LINKING ENVIRONMENTAL AND MICROBIAL PROCESSES FROM COMMUNITY TO GLOBAL SCALES

Life and the environment are inextricably interconnected. From the scale of a single microbe to the entire Earth system, biological and environmental processes have coevolved over billions of years into a complex system of interactions and feedbacks that together produce the geochemical and ecological conditions we observe around us. Community-scale processes result in net biogeochemical fluxes, which vary across regional and global scales in predictable patterns. At the community, regional, and global scale, this dissertation addresses a question central to our understanding of environmental microbial systems: How do microbial community interactions with their environment govern their functional and ecological role in the ecosystem, and how do environmental conditions shape the distribution and functional capacities of microbial genetic diversity? I demonstrate that microbial carbon cycling capacities in warm core ring waters originating from the Gulf Stream during an eddy intrusion event on the Mid-Atlantic Bight continental slope are distinct from those occurring in other shelf and shelf break water masses, illuminating the relationship between marine microbial communities and physical processes at the regional scale. As these eddy intrusion events likely increase in the future, these regional scale interactions have functional and biogeochemical implications in both present and future oceans. At the global scale, I build models to accurately predict genetic diversity of the key marine heterotroph SAR86 from environmental variables, identifying five previously unrecognized ecotypes within the SAR86 clade characterized by distinct environmental distributions, and resulting in the first global-resolution projections of SAR86 ecotype biogeography. From the community to the global scale, each level of inquiry demands solutions tailored to address the key challenges and opportunities unique to it, and new approaches are brought to bear at small and large scales, developing a more effective method to measure microbial activities in sediments to expand the range of environments for which microbial activity measurements are feasible, and providing a data discovery tool that harnesses the potential of publicly available sequencing datasets to scale data-driven discovery to ever more complex microbial systems.Doctor of Philosoph

Heterotrophic Extracellular Enzymatic Activity Across Geospatial Regimes in the Atlantic Ocean

Heterotrophic activity in the marine water column plays a crucial role in the carbon cycle, affecting the amount of particulate carbon available to higher trophic levels, the amount of organic carbon preserved over geological timescales, and the balance of CO2 between the oceans and the atmosphere. Extracellular enzymes initiate the breakdown of organic matter, hydrolyzing it into sizes small enough to transport into the cell. The variability of heterotrophic extracellular enzymatic activity across geospatial regimes in the ocean may have an important impact on global carbon flux, yet the patterns of hydrolysis across latitude and depth, and the factors driving these patterns, remain poorly understood. This project investigates the geospatial variability in extracellular hydrolysis of eight organic substrates, spanning surface to bottom water at latitudes from 38°S to 10°N in the Atlantic Ocean. The extent to which ten environmental variables impact hydrolysis patterns along this latitude-depth range is also discussed.Master of Scienc

Anaerobic Oxidation of Short-Chain Alkanes in Hydrothermal Sediments: Potential Influences on Sulfur Cycling and Microbial Diversity

Short-chain alkanes play a substantial role in carbon and sulfur cycling at hydrocarbon-rich environments globally, yet few studies have examined the metabolism of ethane $(C_2)$, propane $(C_3)$, and butane $(C_4)$ in anoxic sediments in contrast to methane $(C_1)$. In hydrothermal vent systems, short-chain alkanes are formed over relatively short geological time scales via thermogenic processes and often exist at high concentrations. The sediment-covered hydrothermal vent systems at Middle Valley (MV, Juan de Fuca Ridge) are an ideal site for investigating the anaerobic oxidation of $C_1–C_4$ alkanes, given the elevated temperatures and dissolved hydrocarbon species characteristic of these metalliferous sediments. We examined whether MV microbial communities oxidized $C_1–C_4$ alkanes under mesophilic to thermophilic sulfate-reducing conditions. Here we present data from discrete temperature (25, 55, and $75^{\circ}C$) anaerobic batch reactor incubations of MV sediments supplemented with individual alkanes. Co-registered alkane consumption and sulfate reduction (SR) measurements provide clear evidence for $C_1–C_4$ alkane oxidation linked to SR over time and across temperatures. In these anaerobic batch reactor sediments, 16S ribosomal RNA pyrosequencing revealed that Deltaproteobacteria, particularly a novel sulfate-reducing lineage, were the likely phylotypes mediating the oxidation of $C_2–C_4$ alkanes. Maximum $C_1–C_4$ alkane oxidation rates occurred at $55^{\circ}C$, which reflects the mid-core sediment temperature profile and corroborates previous studies of rate maxima for the anaerobic oxidation of methane (AOM). Of the alkanes investigated, $C_3$ was oxidized at the highest rate over time, then $C_4$, $C_2$, and $C_1$, respectively. The implications of these results are discussed with respect to the potential competition between the anaerobic oxidation of $C_2–C_4$ alkanes with AOM for available oxidants and the influence on the fate of $C_1$ derived from these hydrothermal systems.Molecular and Cellular BiologyOrganismic and Evolutionary Biolog

