Seasonal environmental variability drives microdiversity within a coastal Synechococcus population.

Marine microbes often show a high degree of physiological or ecological diversity below the species level. This microdiversity raises questions about the processes that drive diversification and permit coexistence of diverse yet closely related marine microbes, especially given the theoretical efficiency of competitive exclusion. Here, we provide insight with an 8-year time series of diversity within Synechococcus, a widespread and important marine picophytoplankter. The population of Synechococcus on the Northeast U.S. Shelf is comprised of six main types, each of which displays a distinct and consistent seasonal pattern. With compositional data analysis, we show that these patterns can be reproduced with a simple model that couples differential responses to temperature and light with the seasonal cycle of the physical environment. These observations support the hypothesis that temporal variability in environmental factors can maintain microdiversity in marine microbial populations. We also identify how seasonal diversity patterns directly determine overarching Synechococcus population abundance features.

Seasons of Syn.

Synechococcus is a widespread and important marine primary producer. Time series provide critical information for identifying and understanding the factors that determine abundance patterns. Here, we present the results of analysis of a 16-yr hourly time series of Synechococcus at the Martha's Vineyard Coastal Observatory, obtained with an automated, in situ flow cytometer. We focus on understanding seasonal abundance patterns by examining relationships between cell division rate, loss rate, cellular properties (e.g., cell volume, phycoerythrin fluorescence), and environmental variables (e.g., temperature, light). We find that the drivers of cell division vary with season; cells are temperature-limited in winter and spring, but light-limited in the fall. Losses to the population also vary with season. Our results lead to testable hypotheses about Synechococcus ecophysiology and a working framework for understanding the seasonal controls of Synechococcus cell abundance in a temperate coastal system.

Dynamics and functional diversity of the smallest phytoplankton on the Northeast US Shelf.

Picophytoplankton are the most abundant primary producers in the ocean. Knowledge of their community dynamics is key to understanding their role in marine food webs and global biogeochemical cycles. To this end, we analyzed a 16-y time series of observations of a phytoplankton community at a nearshore site on the Northeast US Shelf. We used a size-structured population model to estimate in situ division rates for the picoeukaryote assemblage and compared the dynamics with those of the picocyanobacteria Synechococcus at the same location. We found that the picoeukaryotes divide at roughly twice the rate of the more abundant Synechococcus and are subject to greater loss rates (likely from viral lysis and zooplankton grazing). We describe the dynamics of these groups across short and long timescales and conclude that, despite their taxonomic differences, their populations respond similarly to changes in the biotic and abiotic environment. Both groups appear to be temperature limited in the spring and light limited in the fall and to experience greater mortality during the day than at night. Compared with Synechococcus, the picoeukaryotes are subject to greater top-down control and contribute more to the region's primary productivity than their standing stocks suggest.

Seasonal Succession and Spatial Patterns of Synechococcus Microdiversity in a Salt Marsh Estuary Revealed through 16S rRNA Gene Oligotyping.

Synechococcus are ubiquitous and cosmopolitan cyanobacteria that play important roles in global productivity and biogeochemical cycles. This study investigated the fine scale microdiversity, seasonal patterns, and spatial distributions of Synechococcus in estuarine waters of Little Sippewissett salt marsh (LSM) on Cape Cod, MA. The proportion of Synechococcus reads was higher in the summer than winter, and higher in coastal waters than within the estuary. Variations in the V4-V6 region of the bacterial 16S rRNA gene revealed 12 unique Synechococcus oligotypes. Two distinct communities emerged in early and late summer, each comprising a different set of statistically co-occurring Synechococcus oligotypes from different clades. The early summer community included clades I and IV, which correlated with lower temperature and higher dissolved oxygen levels. The late summer community included clades CB5, I, IV, and VI, which correlated with higher temperatures and higher salinity levels. Four rare oligotypes occurred in the late summer community, and their relative abundances more strongly correlated with high salinity than did other co-occurring oligotypes. The analysis revealed that multiple, closely related oligotypes comprised certain abundant clades (e.g., clade 1 in the early summer and clade CB5 in the late summer), but the correlations between these oligotypes varied from pair to pair, suggesting they had slightly different niches despite being closely related at the clade level. Lack of tidal water exchange between sampling stations gave rise to a unique oligotype not abundant at other locations in the estuary, suggesting physical isolation plays a role in generating additional microdiversity within the community. Together, these results contribute to our understanding of the environmental and ecological factors that influence patterns of Synechococcus microbial community composition over space and time in salt marsh estuarine waters.

