Microbial community composition, extracellular enzymatic activities, and structure-function relationships in the central Arctic Ocean, a high-latitude fjord, and the North Atlantic Ocean

Due to their abundance, diversity, and capabilities to transform and metabolize diverse compounds, microbial communities regulate biogeochemical cycles on micro-, regional, and global scales. The activities of microbial communities affect the flow of matter, energy sources of other organisms, and human health, as well as other aspects of life. Yet, the composition, diversity, and ecological roles of microbes in parts of the global oceans—from the high latitudes to the deep water column—remain underexplored. Drawing from microbiological, oceanographic, and ecological concepts, this dissertation explores several fundamental topics: 1) the manner in which hydrographic conditions influence microbial community composition; 2) the ability of these microbial communities across environmental and depth gradients to hydrolyze organic compounds; and 3) microbial structure-function relationships in different habitats and under altered environmental conditions. In the central Arctic Ocean, the composition and enzymatic function of pelagic, particle associated, and benthic bacterial communities varied with depth and region, in parallel with specific hydrographic features. The microbial structure-function relationship in the pelagic realm indicated functional redundancy, suggesting that bacterial compositional shifts—in response to the changing Arctic—may have complex and less predictable functional consequences than previously anticipated. In Tyrolerfjord-Young Sound, northeast Greenland, microbial enzymatic activity patterns were investigated in rivers and within the fjord. Activity patterns correlated with the composition of bacterial communities and dissolved organic matter in the same waters, suggesting that factors extrinsic (organic matter supply) and intrinsic (composition) to microbial communities may, in concert, influence their heterotrophic activities. Finally, functional consequences of differences in community composition were further explored in the North Atlantic. Enriched with high molecular weight organic matter, compositionally-distinct microbial communities exhibited convergent and divergent successional patterns. While convergent features were driven by several initially rare taxa, overarching successional differences in microbial community composition and enzymatic profiles provide evidence for the functional significance of community structure. The integration of community compositional analyses and enzymatic activity measurements has provided valuable information on the identity, ecological roles, and environmental sensitivity of microbial communities in previously underexplored oceanic regions and depths. These insights can be used to evaluate the potential for environmental changes to alter marine microbial community structure and function.Doctor of Philosoph

Impacts of a large storm disturbance on microbial community composition in the Tar River of North Carolina

Microbial community response to environmental disturbances is a crucial topic to investigate as changes in community composition can have widespread consequences on an ecosystem. Microbes are generally sensitive to disturbances, but can exhibit resilience, capable of returning to pre-disturbance composition or achieving an alternative stable state. Here, I investigate microbial community composition in the Tar River of North Carolina from November 2010 to November 2011, capturing the landfall of Hurricane Irene on August 27, 2011. Using 16S ribosomal RNA sequence analyses, I investigated the response of riverine microbial communities to Hurricane Irene and found a likely hurricane-induced change or signature. A finer analysis on two major groups, Betaproteobacteria and Verrucomicrobia, demonstrate the ecophysiological flexibility of their members, persisting and, in some instances, proliferating in the face of disturbance. The alteration in Tar River microbial community composition indicates sensitivity to disturbances, although a larger sampling window is required to assess resilience.Master of Scienc

Riverine Bacterial Communities Reveal Environmental Disturbance Signatures within the Betaproteobacteria and Verrucomicrobia

Riverine bacterial communities play an essential role in the biogeochemical coupling of terrestrial and marine environments, transforming elements and organic matter in their journey from land to sea. However, precisely due to the fact that rivers receive significant terrestrial input, the distinction between resident freshwater taxa vs. land-derived microbes can often become ambiguous. Furthermore, ecosystem perturbations could introduce allochthonous microbial groups and reshape riverine bacterial communities. Using full- and partial-length 16S ribosomal RNA gene sequences, we analyzed the composition of bacterial communities in the Tar River of North Carolina from November 2010 to November 2011, during which a natural perturbation occurred: the inundation of the lower reaches of an otherwise drought-stricken river associated with Hurricane Irene, which passed over eastern North Carolina in late August 2011. This event provided the opportunity to examine the microbiological, hydrological, and geochemical impacts of a disturbance, defined here as the large freshwater influx into the Tar River, superimposed on seasonal changes or other ecosystem variability independent of the hurricane. Our findings demonstrate that downstream communities are more taxonomically diverse and temporally variable than their upstream counterparts. More importantly, pre- vs. post-disturbance taxonomic comparison of the freshwater-dominant Betaproteobacteria class and the phylum Verrucomicrobia reveal a disturbance signature of previously undetected taxa of diverse origins. We use known traits of closely-related taxa to interpret the ecological function of disturbance-associated bacteria, and hypothesize that carbon cycling was enhanced post-disturbance in the Tar River, likely due to the flux of organic carbon into the system associated with the large freshwater pulse. Our analyses demonstrate the importance of geochemical and hydrological alterations in structuring bacterial communities, and illustrate the response of temperate riverine bacteria on fine taxonomic scales to a disturbance

