Frequent blooms of phytoplankton occur in coastal upwelling zones creating hotspots of biological productivity in the ocean. As cold, nutrient-rich water is brought up to sunlit layers from depth, phytoplankton are also transported upwards to seed surface blooms that are often dominated by diatoms. The physiological response of phytoplankton to this process, commonly referred to as shift-up, is characterized by increases in nitrate assimilation and rapid growth rates. To examine the molecular underpinnings behind this phenomenon, metatranscriptomics was applied to a simulated upwelling experiment using natural phytoplankton communities from the California Upwelling Zone. An increase in diatom growth following 5 days of incubation was attributed to the genera Chaetoceros and Pseudo-nitzschia. Here, we show that certain bloom-forming diatoms exhibit a distinct transcriptional response that coordinates shift-up where diatoms exhibited the greatest transcriptional change following upwelling; however, comparison of co-expressed genes exposed overrepresentation of distinct sets within each of the dominant phytoplankton groups. The analysis revealed that diatoms frontload genes involved in nitrogen assimilation likely in order to outcompete other groups for available nitrogen during upwelling events. We speculate that the evolutionary success of diatoms may be due, in part, to this proactive response to frequently encountered changes in their environment.
Diatoms are prominent eukaryotic phytoplankton despite being limited by the micronutrient iron in vast expanses of the ocean. As iron inputs are often sporadic, diatoms have evolved mechanisms such as the ability to store iron that enable them to bloom when iron is resupplied and then persist when low iron levels are reinstated. Two iron storage mechanisms have been previously described: the protein ferritin and vacuolar storage. To investigate the ecological role of these mechanisms among diatoms, iron addition and removal incubations were conducted using natural phytoplankton communities from varying iron environments. We show that among the predominant diatoms, Pseudo-nitzschia were favored by iron removal and displayed unique ferritin expression consistent with a long-term storage function. Meanwhile, Chaetoceros and Thalassiosira gene expression aligned with vacuolar storage mechanisms. Pseudo-nitzschia also showed exceptionally high iron storage under steady-state high and low iron conditions, as well as following iron resupply to iron-limited cells. We propose that bloom-forming diatoms use different iron storage mechanisms and that ferritin utilization may provide an advantage in areas of prolonged iron limitation with pulsed iron inputs. As iron distributions and availability change, this speculated ferritin-linked advantage may result in shifts in diatom community composition that can alter marine ecosystems and biogeochemical cycles.
Iron availability limits primary productivity in large areas of the world's oceans. Ascertaining the iron status of phytoplankton is essential for understanding the factors regulating their growth and ecology. We developed an incubation-independent, molecular-based approach to assess the iron nutritional status of specific members of the diatom community, initially focusing on the ecologically important pennate diatom Pseudo-nitzschia. Through a comparative transcriptomic approach, we identified two genes that track the iron status of Pseudo-nitzschia with high fidelity. The first gene, ferritin (FTN), encodes for the highly specialized iron storage protein induced under iron-replete conditions. The second gene, ISIP2a, encodes an iron-concentrating protein induced under iron-limiting conditions. In the oceanic diatom Pseudo-nitzschia granii (Hasle) Hasle, transcript abundance of these genes directly relates to changes in iron availability, with increased FTN transcript abundance under iron-replete conditions and increased ISIP2a transcript abundance under iron-limiting conditions. The resulting ISIP2a:FTN transcript ratio reflects the iron status of cells, where a high ratio indicates iron limitation. Field samples collected from iron grow-out microcosm experiments conducted in low iron waters of the Gulf of Alaska and variable iron waters in the California upwelling zone verify the validity of our proposed Pseudo-nitzschia Iron Limitation Index, which can be used to ascertain in situ iron status and further developed for other ecologically important diatoms.