Particles act as ‘specialty centers’ with expanded enzymatic function throughout the water column in the western North Atlantic

Heterotrophic bacteria initiate the degradation of high molecular weight organic matter by producing an array of extracellular enzymes to hydrolyze complex organic matter into sizes that can be taken up into the cell. These bacterial communities differ spatially and temporally in composition, and potentially also in their enzymatic complements. Previous research has shown that particle-associated bacteria can be considerably more active than bacteria in the surrounding bulk water, but most prior studies of particle-associated bacteria have been focused on the upper ocean - there are few measurements of enzymatic activities of particle-associated bacteria in the mesopelagic and bathypelagic ocean, although the bacterial communities in the deep are dependent upon degradation of particulate organic matter to fuel their metabolism. We used a broad suite of substrates to compare the glucosidase, peptidase, and polysaccharide hydrolase activities of particle-associated and unfiltered seawater microbial communities in epipelagic, mesopelagic, and bathypelagic waters across 11 stations in the western North Atlantic. We concurrently determined bacterial community composition of unfiltered seawater and of samples collected via gravity filtration (>3 μm). Overall, particle-associated bacterial communities showed a broader spectrum of enzyme activities compared with unfiltered seawater communities. These differences in enzymatic activities were greater at offshore than at coastal locations, and increased with increasing depth in the ocean. The greater differences in enzymatic function measured on particles with depth coincided with increasing differences in particle-associated community composition, suggesting that particles act as ‘specialty centers’ that are essential for degradation of organic matter even at bathypelagic depths

Heterotrophic Extracellular Enzymatic Activities in the Atlantic Ocean Follow Patterns Across Spatial and Depth Regimes

Heterotrophic microbial communities use extracellular enzymes to initialize degradation of high molecular weight organic matter in the ocean. The potential of microbial communities to access organic matter, and the resultant rates of hydrolysis, affect the efficiency of the biological pump as well as the rate and location of organic carbon cycling in surface and deep waters. In order to investigate spatial- and depth-related patterns in microbial enzymatic capacities in the ocean, we measured hydrolysis rates of six high-molecular-weight polysaccharides and two low-molecular-weight substrate proxies at sites spanning 38°S to 10°N in the Atlantic Ocean, and at six depths ranging from surface to bottom water. In surface to upper mesopelagic waters, the spectrum of substrates hydrolyzed followed distinct patterns, with hydrolytic assemblages more similar vertically within a single station than at similar depths across multiple stations. Additionally, the proportion of total hydrolysis occurring above the pycnocline, and the spectrum of substrates hydrolyzed in mesopelagic and deep waters, was positively related to the strength of stratification at a site, while other physichochemical parameters were generally poor predictors of the measured hydrolysis rates. Spatial as well as depth-driven constraints on heterotrophic hydrolytic capacities result in broad variations in potential carbon-degrading activity in the ocean. The spectrum of enzymatic capabilities and rates of hydrolysis in the ocean, and the proportion of organic carbon hydrolyzed above the permanent thermocline, may influence the efficiency of the biological pump and net carbon export across distinct latitudinal and depth regions

