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ABSTRACT 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. IMPORTANCEIn 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 diatomActinocyclusin 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. 

Photosynthetic carbon (C) fixation by phytoplankton in the Southern Ocean (SO) plays a critical role in regulating air–sea exchange of carbon dioxide and thus global climate. In the SO, photosynthesis (PS) is often constrained by low iron, low temperatures, and low but highly variable light intensities. Recently, proton-pumping rhodopsins (PPRs) were identified in marine phytoplankton, providing an alternate iron-free, light-driven source of cellular energy. These proteins pump protons across cellular membranes through light absorption by the chromophore retinal, and the resulting pH energy gradient can then be used for active membrane transport or for synthesis of adenosine triphosphate. Here, we show that PPR is pervasive in Antarctic phytoplankton, especially in iron-limited regions. In a model SO diatom, we found that it was localized to the vacuolar membrane, making the vacuole a putative alternative phototrophic organelle for light-driven production of cellular energy. Unlike photosynthetic C fixation, which decreases substantially at colder temperatures, the proton transport activity of PPR was unaffected by decreasing temperature. Cellular PPR levels in cultured SO diatoms increased with decreasing iron concentrations and energy production from PPR photochemistry could substantially augment that of PS, especially under high light intensities, where PS is often photoinhibited. PPR gene expression and high retinal concentrations in phytoplankton in SO waters support its widespread use in polar environments. PPRs are an important adaptation of SO phytoplankton to growth and survival in their cold, iron-limited, and variable light environment. 

Abstract Since the middle of the past century, the Western Antarctic Peninsula has warmed rapidly with a significant loss of sea ice but the impacts on plankton biodiversity and carbon cycling remain an open question. Here, using a 5-year dataset of eukaryotic plankton DNA metabarcoding, we assess changes in biodiversity and net community production in this region. Our results show that sea-ice extent is a dominant factor influencing eukaryotic plankton community composition, biodiversity, and net community production. Species richness and evenness decline with an increase in sea surface temperature (SST). In regions with low SST and shallow mixed layers, the community was dominated by a diverse assemblage of diatoms and dinoflagellates. Conversely, less diverse plankton assemblages were observed in waters with higher SST and/or deep mixed layers when sea ice extent was lower. A genetic programming machine-learning model explained up to 80% of the net community production variability at the Western Antarctic Peninsula. Among the biological explanatory variables, the sea-ice environment associated plankton assemblage is the best predictor of net community production. We conclude that eukaryotic plankton diversity and carbon cycling at the Western Antarctic Peninsula are strongly linked to sea-ice conditions. 

The West Antarctic Peninsula (henceforth “Peninsula”) is experiencing rapid warming and melting that is impacting the regional marine food web. The primary phytoplankton groups along the Peninsula are diatoms and cryptophytes. Relative to diatoms, there has been little focus on regional cryptophytes, and thus our understanding of their diversity and ecology is limited, especially at the species level. This gap is important, as diatoms and cryptophytes play distinct roles in the regional marine food web and biogeochemistry. Here, we use a phylogenetic placement approach with 18S rRNA gene amplicon sequence variants to assess surface ocean cryptophyte diversity and its drivers at a high taxonomic resolution along the Peninsula. Data were collected over 5 years (2012–2016) during the regional research cruises of the Palmer Long‐Term Ecological Research program. Our results indicate that there are two major cryptophyte taxa along the Peninsula, consisting of distinctGeminigeraspp., which in aggregate always comprise nearly 100% of the cryptophyte community (indicating low taxa evenness). The primary taxon dominates the cryptophyte community across all samples/years, which span a broad range of oceanographic conditions. A shift in cryptophyte community composition between a lower (higher) primary (secondary) taxon percentage is associated with distinct oceanographic conditions, including lower (higher) temperature, salinity, nutrients, and cryptophyte relative abundance (phytoplankton biomass and diatom relative abundance). These results emphasize the need for a full characterization of the ecology of these two taxa, as it is predicted that cryptophytes will increase along the Peninsula given projections of continued regional environmental change.