Trace metals and B-vitamins play critical roles in regulating marine phytoplankton growth and composition. While some microorganisms are capable of producing certain B-vitamins, others cannot synthesize them and depend on an exogenous supply. Therefore, external factors influencing vitamin synthesis, such as micronutrient concentrations, alter the extent to which B-vitamins are available to auxotrophs in surface waters. We examined iron, B 7 (biotin) and B 12 (cobalamin) dynamics in diatoms through laboratory culture experiments and within natural diatom assemblages present along an iron gradient in the Northeast Pacific Ocean. In laboratory cultures of the diatom Pseudo-nitzschia granii, biotin synthase (BIOB) expression decreased 2-fold under iron limitation, suggesting iron status may affect B 7 production in diatoms. Additionally in laboratory cultures of the diatom Grammonema cf. islandica, which contains a B 12 -independent methionine synthase (METE), a 15-fold increase in the expression of METE was observed when grown in the absence of B 12 with no significant influence of iron status, suggesting METE expression can be driven by B 12 status alone. Iron and B-vitamin amendment experiments with natural diatom assemblages in iron-limited waters of the Northeast Pacific Ocean provide evidence for vitamin-associated molecular responses that suggest elevated B 7 biosynthesis and the emergence of B 12 limitation following iron addition. Furthermore Bvitamin gene modules comprised of partial and/or complete B-vitamin biosynthetic pathways in diatoms increased in response to iron addition, including genes potentially involved in the processing of B 12 intermediates. Our results indicate that vitamins may play an important role in regulating phytoplankton growth and composition in this region, particularly following natural iron addition events. 2076LIMNOLOGY and OCEANOGRAPHY
32Frequent blooms of phytoplankton occur in coastal upwelling zones creating hotspots of biological 33 productivity in the ocean. As cold, nutrient-rich water is brought up to sunlit layers from depth, 34 phytoplankton are also transported upwards to seed surface blooms that are often dominated by 35 diatoms. The physiological response of phytoplankton to this process, commonly referred to as 36 shift-up, is characterized by rapid growth rates and increases in nitrate assimilation. To examine 37 the molecular underpinnings behind this phenomenon, metatranscriptomics was applied to a 38 simulated upwelling experiment using natural phytoplankton communities from the California 39Upwelling Zone. An increase in diatom growth following five days of incubation was attributed 40 to the genera Chaetoceros and Pseudo-nitzschia. Here we show that certain bloom-forming 41 diatoms exhibit a distinct transcriptional response that coordinates shift-up where diatoms 42 exhibited the greatest transcriptional change following upwelling; however, comparison of co-43 expressed genes exposed overrepresentation of distinct sets within each of the dominant 44 phytoplankton groups. The analysis revealed that diatoms frontload genes involved in nitrogen 45 assimilation likely in order to outcompete other groups for available nitrogen during upwelling 46 events. We speculate that the evolutionary success of diatoms may be due, in part, to this proactive 47
The ecological and oceanographic processes that drive the response of pelagic ocean microbiomes to environmental changes remain poorly understood, particularly in coastal upwelling ecosystems. Here we show that seasonal and interannual variability in coastal upwelling predicts pelagic ocean microbiome diversity and community structure in the Southern California Current region. Ribosomal RNA gene sequencing, targeting prokaryotic and eukaryotic microbes, from samples collected seasonally during 2014-2020 indicate that nitracline depth is the most robust predictor of spatial microbial community structure and biodiversity in this region. Striking ecological changes occurred due to the transition from a warm anomaly during 2014-2016, characterized by intense stratification, to cooler conditions in 2017-2018, representative of more typical upwelling conditions, with photosynthetic eukaryotes, especially diatoms, changing most strongly. The regional slope of nitracline depth exerts strong control on the relative proportion of highly diverse offshore communities and low biodiversity, but highly productive nearshore communities.
Despite generally low primary productivity and diatom abundances in oligotrophic subtropical gyres, the North Atlantic Subtropical Gyre (NASG) exhibits significant diatom-driven carbon export on an annual basis. Subsurface pulses of nutrients likely fuel brief episodes of diatom growth, but the exact mechanisms utilized by diatoms in response to these nutrient injections remain understudied within near-natural settings. Here we simulated delivery of subsurface nutrients and compare the response among eukaryotic phytoplankton using a combination of physiological techniques and metatranscriptomics. We show that eukaryotic phytoplankton groups exhibit differing levels of transcriptional responsiveness and expression of orthologous genes in response to release from nutrient limitation. In particular, strategies for use of newly delivered nutrients are distinct among phytoplankton groups. Diatoms channel new nitrate to growth-related strategies while physiological measurements and gene expression patterns of other groups suggest alternative strategies. The gene expression patterns displayed here provide insights into the cellular mechanisms that underlie diatom subsistence during chronic nitrogen-depleted conditions and growth upon nutrient delivery that can enhance carbon export from the surface ocean.
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