Molecular physiology of Antarctic diatom natural assemblages and bloom event reveal insights into strategies contributing to their ecological success.

The continental shelf of the Western Antarctic Peninsula (WAP) is a highly variable system characterized by strong cross-shelf gradients, rapid regional change, and large blooms of phytoplankton, notably diatoms. Rapid environmental changes coincide with shifts in plankton community composition and productivity, food web dynamics, and biogeochemistry. Despite the progress in identifying important environmental factors influencing plankton community composition in the WAP, the molecular basis for their survival in this oceanic region, as well as variations in species abundance, metabolism, and distribution, remains largely unresolved. Across a gradient of physicochemical parameters, we analyzed the metabolic profiles of phytoplankton as assessed through metatranscriptomic sequencing. Distinct phytoplankton communities and metabolisms closely mirrored the strong gradients in oceanographic parameters that existed from coastal to offshore regions. Diatoms were abundant in coastal, southern regions, where colder and fresher waters were conducive to a bloom of the centric diatom, Actinocyclus. Members of this genus invested heavily in growth and energy production; carbohydrate, amino acid, and nucleotide biosynthesis pathways; and coping with oxidative stress, resulting in uniquely expressed metabolic profiles compared to other diatoms. We observed strong molecular evidence for iron limitation in shelf and slope regions of the WAP, where diatoms in these regions employed iron-starvation induced proteins, a geranylgeranyl reductase, aquaporins, and urease, among other strategies, while limiting the use of iron-containing proteins. The metatranscriptomic survey performed here reveals functional differences in diatom communities and provides further insight into the environmental factors influencing the growth of diatoms and their predicted response to changes in ocean conditions. IMPORTANCE: In the Southern Ocean, phytoplankton must cope with harsh environmental conditions such as low light and growth-limiting concentrations of the micronutrient iron. Using metratranscriptomics, we assessed the influence of oceanographic variables on the diversity of the phytoplankton community composition and on the metabolic strategies of diatoms along the Western Antarctic Peninsula, a region undergoing rapid climate change. We found that cross-shelf differences in oceanographic parameters such as temperature and variable nutrient concentrations account for most of the differences in phytoplankton community composition and metabolism. We opportunistically characterized the metabolic underpinnings of a large bloom of the centric diatom Actinocyclus in coastal waters of the WAP. Our results indicate that physicochemical differences from onshore to offshore are stronger than between southern and northern regions of the WAP; however, these trends could change in the future, resulting in poleward shifts in functional differences in diatom communities and phytoplankton blooms.

Synechococcus nitrogen gene loss in iron-limited ocean regions.

Synechococcus are the most abundant cyanobacteria in high latitude regions and are responsible for an estimated 17% of annual marine net primary productivity. Despite their biogeochemical importance, Synechococcus populations have been unevenly sampled across the ocean, with most studies focused on low-latitude strains. In particular, the near absence of Synechococcus genomes from high-latitude, High Nutrient Low Chlorophyll (HNLC) regions leaves a gap in our knowledge of picocyanobacterial adaptations to iron limitation and their influence on carbon, nitrogen, and iron cycles. We examined Synechococcus populations from the subarctic North Pacific, a well-characterized HNLC region, with quantitative metagenomics. Assembly with short and long reads produced two near complete Synechococcus metagenome-assembled genomes (MAGs). Quantitative metagenome-derived abundances of these populations matched well with flow cytometry counts, and the Synechococcus MAGs were estimated to comprise >99% of the Synechococcus at Station P. Whereas the Station P Synechococcus MAGs contained multiple genes for adaptation to iron limitation, both genomes lacked genes for uptake and assimilation of nitrate and nitrite, suggesting a dependence on ammonium, urea, and other forms of recycled nitrogen leading to reduced iron requirements. A global analysis of Synechococcus nitrate reductase abundance in the TARA Oceans dataset found nitrate assimilation genes are also lower in other HNLC regions. We propose that nitrate and nitrite assimilation gene loss in Synechococcus may represent an adaptation to severe iron limitation in high-latitude regions where ammonium availability is higher. Our findings have implications for models that quantify the contribution of cyanobacteria to primary production and subsequent carbon export.