An official website of the United States government
Abstract Disturbance response and recovery are increasingly important in microbial ecology, as microbes may recover from disturbances differently than macro communities. Past disturbances can alter microbial community structure and their response to subsequent disturbance events, but it remains unclear if the same recovery patterns persist after long‐term exposure to stress. Here, we compare bacterial community composition in a community that experienced 2 years of monthly salinity addition disturbances with a community that has not experienced salinity additions. We then track the response and recovery to an additional salinity addition based on past disturbance exposure. We tested the following hypotheses: first, communities with a repeated disturbance history will have a different community composition than communities without a disturbance history; second, communities exposed to repeated disturbances will undergo a different recovery trajectory than communities experiencing a novel disturbance. We find that repeated disturbances alter community composition and affect community response and recovery to a subsequent disturbance after 2 years, primarily through increased resistance. This work enhances our understanding of microbial temporal dynamics and suggests that novel disturbances may pose a threat to microbial community structure and function.
more »
« less
Rapid changes in coastal ocean microbiomes uncoupled with shifts in environmental variables
Summary Disturbances, here defined as events that directly alter microbial community composition, are commonly studied in host‐associated and engineered systems. In spite of global change both altering environmental averages and increasing extreme events, there has been relatively little research into the causes, persistence and population‐level impacts of disturbance in the dynamic coastal ocean. Here, we utilize 3 years of observations from a coastal time series to identify disturbances based on the largest week‐over‐week changes in the microbiome (i.e. identifying disturbance as events that alter the community composition). In general, these microbiome disturbances were not clearly linked to specific environmental factors and responsive taxa largely differed, aside from SAR11, which generally declined. However, several disturbance metagenomes identified increased phage‐associated genes, suggesting that unexplained community shifts might be caused by increased mortality. Furthermore, a category 1 hurricane, the only event that would likely be classifieda priorias an environmental disturbance, was not an outlier in microbiome composition, but did enhance a bloom in seasonally abundant phytoplankton. Thus, as extreme environmental changes intensify, assumptions of what constitutes a disturbance should be re‐examined in the context of ecological history and microbiome responses.
more »
« less
- Award ID(s):
- 2033934
- PAR ID:
- 10444654
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Environmental Microbiology
- Volume:
- 24
- Issue:
- 9
- ISSN:
- 1462-2912
- Format(s):
- Medium: X Size: p. 4167-4177
- Size(s):
- p. 4167-4177
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
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 diaphanaand 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’smicrobiome 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.IMPORTANCEExaiptasia diaphanais an emerging model used to define the cellular and molecular mechanisms of coral-algal symbioses.E. diaphanaalso 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.more » « less
-
Abstract Climate change is causing rapid, unexpected changes to ecosystems through alteration to environmental regimes, modification of species interactions, and increased frequency and magnitude of disturbances. Yet, how the type of disturbance affects food webs remains ambiguous. Long‐term studies capturing ecosystem responses to extreme events are necessary to understand climate effects on species interactions and ecosystem resilience but remain rare. In the Gulf of Mexico, our 8‐year study captured two disturbances that had contrasting effects on predator abundance and cascading effects on estuarine food webs. In 2017, Hurricane Harvey destroyed fishing infrastructure, fishing activity declined, and sportfish populations increased ~40% while intermediate trophic levels that sportfish prey upon declined ~50%. Then, in 2021, a fish kill caused by freezing temperatures during Winter Storm Uri reduced sportfish populations by ~60% and intermediate trophic levels increased by over 250%. Sportfish abundance affected the abundance and size of oyster reef mesopredators. Excluding fish predators significantly altered oyster reef community structure. These results demonstrate how extreme events shape communities and influence their resilience based on their effects on top predators. Moreover, top‐down forces from sportfish are important in estuaries, persist through disturbances, and influence community resilience, highlighting the necessity of proper recreational fisheries management through extreme events.more » « less
-
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
-
Abstract Tropical forest understory regeneration occurs rapidly after disturbance with compositional trajectories that depend on species availability and environmental conditions. To predict future tropical forest regeneration dynamics, we need a deeper understanding of how pulse disturbance events, like hurricanes, interact with environmental variability to affect understory demography and composition. We examined fern and sapling mortality, recruitment, and community composition in relation to solar radiation and soil moisture using 17 years of forest dynamics data (2003–2019) from the Canopy Trimming Experiment in the Luquillo Experimental Forest, Puerto Rico. Solar radiation increased 150% and soil moisture increased 40% following canopy trimming of experimental plots relative to control plots. All plots were disturbed in 2017 by Hurricanes Irma and Maria, so experimentally trimmed plots presented the opportunity to study the effects of multiple hurricanes, while control plots isolated the effects of a single natural hurricane. Recruitment rates maximized at 0.14 individuals/plot/month for ferns and 0.20 stems/plot/month for saplings. Recruitment and mortality were distributed more evenly over the 17 years of monitoring in experimentally trimmed plots than in control plots; however, following Hurricane Maria demographic rates substantially increased in control plots only. In experimentally trimmed plots, the largest community compositional shifts occurred as a result of the trimming events, and compositional changes were greatest for control plots after Hurricane Maria in 2017. Pioneer tree and fern species increased in abundance in response to both simulated and natural hurricanes. Following Hurricane Maria, two dominant pioneer species,Cyathea arboreaandCecropia schreberiana, recruited abundantly, but only in control plots. In trimmed plots, increased solar radiation and soil moisture shifted understory species composition steadily toward pioneer and secondary‐successional species, with soil moisture interacting strongly with canopy trimming. Thus, both solar radiation and soil moisture are environmental drivers affecting pioneer species recruitment following disturbance, which interact with canopy opening following hurricanes. Our results suggest that if hurricane disturbances increase in frequency and severity, as suggested by climate change predictions, the understory regeneration of late‐successional species, such asManilkara bidentataandSloanea berteroana, which prefer deeper shade and slightly drier soil microsites, may become imperiled.more » « less
