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1. Representative Diatom and Coccolithophore Species Exhibit Divergent Responses throughout Simulated Upwelling Cycles

   https://doi.org/10.1128/mSystems.00188-21  

   Lampe, Robert H. ; Hernandez, Gustavo ; Lin, Yuan Yu ; Marchetti, Adrian ( April 2021 , mSystems)

   Huber, Julie A. (Ed.)

   ABSTRACT Wind-driven upwelling followed by relaxation results in cycles of cold nutrient-rich water fueling intense phytoplankton blooms followed by nutrient depletion, bloom decline, and sinking of cells. Surviving cells at depth can then be vertically transported back to the surface with upwelled waters to seed another bloom. As a result of these cycles, phytoplankton communities in upwelling regions are transported through a wide range of light and nutrient conditions. Diatoms appear to be well suited for these cycles, but their responses to them remain understudied. To investigate the bases for diatoms’ ecological success in upwelling environments, we employed laboratory simulations of a complete upwelling cycle with a common diatom, Chaetoceros decipiens , and coccolithophore, Emiliania huxleyi . We show that while both organisms exhibited physiological and transcriptomic plasticity, the diatom displayed a distinct response enabling it to rapidly shift-up growth rates and nitrate assimilation when returned to light and available nutrients following dark nutrient-deplete conditions. As observed in natural diatom communities, C. decipiens highly expresses before upwelling, or frontloads, key transcriptional and nitrate assimilation genes, coordinating its rapid response to upwelling conditions. Low-iron simulations showed that C. decipiens is capable of maintaining this response when iron is limiting to growth, whereas E. huxleyi is not. Differential expression between iron treatments further revealed specific genes used by each organism under low iron availability. Overall, these results highlight the responses of two dominant phytoplankton groups to upwelling cycles, providing insight into the mechanisms fueling diatom blooms during upwelling events. IMPORTANCE Coastal upwelling regions are among the most biologically productive ecosystems. During upwelling events, nutrient-rich water is delivered from depth resulting in intense phytoplankton blooms typically dominated by diatoms. Along with nutrients, phytoplankton may also be transported from depth to seed these blooms then return to depth as upwelling subsides creating a cycle with varied conditions. To investigate diatoms’ success in upwelling regions, we compare the responses of a common diatom and coccolithophore throughout simulated upwelling cycles under iron-replete and iron-limiting conditions. The diatom exhibited a distinct rapid response to upwelling irrespective of iron status, whereas the coccolithophore’s response was either delayed or suppressed depending on iron availability. Concurrently, the diatom highly expresses, or frontloads, nitrate assimilation genes prior to upwelling, potentially enabling this rapid response. These results provide insight into the molecular mechanisms underlying diatom blooms and ecological success in upwelling regions. 

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2. Diminished carbon and nitrate assimilation drive changes in diatom elemental stoichiometry independent of silicification in an iron-limited assemblage

   https://doi.org/10.1038/s43705-022-00136-1  

   Maniscalco, Michael A. ; Brzezinski, Mark A. ; Lampe, Robert H. ; Cohen, Natalie R. ; McNair, Heather M. ; Ellis, Kelsey A. ; Brown, Matthew ; Till, Claire P. ; Twining, Benjamin S. ; Bruland, Kenneth W. ; et al ( July 2022 , ISME Communications)

   In the California Current Ecosystem, upwelled water low in dissolved iron (Fe) can limit phytoplankton growth, altering the elemental stoichiometry of the particulate matter and dissolved macronutrients. Iron-limited diatoms can increase biogenic silica (bSi) content >2-fold relative to that of particulate organic carbon (C) and nitrogen (N), which has implications for carbon export efficiency given the ballasted nature of the silica-based diatom cell wall. Understanding the molecular and physiological drivers of this altered cellular stoichiometry would foster a predictive understanding of how low Fe affects diatom carbon export. In an artificial upwelling experiment, water from 96 m depth was incubated shipboard and left untreated or amended with dissolved Fe or the Fe-binding siderophore desferrioxamine-B (+DFB) to induce Fe-limitation. After 120 h, diatoms dominated the communities in all treatments and displayed hallmark signatures of Fe-limitation in the +DFB treatment, including elevated particulate Si:C and Si:N ratios. Single-cell, taxon-resolved measurements revealed no increase in bSi content during Fe-limitation despite higher transcript abundance of silicon transporters and silicanin-1. Based on these findings we posit that the observed increase in bSi relative to C and N was primarily due to reductions in C fixation and N assimilation, driven by lower transcript expression of key Fe-dependent genes.

