skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Variability in the phytoplankton response to upwelling across an iron limitation mosaic within the California current system
Abstract Coastal upwelling currents such as the California Current System (CCS) comprise some of the most productive biological systems on the planet. Diatoms dominate these upwelling events in part due to their rapid response to nutrient entrainment. In this region, they may also be limited by the micronutrient iron (Fe), an important trace element primarily involved in photosynthesis and nitrogen assimilation. The mechanisms behind how diatoms physiologically acclimate to the different stages of the upwelling conveyor belt cycle remain largely uncharacterized. Here, we explore their physiological and metatranscriptomic response to the upwelling cycle with respect to the Fe limitation mosaic that exists in the CCS. Subsurface, natural plankton assemblages that would potentially seed surface blooms were examined over wide and narrow shelf regions. The initial biomass and physiological state of the phytoplankton community had a large impact on the overall response to simulated upwelling. Following on‐deck incubations under varying Fe physiological states, our results suggest that diatoms quickly dominated the blooms by “frontloading” nitrogen assimilation genes prior to upwelling. However, diatoms subjected to induced Fe limitation exhibited reductions in carbon and nitrogen uptake and decreasing biomass accumulation. Simultaneously, they exhibited a distinct gene expression response which included increased expression of Fe‐starvation induced proteins and decreased expression of nitrogen assimilation and photosynthesis genes. These findings may have significant implications for upwelling events in future oceans, where changes in ocean conditions are projected to amplify the gradient of Fe limitation in coastal upwelling regions.  more » « less
Award ID(s):
1751805
PAR ID:
10507715
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ; ; ;
Publisher / Repository:
Wiley
Date Published:
Journal Name:
Limnology and Oceanography
Volume:
69
Issue:
4
ISSN:
0024-3590
Page Range / eLocation ID:
888 to 901
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. 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. 
    more » « less
  2. Abstract 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. 
    more » « less
  3. Abstract Diatoms are important primary producers in the world's oceans, yet their growth is constrained in large regions by low bioavailable iron (Fe). Low‐Fe stress‐induced limitation of primary production is due to requirements for Fe in components of essential metabolic pathways including photosynthesis and other chloroplast plastid functions. Studies have shown that under low‐Fe stress, diatoms alter plastid‐specific processes, including components of electron transport. These physiological changes suggest changes of protein content and in protein abundances within the diatom plastid. While in silico predictions provide putative information on plastid‐localized proteins, knowledge of diatom plastid proteins remains limited in comparison to well‐studied model photosynthetic organisms. To address this, we employed shotgun proteomics to investigate the proteome of subcellular plastid‐enriched fractions fromThalassiosira pseudonanato gain a better understanding of how the plastid proteome is remodeled in response to Fe limitation. Using mass spectrometry‐based peptide identification and quantification, we analyzedT. pseudonanagrown under Fe‐replete and ‐limiting conditions. Through these analyses, we inferred the relative quantities of each protein, revealing that Fe limitation regulates major metabolic pathways in the plastid, including the Calvin cycle. Additionally, we observed changes in the expression of light‐harvesting proteins. In silico localization predictions of proteins identified in this plastid‐enriched proteome allowed for an in‐depth comparison of theoretical versus observed plastid‐localization, providing evidence for the potential of additional protein import pathways into the diatom plastid. 
    more » « less
  4. Coastal Antarctic marine ecosystems are significant in carbon cycling because of their intense seasonal phytoplankton blooms. Southern Ocean algae are primarily limited by light and iron (Fe) and can be co-limited by cobalamin (vitamin B12). Micronutrient limitation controls productivity and shapes the composition of blooms which are typically dominated by either diatoms or the haptophytePhaeocystis antarctica. However, the vitamin requirements and ecophysiology of the keystone speciesP. antarcticaremain poorly characterized. Using cultures, physiological analysis, and comparative omics, we examined the response ofP. antarcticato a matrix of Fe-B12conditions. We show thatP. antarcticais not auxotrophic for B12, as previously suggested, and identify mechanisms underlying its B12response in cultures of predominantly solitary and colonial cells. A combination of proteomics and proteogenomics reveals a B12-independent methionine synthase fusion protein (MetE-fusion) that is expressed under vitamin limitation and interreplaced with the B12-dependent isoform under replete conditions. Database searches return homologues of the MetE-fusion protein in multiplePhaeocystisspecies and in a wide range of marine microbes, including other photosynthetic eukaryotes with polymorphic life cycles as well as bacterioplankton. Furthermore, we find MetE-fusion homologues expressed in metaproteomic and metatranscriptomic field samples in polar and more geographically widespread regions. As climate change impacts micronutrient availability in the coastal Southern Ocean, our finding thatP. antarcticahas a flexible B12metabolism has implications for its relative fitness compared to B12-auxotrophic diatoms and for the detection of B12-stress in a more diverse set of marine microbes. 
    more » « less
  5. Diatoms serve as the major link between the marine carbon (C) and silicon (Si) biogeochemical cycles through their contributions to primary productivity and requirement for Si during cell wall formation. Although several culture-based studies have investigated the molecular response of diatoms to Si and nitrogen (N) starvation and replenishment, diatom silicon metabolism has been understudied in natural populations. A series of deckboard Si-amendment incubations were conducted using surface water collected in the California Upwelling Zone near Monterey Bay. Steep concentration gradients in macronutrients in the surface ocean coupled with substantial N and Si utilization led to communities with distinctly different macronutrient states: replete (‘healthy’), low N (‘N-stressed’), and low N and Si (‘N- and Si-stressed’). Biogeochemical measurements of Si uptake combined with metatranscriptomic analysis of communities incubated with and without added Si were used to explore the underlying molecular response of diatom communities to different macronutrient availability. Metatranscriptomic analysis revealed that N-stressed communities exhibited dynamic shifts in N and C transcriptional patterns suggestive of compromised metabolism. Expression patterns in communities experiencing both N and Si stress imply that the presence of Si stress may partially ameliorate N stress and dampen the impact on organic matter metabolism. This response builds upon previous observations that the regulation of C and N metabolism is decoupled from Si limitation status, where Si stress allows the cell to optimize the metabolic machinery necessary to respond to episodic pulses of nutrients. Several well-characterized Si-metabolism associated genes were found to be poor molecular markers of Si physiological status; however, several uncharacterized Si-responsive genes were revealed to be potential indicators of Si stress or silica production. 
    more » « less