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

Multiomics in the central Arctic Ocean for benchmarking biodiversity change

Multiomics approaches need to be applied in the central Arctic Ocean to benchmark biodiversity change and to identify novel species and their genes. As part of MOSAiC, EcoOmics will therefore be essential for conservation and sustainable bioprospecting in one of the least explored ecosystems on Earth

Exoenzyme activities associated with sinking diatom aggregates incubated in rotating pressure and control tanks

The effect of increasing hydrostatic pressure on the microbial degradation, the organic matter composition, and the microbiome of 'marine snow' particles was studied in laboratory incubation experiments. Model aggregates were produced from the diatom Skeletonema marinoi and the natural microbial community of surface seawater collected in the Kattegat. The aggregates were incubated individually in rotating pressure and control tanks to keep them suspended during 20-day incubations in the dark and at 3°C. In the pressure tanks, hydrostatic pressure was increased at increments of 5 MPa per day to finally reach 100 MPa. This pressure scheme simulates the descent of diatom aggregates from the surface ocean down into a 10-km deep hadal trench. In the control tanks, pressure was always left at atmospheric level. The activities of 5 exoenzymes (leucine-aminopeptidase, beta-glucosidase, laminarase, pullulanase, chondroitin sulfatase) associated with diatom aggregates were determined using fluorescently labeled substrates. Volumetric exoenzyme activities were calculated from the temporal change in fluorophore concentrations and the individual aggregate volume for samples retrieved every 4-8 days throughout the 20-day incubation experiment

A sea change in microbial enzymes : Heterogeneous latitudinal and depth-related gradients in bulk water and particle-associated enzymatic activities from 30 degrees S to 59 degrees N in the Pacific Ocean

Heterotrophic microbes initiate the degradation of high molecular weight organic matter using extracellular enzymes. Our understanding of differences in microbial enzymatic capabilities, especially among particle-associated taxa and in the deep ocean, is limited by a paucity of hydrolytic enzyme activity measurements. Here, we measured the activities of a broad range of hydrolytic enzymes (glucosidases, peptidases, polysaccharide hydrolases) in epipelagic to bathypelagic bulk water (nonsize-fractionated), and on particles (>= 3 mu m) along a 9800 km latitudinal transect from 30 degrees S in the South Pacific to 59 degrees N in the Bering Sea. Individual enzyme activities showed heterogeneous latitudinal and depth-related patterns, with varying biotic and abiotic correlates. With increasing latitude and decreasing temperature, lower laminarinase activities sharply contrasted with higher leucine aminopeptidase (leu-AMP) and chondroitin sulfate hydrolase activities in bulk water. Endopeptidases (chymotrypsins, trypsins) exhibited patchy spatial patterns, and their activities can exceed rates of the widely measured exopeptidase, leu-AMP. Compared to bulk water, particle-associated enzymatic profiles featured a greater relative importance of endopeptidases, as well as a broader spectrum of polysaccharide hydrolases in some locations, and latitudinal and depth-related trends that are likely consequences of varying particle fluxes. As water depth increased, enzymatic spectra on particles and in bulk water became narrower, and diverged more from one another. These distinct latitudinal and depth-related gradients of enzymatic activities underscore the biogeochemical consequences of emerging global patterns of microbial community structure and function, from surface to deep waters, and among particle-associated taxa

Distinct bacterial succession and functional response to alginate in the South, Equatorial, and North Pacific Ocean

The availability of alginate, an abundant macroalgal polysaccharide, induces compositional and functional responses among marine microbes, but these dynamics have not been characterized across the Pacific Ocean. We investigated alginate-induced compositional and functional shifts (e.g., heterotrophic production, glucose turnover, hydrolytic enzyme activities) of microbial communities in the South Subtropical, Equatorial, and Polar Frontal North Pacific in mesocosms. We observed that shifts in response to alginate were site-specific. In the South Subtropical Pacific, prokaryotic cell counts, glucose turnover, and peptidase activities changed the most with alginate addition, along with the enrichment of the widest range of particle-associated taxa (161 amplicon sequence variants; ASVs) belonging to Alteromonadaceae, Rhodobacteraceae, Phormidiaceae, and Pseudoalteromonadaceae. Some of these taxa were detected at other sites but only enriched in the South Pacific. In the Equatorial Pacific, glucose turnover and heterotrophic prokaryotic production increased most rapidly; a single Alteromonas taxon dominated (60% of the community) but remained low (<2%) elsewhere. In the North Pacific, the particle-associated community response to alginate was gradual, with a more limited range of alginate-enriched taxa (82 ASVs). Thus, alginate-related ecological and biogeochemical shifts depend on a combination of factors that include the ability to utilize alginate, environmental conditions, and microbial interactions

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