Bacterial niche differentiation in Arctic sandy surface sediments

Permeable sandy sediments cover at least half of the continental margins and are regions of high biogeochemical activity. Central to remineralization processes in sediments are heterotrophic microbial communities, which possess a vast array of metabolic capabilities that allow them to use diverse substrates, ranging from complex organic matter to simple sugars and amino acids. These benthic microorganisms colonize surfaces of sand grains, as well as the interstitial porewater. This thesis aims to improve our knowledge of carbon cycling by benthic bacterial communities using a novel fractionation method which separates cells in sandy surface sediments based on their attachment to the grains. The work focuses on high latitude environments, specifically Isfjorden, Svalbard (78°N), which experiences extreme seasonality in primary productivity with prolonged periods of continuous daylight followed by a rapid transition to months of continuous darkness.
Collecting undisturbed sediment samples is the critical first step in disentangling niches and microhabitats within surface sediments. Thus, in this thesis a new small and lightweight sediment sampler, the Ellrott grab, was developed, which was designed specifically for sampling undisturbed sandy surface sediments with the porewater and overlying seawater (Chapter 2). By comparing oxygen profiles measured in situ with those in cores subsampled from the grab, I showed that the Ellrott grab causes minimal disturbance to the sample.
Furthermore, a novel fractionation method that separates microorganisms in the porewater (PW) from those loosely attached (LA) and firmly attached (FA) to the grains was developed (Chapter 3). The PW and LA cells, which comprised 3% and 8-13% of cells, respectively, were significantly enriched in aerobic heterotrophs and had faster per-cell oxygen consumption and laminarin hydrolysis rates compared to the FA fraction. In contrast, the FA fraction (84-89% of cells) was significantly enriched in anaerobes such as sulfate reducers. I hypothesize that these fractions occupy distinct niches in surface sediments: the FA fraction likely consists of cells colonizing protected areas on the grain, but are more diffusion-limited. On the other hand, the PW and LA fractions are less resource-limited but abrasion and grazing may keep their cell numbers low. These differences in composition and activity could point towards distinct contributions by these fractions to benthic carbon cycling. Next, the composition and activities of the sediment fractions across polar day and polar night in Isfjorden were compared (Chapter 4). During polar day, taxa specialized in degrading high molecular weight organic matter increased in relative abundance in the PW and LA fractions. These two fractions also showed increased laminarin hydrolysis rates. While the FA fraction remained more stable, I observed an increase in sulfate reducers in this fraction during polar night. Across seasons, Woeseia and Maribacter remained abundant in the FA fraction. I propose a partitioning of the benthic bacterial community into seasonal and stable microbial guilds, wherein the PW and LA fractions comprise the seasonally responsive communities. On the other hand, the FA fraction comprises the more stable community, potentially utilizing constantly available or less labile substrates.
The hydrolysis and uptake of mucin, an animal-derived glycoprotein, by the fractions across seasons was the focus of Chapter 5. During polar day, maximum extracellular hydrolysis rates in the PW and LA increased, while the maximum rate did not fluctuate in the FA. Selfish uptake (i.e., taking up oligosaccharides into the periplasm), was mainly mediated by Verrucomicrobiota and Planctomycetota, and was restricted to a maximum of 2% of the microbial community.
In Chapter 6, I contextualize my findings from this thesis by presenting macro-scale observations from the station in Isfjorden. Then, I synthesize the key findings presented across the chapters, and provide a cohesive overview on how this work advances our understanding of carbon cycling processes in sandy surface sediments. Finally, I propose potential directions for future research, identifying approaches that can further investigate the remaining open questions and new hypotheses generated from this thesis.