The Balance of Bottom-up and Top-down Processes in Regulating the Phenology of Closely Related Populations of Marine Cyanobacteria

Abstract

As cornerstones of marine ecosystems, cyanobacteria display repeatable seasonal and inter-annual patterns in community abundance and structure that help to drive the primary production of most near surface locations. Many factors have been hypothesized to account for their seasonal patterns including bottom-up (i.e. growth related) and top-down (i.e. mortality) processes. While their impact is widely recognized, the relative importance of bottom-up and top-down factors in structuring these communities is not well-characterized. Further, most previous studies have primarily explored these patterns and regulating mechanisms at course phylogenetic scale, but there is growing evidence that fine genetic diversity is important to the ecology of these organisms. To address these knowledge gaps, in this dissertation, I first did a comparative analysis to determine the regulating mechanisms of cyanobacteria community at fine scales across ecologies/trophic levels using data from a temperate coastal ocean time series (Piver’s Island Coastal Observatory – Beaufort, NC, USA) with strong, repeating seasonality in environmental variables. Comparisons were made between cyanobacteria and SAR11 because they are dominant autotrophic and heterotrophic microbes respectively, in our study site and they both harbor substantial fine scale phylogenetic diversity that is structured along temporal and spatial environmental gradients. Results show that finer-scale (oligotype) resolution better captures the complexity of the Synechococcaceae and SAR11 community seasonal shifts compared to 97% operational taxonomic units (OTUs). In both taxa closely-related strains exhibit similar recurring patterns with Synechococcaceae showing stronger seasonality. However, these similarities erode at a coarser phylogenetic depth in SAR11 compared to Synechococcaceae. These results suggest that to enhance mechanistic insight, ecological and biogeochemical processes of these communities should be assessed at the finest population level resolution possible and that phylogenetic relationships offer insight into these patterns. Second, I combined molecular community analysis with a traditional dilution technique to develop a novel technique to estimate the specific growth rates and mortality rates of cyanobacteria at the finest phylogenetic resolution. To assess this novel technique, I compared traditional and novel techniques in estimating the growth rates of model cyanobacteria in laboratory culture and also natural phytoplankton communities collected from local seawaters. The comparable growth estimates prove the reliability and applicability of our new approach in exploring the relative importance of bottom-up and top-down processes in shaping coastal cyanobacteria at the finest scale. Finally, I utilized the new approach at our coastal sampling site to assess the balance of bottom-up and top-down controls in regulating natural cyanobacteria communities across seasons. I found that coastal cyanobacteria populations have different daily and seasonal patterns of growth and mortality at the amplicon sequence variant (ASV) level. Such patterns may explain the seasonal patterns in abundance and structure observed. Together, my dissertation contributes new insights into the mechanisms of phenology of cyanobacteria across taxonomic ranks in the coastal oceans and more broadly clarifies marine microbial community assembly and niche-differentiation in a changing environment. The newly developed approach will help disentangle the effects of environment variables and predation pressure in driving the composition and function of marine microbial communities across seasonal cycles and opens lines of inquiry into how closely related, but genomically distinct populations, can have dramatically different growth and mortality rates.