Physiological and ecological drivers of early spring blooms of a coastal phytoplankter.

Climate affects the timing and magnitude of phytoplankton blooms that fuel marine food webs and influence global biogeochemical cycles. Changes in bloom timing have been detected in some cases, but the underlying mechanisms remain elusive, contributing to uncertainty in long-term predictions of climate change impacts. Here we describe a 13-year hourly time series from the New England shelf of data on the coastal phytoplankter Synechococcus, during which the timing of its spring bloom varied by 4 weeks. We show that multiyear trends are due to temperature-induced changes in cell division rate, with earlier blooms driven by warmer spring water temperatures. Synechococcus loss rates shift in tandem with division rates, suggesting a balance between growth and loss that has persisted despite phenological shifts and environmental change.

Diversity of Synechococcus at the Martha's Vineyard Coastal Observatory: Insights from Culture Isolations, Clone Libraries, and Flow Cytometry.

The cyanobacterium Synechococcus is a ubiquitous, important phytoplankter across the world's oceans. A high degree of genetic diversity exists within the marine group, which likely contributes to its global success. Over 20 clades with different distribution patterns have been identified. However, we do not fully understand the environmental factors that control clade distributions. These factors are likely to change seasonally, especially in dynamic coastal systems. To investigate how coastal Synechococcus assemblages change temporally, we assessed the diversity of Synechococcus at the Martha's Vineyard Coastal Observatory (MVCO) over three annual cycles with culture-dependent and independent approaches. We further investigated the abundance of both phycoerythrin (PE)-containing and phycocyanin (PC)-only Synechococcus with a flow cytometric setup that distinguishes PC-only Synechococcus from picoeukaryotes. We found that the Synechococcus assemblage at MVCO is diverse (13 different clades identified), but dominated by clade I representatives. Many clades were only isolated during late summer and fall, suggesting more favorable conditions for isolation at this time. PC-only strains from four different clades were isolated, but these cells were only detected by flow cytometry in a few samples over the time series, suggesting they are rare at this site. Within clade I, we identified four distinct subclades. The relative abundances of each subclade varied over the seasonal cycle, and the high Synechococcus cell concentration at MVCO may be maintained by the diversity found within this clade. This study highlights the need to understand how temporal aspects of the environment affect Synechococcus community structure and cell abundance.

Diel size distributions reveal seasonal growth dynamics of a coastal phytoplankter.

Phytoplankton account for roughly half of global primary production; it is vital that we understand the processes that control their abundance. A key process is cell division. We have, however, been unable to estimate division rate in natural populations at the appropriate timescale (hours to days) for extended periods of time (months to years). For phytoplankton, the diel change in cell size distribution is related to division rate, which offers an avenue to obtain estimates from in situ observations. We show that a matrix population model, fit to hourly cell size distributions, accurately estimates division rates of both cultured and natural populations of Synechococcus. Application of the model to Synechococcus at the Martha's Vineyard Coastal Observatory provides an unprecedented view that reveals a distinct seasonality in division rates. This information allows us to separate the effects of growth and loss quantitatively over an entire seasonal cycle. We find that division and loss processes are tightly coupled throughout the year. The large seasonal changes in cell abundance are the result of periods of time (weeks to months) when there are small systematic differences that favor either net growth or loss. We also find that temperature plays a critical role in limiting division rate during the annual spring bloom. This approach opens a path to quantify the role of Synechococcus in ecological and biogeochemical processes in natural systems.