Microbial assemblage dynamics of disturbed, tropical, high-island estuarine systems

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2024

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Marine microbes exhibit characteristic distributions both temporally and across physiochemical gradients that drive biogeochemical cycling. Understanding how the taxonomic and functional diversity of microbial assemblages change in response to disturbances is critical for identifying vulnerabilities or critical tipping points toward alternative stable states to an ecosystem’s microbe-dependent biogeochemical cycling. Environmental conditions, trophic interactions, immigration from adjacent ecosystems, and the history and evolution of community members underlie microbial assemblage shifts, and the relative contribution of these factors varies across ecosystems. Better characterization of how these factors drive microbial assemblage dynamics is necessary to build robust assemblage models, improve our understanding of microbial function and resilience in ecosystems, and can provide insight into the functions of individual clades within distinct ecological niches. While several temperate estuaries serve as systems for studying the effects of anthropogenic and climatic impacts on the coastal environment, few cognate systems have been thoroughly examined in the tropics. We set out to provide a baseline understanding of microbial responses to a variety of disturbances faced by Pacific, high-island communities. We took a genomic approach to characterize planktonic microbial assemblages from Hawaiʻi [RA1] and American Samoa estuaries and embayments. At Heʻeia Fishpond (HFP) on the island of Oʻahu, we used 16S V4 and 18S V9 amplicon sequencing to characterize microbial resistance, resilience, and recovery in response to diverse external disturbances during a year-long sampling campaign (Chapters 2 and 4). In HFP, we found that prokaryotic diversity recovered following a tropical storm to pre-storm levels within two weeks and were lowly resistant but highly resilient to multiple tropical storms and a SSTA. A marked shift in the dominant primary producers from cyanobacteria-dominated assemblages to diatom-dominated assemblages occurred immediately following and up to at least one week following the largest tropical storm. Eukaryotic assemblages did not immediately recover within two weeks of a tropical storm. However, we observed strong successional shifts in these groups, possibly driven by seasonal changes, that contributed to microbial recovery on longer time scales. In this manner, seasonal forcing may serve as a stabilizing mechanism for disturbed microbial assemblages. Notably, we characterized a marked shift in the most dominant microeukaryote group from Cyclotella to Chaetoceros in the last quarter of our rigorous sampling campaign. We hypothesize that this shift is the result of increased freshwater input and mixing achieved through intensive biocultural restoration efforts, with potentially profound implications to fishpond food-web dynamics. We also investigated disturbed plankton and biofilm microbial assemblages using 16S V4 amplicon sequencing and quantitative polymerase chain reaction (qPCR) across four watersheds on the island of Tutuila, American Samoa[RA2] . How does nitrogen loading, at different scales, alter reef microbial assemblages? And how does the capacity of reef microbial assemblages to cycle nitrogen respond to altered nitrogen input (Chapter 3)? [RA3] In Tutuila watersheds, we found that both plankton and biofilm assemblages were differentiated between nitrogen concentrations but with distinct patterns. We detected areas of higher-than-expected nitrogen contamination and microbial metabolisms supporting nitrogen loss at two of the more impacted sites, one of which was also identified as a potential hotspot for algal blooms. We identified novel microbial indicators with metabolisms directly linked to the consumption and cycling of NH3, the concentration and cycling ability of which was found to be critically elevated in Tutuila’s more urbanized watersheds. These analyses support the findings of mesocosm experiments approximating biofilm development of coastal reefs experiencing nutrient enrichment and provide in-situ evidence that biofilms are strongly influenced by nutrient pollution and the composition of DOM altered by anthropogenic activities in coral reef ecosystems. Taken together, my work provides a foundational understanding of important food-web and nutrient cycling contributors in tropical estuarine environments undergoing different types of disturbances. This research establishes HFP as an ecosystem model for tropical, high-island estuaries. Finally, my work was co-produced and co-published with the local community stakeholders and stewards that care for these remarkable places and demonstrates how ʻōiwi methodologies support and empower communities to protect their natural and cultural resources.

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Microbiology, Ecology, Natural resource management, bacterial, disturbance, microbial ecology, microbial eukaryotes, resilience, storms

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283 pages

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