This content will become publicly available on December 1, 2025
Disturbances alter the diversity and composition of microbial communities. Yet a generalized empirical assessment of microbiome responses to disturbance across different environments is needed to understand the factors driving microbiome recovery, and the role of the environment in driving these patterns.
To this end, we combined null models with Bayesian generalized linear models to examine 86 time series of disturbed mammalian, aquatic, and soil microbiomes up to 50 days following disturbance. Overall, disturbances had the strongest effect on mammalian microbiomes, which lost taxa and later recovered their richness, but not their composition. In contrast, following disturbance, aquatic microbiomes tended away from their pre-disturbance composition over time. Surprisingly, across all environments, we found no evidence of increased compositional dispersion (i.e., variance) following disturbance, in contrast to the expectations of the Anna Karenina Principle.
This is the first study to systematically compare secondary successional dynamics across disturbed microbiomes, using a consistent temporal scale and modeling approach. Our findings show that the recovery of microbiomes is environment-specific, and helps to reconcile existing, environment-specific research into a unified perspective.
- Award ID(s):
- 1749544
- PAR ID:
- 10509959
- Publisher / Repository:
- Springer Nature
- Date Published:
- Journal Name:
- Microbiome
- Volume:
- 12
- Issue:
- 1
- ISSN:
- 2049-2618
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
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
-
Wilkins, Laetitia_G E (Ed.)
ABSTRACT Microbial species that comprise host-associated microbiomes play an essential role in maintaining and mediating the health of plants and animals. While defining the role of individual or even complex communities is important toward quantifying the effect of the microbiome on host health, it is often challenging to develop causal studies that link microbial populations to changes in host fitness. Here, we investigated the impacts of reduced microbial load following antibiotic exposure on the fitness of the anemone,
Exaiptasia diaphana and subsequent recovery of the host’s microbiome. Anemones were exposed to two different types of antibiotic solutions for 3 weeks and subsequently held in sterilized seawater for a 3-week recovery period. Our results revealed that both antibiotic treatments reduced the overall microbial load during and up to 1 week post-treatment. The observed reduction in microbial load was coupled with reduced anemone biomass, halted asexual reproduction rates, and for one of the antibiotic treatments, the partial removal of the anemone’s algal symbiont. Finally, our amplicon sequencing results of the 16S rRNA gene revealed that anemone bacterial composition only shifted in treated individuals during the recovery phase of the experiment, where we also observed a significant reduction in the overall diversity of the microbial community. Our work implies that theE. diaphana’s microbiome contributes to host fitness and that the recovery of the host’s microbiome following disturbance with antibiotics leads to a reduced, but stable microbial state.IMPORTANCE Exaiptasia diaphana is an emerging model used to define the cellular and molecular mechanisms of coral-algal symbioses.E. diaphana also houses a diverse microbiome, consisting of hundreds of microbial partners with undefined function. Here, we applied antibiotics to quantify the impact of microbiome removal on host fitness as well as define trajectories in microbiome recovery following disturbance. We showed that reduction of the microbiome leads to negative impacts on host fitness, and that the microbiome does not recover to its original composition while held under aseptic conditions. Rather the microbiome becomes less diverse, but more consistent across individuals. Our work is important because it suggests that anemone microbiomes play a role in maintaining host fitness, that they are susceptible to disturbance events, and that it is possible to generate gnotobiotic individuals that can be leveraged in microbiome manipulation studies to investigate the role of individual species on host health. -
Abstract Insights into symbiosis between eukaryotic hosts and their microbiomes have shifted paradigms on what determines host fitness, ecology, and behavior. Questions remain regarding the roles of host versus environment in shaping microbiomes, and how microbiome composition affects host fitness. Using a model system in ecology, phytoplankton, we tested whether microbiomes are host-specific, confer fitness benefits that are host-specific, and remain conserved in time in their composition and fitness effects. We used an experimental approach in which hosts were cleaned of bacteria and then exposed to bacterial communities from natural environments to permit recruitment of microbiomes. We found that phytoplankton microbiomes consisted of a subset of taxa recruited from these natural environments. Microbiome recruitment was host-specific, with host species explaining more variation in microbiome composition than environment. While microbiome composition shifted and then stabilized over time, host specificity remained for dozens of generations. Microbiomes increased host fitness, but these fitness effects were host-specific for only two of the five species. The shifts in microbiome composition over time amplified fitness benefits to the hosts. Overall, this work solidifies the importance of host factors in shaping microbiomes and elucidates the temporal dynamics of microbiome compositional and fitness effects.
-
Abstract Mammalian gut microbiomes differ within and among hosts. Hosts that occupy a broad range of environments may exhibit greater spatiotemporal variation in their microbiome than those constrained as specialists to narrower subsets of resources or habitats. This can occur if widespread host encounter a variety of ecological conditions that act to diversify their gut microbiomes and/or if generalized host species tend to form large populations that promote sharing and maintenance of diverse microbes. We studied spatiotemporal variation in the gut microbiomes of three co‐occurring rodent species across an environmental gradient in a Kenyan savanna. We hypothesized: (1) the taxonomic, phylogenetic, and functional compositions of gut microbiomes as predicted using the Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt) differ significantly among host species; (2) microbiome richness increases with population size for all host species; and (3) host species exhibit different levels of seasonal change in their gut microbiomes, reflecting different sensitivities to the environment. We evaluated changes in gut microbiome composition according to host species identity, site, and host population size using three years of capture–mark–recapture data and 351 microbiome samples. Host species differed significantly in microbiome composition, though the two species with more specialized diets and higher demographic sensitivities showed only slightly greater microbiome variability than those of a widespread dietary generalist. Total microbiome richness increased significantly with host population size for all species, but only one of the more specialized species also exhibited greater individual‐level microbiome richness in large populations. Across co‐occurring rodent species with diverse diets and life histories, large host population sizes were associated both with greater population‐level microbiome richness (sampling effects) and turnover in the relative abundance of bacterial taxa (environmental effects), but there was no consistent pattern for individual‐level richness (individual specialization). Together, our results show that maintenance of large host populations contributes to the maintenance of gut microbiome diversity in wild mammals.
-
Abstract 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, Batrachochytrium dendrobatidis (Bd). Skin microbial communities of laboratory-reared mountain yellow-legged frogs were tracked through three experimental phases: prior to Bd infection, after Bd infection (disturbance), and after clearing Bd infection (recovery period). Bd infection disturbed microbiome composition and altered the relative abundances of several dominant bacterial taxa. After Bd infection, frogs were treated with an antifungal drug that cleared Bd infection, but this did not lead to recovery of microbiome composition (measured as Unifrac distance) or relative abundances of dominant bacterial groups. These results indicate that Bd infection can lead to an alternate stable state in the microbiome of sensitive amphibians, or that microbiome recovery is extremely slow—in either case resilience is low. Furthermore, antifungal treatment and clearance of Bd infection had the additional effect of reducing microbial community variability, which we hypothesize results from similarity across frogs in the taxa that colonize community vacancies resulting from the removal of Bd. Our results indicate that the skin microbiota of mountain yellow-legged frogs has low resilience following Bd-induced disturbance and is further altered by the process of clearing Bd infection, which may have implications for the conservation of this endangered amphibian.