skip to main content

Title: Diel Transcriptional Oscillations of a Plastid Antiporter Reflect Increased Resilience of Thalassiosira pseudonana in Elevated CO2
Acidification of the ocean due to high atmospheric CO 2 levels may increase the resilience of diatoms causing dramatic shifts in abiotic and biotic cycles with lasting implications on marine ecosystems. Here, we report a potential bioindicator of a shift in the resilience of a coastal and centric model diatom Thalassiosira pseudonana under elevated CO 2 . Specifically, we have discovered, through EGFP-tagging, a plastid membrane localized putative Na + (K + )/H + antiporter that is significantly upregulated at >800 ppm CO 2 , with a potentially important role in maintaining pH homeostasis. Notably, transcript abundance of this antiporter gene was relatively low and constant over the diel cycle under contemporary CO 2 conditions. In future acidified oceanic conditions, dramatic oscillation with >10-fold change between nighttime (high) and daytime (low) transcript abundances of the antiporter was associated with increased resilience of T. pseudonana . By analyzing metatranscriptomic data from the Tara Oceans project, we demonstrate that phylogenetically diverse diatoms express homologs of this antiporter across the globe. We propose that the differential between night- and daytime transcript levels of the antiporter could serve as a bioindicator of a shift in the resilience of diatoms in response to high CO more » 2 conditions in marine environments. « less
; ; ; ; ; ; ;
Award ID(s):
Publication Date:
Journal Name:
Frontiers in Marine Science
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    The fate of diatoms in future acidified oceans could have dramatic implications on marine ecosystems, because they account for ~40% of marine primary production. Here, we quantify resilience ofThalassiosira pseudonanain mid-20th century (300 ppm CO2) and future (1000 ppm CO2) conditions that cause ocean acidification, using a stress test that probes its ability to recover from incrementally higher amount of low-dose ultraviolet A (UVA) and B (UVB) radiation and re-initiate growth in day–night cycles, limited by nitrogen. While all cultures eventually collapse, those growing at 300 ppm CO2succumb sooner. The underlying mechanism for collapse appears to be a system failure resulting from “loss of relational resilience,” that is, inability to adopt physiological states matched to N-availability and phase of the diurnal cycle. Importantly, under elevated CO2conditions diatoms sustain relational resilience over a longer timeframe, demonstrating increased resilience to future acidified ocean conditions. This stress test framework can be extended to evaluate and predict how various climate change associated stressors may impact microbial community resilience.

  2. High‐affinity nitrate transporters are considered to be the major transporter system for nitrate uptake in diatoms. In the diatom genus Skeletonema, three forms of genes encoding high‐affinity nitrate transporters (NRT2) were newly identified from transcriptomes generated as part of the marine microbial eukaryote transcriptome sequencing project. To examine the expression of each form of NRT2 under different nitrogen environments, laboratory experiments were conducted under nitrate‐sufficient, ammonium‐sufficient, and nitrate‐limited conditions using three ecologically important Skeletonema species: S. dohrnii, S. menzelii, and S. marinoi. Primers were developed for each NRT2 form and species and Q‐RT‐PCR was performed. For each NRT2 form, the three Skeletonema species had similar transcriptional patterns. The transcript levels of NRT2:1 were significantly elevated under nitrogen‐limited conditions, but strongly repressed in the presence of ammonium. The transcript levels of NRT2:2 were also repressed by ammonium, but increased 5‐ to 10‐fold under nitrate‐sufficient and nitrogen‐limited conditions. Finally, the transcript levels of NRT2:3 did not vary significantly under various nitrogen conditions, and behaved more like a constitutively expressed gene. Based on the observed transcript variation among NRT2 forms, we propose a revised model describing nitrate uptake kinetics regulated by multiple forms of nitrate transporter genes in response to various nitrogen conditionsmore »in Skeletonema. The differential NRT2 transcriptional responses among species suggest that species‐specific adaptive strategies exist within this genus to cope with environmental changes.« less
  3. The importance of zinc (Zn) as a nutrient and its ability to be substituted for by cobalt (Co) have been characterized in model marine diatoms. However, the extent to which this substitution capability is distributed among diatom taxa is unknown. Zn/Co metabolic substitution was assayed in four diatom species as measured by the effect of free ion concentrations of Zn2+ and Co2+ on specific growth rate. Analysis of growth responses found substitution of these metals can occur within the northwest Atlantic isolate Thalassiosira pseudonana CCMP1335, the northeast Atlantic isolate Phaeodactylum tricornutum CCMP632, and within the northeast Pacific isolates Pseudo-nitzschia delicatissima UNC1205 and Thalassiosira sp. UNC1203. Metabolic substitution of Co in place of Zn in the Atlantic diatoms supports their growth in media lacking added Zn, but at the cost of reduced growth rates. In contrast, highly efficient Zn/Co substitution that supported growth even in media lacking added Zn was observed in the northeast Pacific diatoms. We also present new data from the northeast Pacific Line P transect that revealed dissolved Co and Zn ratios (dCo : dZn) as high as 3.52 : 1 at surface (0–100 m) depths. We posit that the enhanced ability of the NE Pacific diatoms tomore »grow using Co is an adaptation to these high surface dCo : dZn ratios. Particulate metal data and single-cell metal quotas also suggest a high Zn demand in diatoms that may be partially compensated for by Co.« less