    

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3. Diatom populations in an upwelling environment decrease silica content to avoid growth limitation

   https://doi.org/10.1111/1462-2920.14431  

   McNair, Heather M. ; Brzezinski, Mark A. ; Krause, Jeffrey W. ( October 2018 , Environmental Microbiology)

   A mix of adaptive strategies enable diatoms to sustain rapid growth in dynamic ocean regions, making diatoms one of the most productive primary producers in the world. We illustrate one such strategy off coastal California that facilitates continued, high, cell division rates despite silicic acid stress. Using a fluorescent dye to measure single‐cell diatom silica production rates, silicification (silica per unit area) and growth rates we show diatoms decrease silicification and maintain growth rate when silicon concentration limits silica production rates. While this physiological response to silicon stress was similar across taxa,in situsilicic acid concentration limited silica production rates by varying degrees for taxa within the same community. Despite this variability among taxa, silicon stress did not alter the contribution of specific taxa to total community silica production or to community composition. Maintenance of division rate at the expense of frustule thickness decreases cell density which could affect regional biogeochemical cycles. The reduction in frustule silicification also creates an ecological tradeoff: thinner frustules increase susceptibility to predation but reducing Si quotas maximizes cell abundance for a given pulse of silicic acid, thereby favouring a larger eventual population size which facilitates diatom persistence in habitats with pulsed resource supplies.

    

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4. The evolution of silicon transporters in diatoms

   https://doi.org/10.1111/jpy.12441  

   Durkin, Colleen A. ; Koester, Julie A. ; Bender, Sara J. ; Armbrust, E. Virginia ; Kroth, ed., P. ( August 2016 , Journal of Phycology)

   Diatoms are highly productive single‐celled algae that form an intricately patterned silica cell wall after every cell division. They take up and utilize silicic acid from seawater via silicon transporter (SIT) proteins. This study examined the evolution of theSITgene family to identify potential genetic adaptations that enable diatoms to thrive in the modern ocean. By searching for sequence homologs in available databases, the diversity of organisms found to encodeSITs increased substantially and included all major diatom lineages and other algal protists. A bacterial‐encoded gene with homology toSITsequences was also identified, suggesting that a lateral gene transfer event occurred between bacterial and protist lineages. In diatoms, theSITgenes diverged and diversified to produce five distinct clades. The most basalSITclades were widely distributed across diatom lineages, while the more derived clades were lineage‐specific, which together produced a distinct repertoire ofSITtypes among major diatom lineages. Differences in the predicted protein functional domains encoded amongSITclades suggest that the divergence of clades resulted in functional diversification amongSITs. Both laboratory cultures and natural communities changed transcription of eachSITclade in response to experimental or environmental growth conditions, with distinct transcriptional patterns observed among clades. Together, these data suggest that the diversification ofSITs within diatoms led to specialized adaptations among diatoms lineages, and perhaps their dominant ability to take up silicic acid from seawater in diverse environmental conditions.

    

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5. The rate and fate of N2 and C fixation by marine diatom-diazotroph symbioses

   https://doi.org/10.1038/s41396-021-01086-7  

   Foster, Rachel A. ; Tienken, Daniela ; Littmann, Sten ; Whitehouse, Martin J. ; Kuypers, Marcel M. M. ; White, Angelicque E. ( August 2021 , The ISME Journal)

   N2 fixation constitutes an important new nitrogen source in the open sea. One group of filamentous N2 fixing cyanobacteria (Richelia intracellularis, hereafter Richelia) form symbiosis with a few genera of diatoms. High rates of N2 fixation and carbon (C) fixation have been measured in the presence of diatom-Richelia symbioses. However, it is unknown how partners coordinate C fixation and how the symbiont sustains high rates of N2 fixation. Here, both the N2 and C fixation in wild diatom-Richelia populations are reported. Inhibitor experiments designed to inhibit host photosynthesis, resulted in lower estimated growth and depressed C and N2 fixation, suggesting that despite the symbionts ability to fix their own C, they must still rely on their respective hosts for C. Single cell analysis indicated that up to 22% of assimilated C in the symbiont is derived from the host, whereas 78–91% of the host N is supplied from their symbionts. A size-dependent relationship is identified where larger cells have higher N2 and C fixation, and only N2 fixation was light dependent. Using the single cell measures, the N-rich phycosphere surrounding these symbioses was estimated and contributes directly and rapidly to the surface ocean rather than the mesopelagic, even at high estimated sinking velocities (<10 m d−1). Several eco-physiological parameters necessary for incorporating symbiotic N2 fixing populations into larger basin scale biogeochemical models (i.e., N and C cycles) are provided.

    

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