Microbiome-centered Approaches to Marine Disturbance Ecology

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2023

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Abstract

As climate change continues to alter our global ecosystem, ecological disturbances will increase in both frequency and intensity. These ecological disturbances have been shown to significantly impact microbial communities, often altering composition and/or function. However, while disturbance events are commonly studied in host-associated and engineered systems, there has been relatively little research into the causes, persistence and population-level impacts of disturbance in the dynamic ocean. Furthermore, the research that has been performed on marine microbiome responses to perturbation has been limited to the a priori identification of disturbances, limiting the scope of current research to events considered disturbances from the researchers’ perspective (e.g. hurricanes, contamination, etc.). In this dissertation, I investigate ecological disturbances using a microbiome-centered approach focusing on the role of perturbation in shaping marine microbial assemblies. In my first chapter, I provide an overview of current and historical theoretical frameworks in disturbance ecology and discuss the potential limitations of these approaches. In my second chapter, I apply a microbiome-centered approach to identify disturbances in the coastal ocean. Using three years of observations from a coastal time series, we identified ten disturbance events based on the largest week-over-week changes in microbiome composition. These microbiome disturbances were not clearly linked to specific environmental changes and did not exhibit common responsive taxa. Further, a category 1 hurricane, the only event that would likely be classified a priori as an environmental disturbance, was not an outlier in microbiome composition, but did enhance a bloom in seasonally-abundant phytoplankton. Although large storms can have significant impacts on marine microbiomes, we propose that unmeasured disturbances may have large impacts on the microbiome and may only be detected from a microbial perspective. In my third chapter, I investigate a cyclonic, Gulf Stream frontal eddy as a potential spatial disturbance that can trap and transport microbial communities along this current. By parsing our samples based on microbial community composition, we were able to identify an eddy-specific microbiome even in highly dynamic frontal zones. Furthermore, the eddy microbiome was defined by a higher abundance of a specific high-light Prochlorococcus ASV that was also enriched in slope waters, suggesting that the eddy may harbor signatures of the nearshore community entrapped during eddy formation. Although the eddy microbiome is distinct from the Gulf Stream’s, especially in cyanobacteria (e.g. lower Trichodesmium and higher Prochlorococcus), it is most similar to the Gulf Stream, suggesting eddy microbiome assembly favors environmental filtering over historical contingencies. In my final chapter, I investigate the proximal drivers of hurricane-driven responses in coastal microbiomes using experimental incubations intended to mimic specific hurricane attributes. Coastal microbiomes experienced either a dilution, intended to mimic the initial dilution of the bacterioplankton community from extensive precipitation, or to a daily addition of dissolved organic matter (DOM) intended to mimic a hurricane-induced phytoplankton bloom. The dilution treatment, which represents a more immediate and stochastic effect of hurricane landfall, led to changes in several taxonomic groups, while the DOM treatment, which represents the more latent and deterministic phase of hurricane effects that peaks days to weeks after landfall induced a consistent change among a few taxa. Thus, manipulating specific hurricane-associated drivers can help to differentiate responses to different hurricane components. Together, my dissertation approaches disturbances in time, space and complexity from a microbiome-centered perspective. By broadening our concept of disturbance to include a microbiome-centered perspective, we can better identify how these events shape the microbiome. As global climate change and the associated increase in ecological disturbances i continues to alter our ecosystems, we must understand the full scope of these disturbance responses and the potential ramifications for critical biogeochemical cycles as we strive to predict and mitigate ecosystem changes.

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Gronniger, Jessica (2023). Microbiome-centered Approaches to Marine Disturbance Ecology. Dissertation, Duke University. Retrieved from https://hdl.handle.net/10161/27634.

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