Gulf Stream Ring Water Intrusion on the Mid-Atlantic Bight Continental Shelf Break Affects Microbially Driven Carbon Cycling

Warm core, anticyclonic rings that spin off from the Gulf Stream circulate through the region directly offshore of the Mid-Atlantic Bight. If a warm core ring reaches the continental shelf break, its warm, highly saline water may subduct under cooler, fresher continental shelf surface water, resulting in subsurface waters at the shelf break and over the upper continental slope with high temperatures and salinities and distinct physical and chemical properties characteristic of Gulf Stream water. Such intruding water may also have microbial communities with distinct functional capacities, which may in turn affect the rate and nature of carbon cycling in this coastal/shelf environment. However, the functional capabilities of microbial communities within ring intrusion waters relative to surrounding continental shelf waters are largely unexplored. We investigated microbial community capacity to initiate organic matter remineralization by measuring hydrolysis of a suite of polysaccharide, peptide, and glucose substrates along a transect oriented across the Mid-Atlantic Bight shelf, shelf break, and upper slope. At the outermost sampling site, warm and salty water derived from a Gulf Stream warm core ring was present in the lower portion of the water column. This water exhibited hydrolytic capacities distinct from other sampling sites, and exhibited lower heterotrophic bacterial productivity overall. Warm core rings adjacent to the Mid-Atlantic Bight shelf have increased in frequency and duration in recent years. As the influence of warm core rings on the continental shelf and slope increases in the future, the rate and nature of organic matter remineralization on the continental shelf may also shift

Global ecotypes in the ubiquitous marine clade SAR86.

SAR86 is an abundant and ubiquitous heterotroph in the surface ocean that plays a central role in the function of marine ecosystems. We hypothesized that despite its ubiquity, different SAR86 subgroups may be endemic to specific ocean regions and functionally specialized for unique marine environments. However, the global biogeographical distributions of SAR86 genes, and the manner in which these distributions correlate with marine environments, have not been investigated. We quantified SAR86 gene content across globally distributed metagenomic samples and modeled these gene distributions as a function of 51 environmental variables. We identified five distinct clusters of genes within the SAR86 pangenome, each with a unique geographic distribution associated with specific environmental characteristics. Gene clusters are characterized by the strong taxonomic enrichment of distinct SAR86 genomes and partial assemblies, as well as differential enrichment of certain functional groups, suggesting differing functional and ecological roles of SAR86 ecotypes. We then leveraged our models and high-resolution, remote sensing-derived environmental data to predict the distributions of SAR86 gene clusters across the world's oceans, creating global maps of SAR86 ecotype distributions. Our results reveal that SAR86 exhibits previously unknown, complex biogeography, and provide a framework for exploring geographic distributions of genetic diversity from other microbial clades

Global ecotypes in the ubiquitous marine clade SAR86.

SAR86 is an abundant and ubiquitous heterotroph in the surface ocean that plays a central role in the function of marine ecosystems. We hypothesized that despite its ubiquity, different SAR86 subgroups may be endemic to specific ocean regions and functionally specialized for unique marine environments. However, the global biogeographical distributions of SAR86 genes, and the manner in which these distributions correlate with marine environments, have not been investigated. We quantified SAR86 gene content across globally distributed metagenomic samples and modeled these gene distributions as a function of 51 environmental variables. We identified five distinct clusters of genes within the SAR86 pangenome, each with a unique geographic distribution associated with specific environmental characteristics. Gene clusters are characterized by the strong taxonomic enrichment of distinct SAR86 genomes and partial assemblies, as well as differential enrichment of certain functional groups, suggesting differing functional and ecological roles of SAR86 ecotypes. We then leveraged our models and high-resolution, remote sensing-derived environmental data to predict the distributions of SAR86 gene clusters across the world's oceans, creating global maps of SAR86 ecotype distributions. Our results reveal that SAR86 exhibits previously unknown, complex biogeography, and provide a framework for exploring geographic distributions of genetic diversity from other microbial clades