrium dendrobatidis (Bd) alters the skin microbial community in some host species, whereas in other species, the skin microbial community appears to mediate infection dynamics. In this study, we completed experimental Bd exposures in three species of tropical frogs (Agalychnis callidryas, Dendropsophus ebraccatus,andCraugastor fitzingeri) that were sympatric with Bd at the time of the study. For all three species, we identified key taxa within the skin bacterial communities that were linked to Bd infection dynamics. We also measured higher Bd infection intensities in D. ebraccatus and C. fitzingeri that were associated with higher mortality in C. fitzingeri. Our findings indicate that microbially mediated pathogen resistance is a complex trait that can vary within and across host species, and suggest that symbiont communities that have experienced prior selection for defensive microbes may be less likely to be disturbed by pathogen exposure.
Raina, Jean-Baptiste (Ed.)ABSTRACT Microbial relationships are critical to coral health, and changes in microbiomes are often exhibited following environmental disturbance. However, the dynamics of coral-microbial composition and external factors that govern coral microbiome assembly and response to disturbance remain largely uncharacterized. Here, we investigated how antibiotic-induced disturbance affects the coral mucus microbiota in the facultatively symbiotic temperate coral Astrangia poculata , which occurs naturally with high (symbiotic) or low (aposymbiotic) densities of the endosymbiotic dinoflagellate Breviolum psygmophilum . We also explored how differences in the mucus microbiome of natural and disturbed A. poculata colonies affected levels of extracellular superoxide, a reactive oxygen species thought to have both beneficial and detrimental effects on coral health. Using a bacterial and archaeal small-subunit (SSU) rRNA gene sequencing approach, we found that antibiotic exposure significantly altered the composition of the mucus microbiota but that it did not influence superoxide levels, suggesting that superoxide production in A. poculata is not influenced by the mucus microbiota. In antibiotic-treated A. poculata exposed to ambient seawater, mucus microbiota recovered to its initial state within 2 weeks following exposure, and six bacterial taxa played a prominent role in this reassembly. Microbial composition among symbiotic colonies was more similar throughout the 2-week recovery period than that among aposymbiotic colonies, whose microbiota exhibited significantly more interindividual variability after antibiotic treatment and during recovery. This work suggests that the A. poculata mucus microbiome can rapidly reestablish itself and that the presence of B. psygmophilum , perhaps by supplying nutrients, photosynthate, or other signaling molecules, exerts influence on this process. IMPORTANCE Corals are animals whose health is often maintained by symbiotic microalgae and other microorganisms, yet they are highly susceptible to environmental-related disturbances. Here, we used a known disruptor, antibiotics, to understand how the coral mucus microbial community reassembles itself following disturbance. We show that the Astrangia poculata microbiome can recover from this disturbance and that individuals with algal symbionts reestablish their microbiomes in a more consistent manner compared to corals lacking symbionts. This work is important because it suggests that this coral may be able to recover its mucus microbiome following disturbance, it identifies specific microbes that may be important to reassembly, and it demonstrates that algal symbionts may play a previously undocumented role in microbial recovery and resilience to environmental change.more » « less