  4. Rising atmospheric CO 2 reduces seawater pH causing ocean acidification (OA). Understanding how resilient marine organisms respond to OA may help predict how community dynamics will shift as CO 2 continues rising. The common slipper shell snail Crepidula fornicata is a marine gastropod native to eastern North America that has been a successful invader along the western European coastline and elsewhere. It has also been previously shown to be resilient to global change stressors. To examine the mechanisms underlying C. fornicata’s resilience to OA, we conducted two controlled laboratory experiments. First, we examined several phenotypes and genome-wide gene expression of C. fornicata in response to pH treatments (7.5, 7.6, and 8.0) throughout the larval stage and then tested how conditions experienced as larvae influenced juvenile stages (i.e., carry-over effects). Second, we examined genome-wide gene expression patterns of C. fornicata larvae in response to acute (4, 10, 24, and 48 h) pH treatment (7.5 and 8.0). Both C. fornicata larvae and juveniles exhibited resilience to OA and their gene expression responses highlight the role of transcriptome plasticity in this resilience. Larvae did not exhibit reduced growth under OA until they were at least 8 days old. These phenotypic effects were precededmore »by broad transcriptomic changes, which likely served as an acclimation mechanism for combating reduced pH conditions frequently experienced in littoral zones. Larvae reared in reduced pH conditions also took longer to become competent to metamorphose. In addition, while juvenile sizes at metamorphosis reflected larval rearing pH conditions, no carry-over effects on juvenile growth rates were observed. Transcriptomic analyses suggest increased metabolism under OA, which may indicate compensation in reduced pH environments. Transcriptomic analyses through time suggest that these energetic burdens experienced under OA eventually dissipate, allowing C. fornicata to reduce metabolic demands and acclimate to reduced pH. Carry-over effects from larval OA conditions were observed in juveniles; however, these effects were larger for more severe OA conditions and larvae reared in those conditions also demonstrated less transcriptome elasticity. This study highlights the importance of assessing the effects of OA across life history stages and demonstrates how transcriptomic plasticity may allow highly resilient organisms, like C. fornicata , to acclimate to reduced pH environments.« less
  5. Atomi, Haruyuki (Ed.)
    ABSTRACT Genome and proteome data predict the presence of both the reductive citric acid cycle (rCAC; also called the reductive tricarboxylic acid cycle) and the Calvin-Benson-Bassham cycle (CBB) in “ Candidatus Endoriftia persephonae,” the autotrophic sulfur-oxidizing bacterial endosymbiont from the giant hydrothermal vent tubeworm Riftia pachyptila . We tested whether these cycles were differentially induced by sulfide supply, since the synthesis of biosynthetic intermediates by the rCAC is less energetically expensive than that by the CBB. R. pachyptila was incubated under in situ conditions in high-pressure aquaria under low (28 to 40 μmol · h −1 ) or high (180 to 276 μmol · h −1 ) rates of sulfide supply. Symbiont-bearing trophosome samples excised from R. pachyptila maintained under the two conditions were capable of similar rates of CO 2 fixation. Activities of the rCAC enzyme ATP-dependent citrate lyase (ACL) and the CBB enzyme 1,3-bisphosphate carboxylase/oxygenase (RubisCO) did not differ between the two conditions, although transcript abundances for ATP-dependent citrate lyase were 4- to 5-fold higher under low-sulfide conditions. δ 13 C values of internal dissolved inorganic carbon (DIC) pools were varied and did not correlate with sulfide supply rate. In samples taken from freshly collected R. pachyptila , δ 13more »C values of lipids fell between those collected for organisms using either the rCAC or the CBB exclusively. These observations are consistent with cooccurring activities of the rCAC and the CBB in this symbiosis. IMPORTANCE Previous to this study, the activities of the rCAC and CBB in R. pachyptila had largely been inferred from “omics” studies of R. pachyptila without direct assessment of in situ conditions prior to collection. In this study, R. pachyptila was maintained and monitored in high-pressure aquaria prior to measuring its CO 2 fixation parameters. Results suggest that ranges in sulfide concentrations similar to those experienced in situ do not exert a strong influence on the relative activities of the rCAC and the CBB. This observation highlights the importance of further study of this symbiosis and other organisms with multiple CO 2 -fixing pathways, which recent genomics and biochemical studies suggest are likely to be more prevalent than anticipated.« less