Diel Transcriptional Oscillations of a Plastid Antiporter Reflect Increased Resilience of Thalassiosira pseudonana in Elevated CO2

Jacob J Valenzuela,Mark Hildebrand,Allison Cusick,Justin Ashworth,Nitin S Baliga,E Virginia Armbrust,Mónica V Orellana,Raffaela M Abbriano

doi:10.3389/fmars.2021.633225

Abstract

Acidification of the ocean due to high atmospheric CO2 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 CO2. Specifically, we have discovered, through EGFP-tagging, a plastid membrane localized putative Na+(K+)/H+ antiporter that is significantly upregulated at &gt;800 ppm CO2, 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 CO2 conditions. In future acidified oceanic conditions, dramatic oscillation with &gt;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 CO2 conditions in marine environments.

Highlights

Diatoms (Bacillariophyta) represent a diverse group of marine phytoplankton widely distributed across the globe, from coastal habitats to the open oceans (Malviya et al, 2016)
We observed that > 1,400 genes were differentially regulated (FDR < 0.001) during the growth of T. pseudonana in combinations of perturbations in light (HL and LL), and CO2 levels (HC and LC), which simulated daytime bloomlike dynamics of rapid growth in nutrient-replete conditions followed by a transition to a more quiescent state in nutrientdeplete stationary phase
It is noteworthy that the differential expression of the putative antiporter was directly reflective of the response to CO2, across different intensities of light, UV stress, and nutrient availability. We postulate that this is because the gene is potentially an intracellular pH-sensitive Na+(K+)/H+ antiporter with a direct role in maintaining pH homeostasis across the plastid membrane, similar to the chx23 Na+(K+)/H+ antiporter in Arabidopsis thaliana, which by itself has been shown to maintain pH homeostasis in the chloroplast stroma (Song et al, 2004)

Summary

Introduction

Diatoms (Bacillariophyta) represent a diverse group of marine phytoplankton widely distributed across the globe, from coastal habitats to the open oceans (Malviya et al, 2016). They account for 40% of the marine primary productivity (20% globally) (Nelson and Gordon, 1982; Falkowski et al, 1998; Field et al, 1998) and facilitate carbon export to the deep ocean through the biological carbon pump (Falkowski et al, 1998; Smetacek, 1999). Under increasing CO2 concentrations, T. pseudonana remodels chromatin and transcriptionally downregulates photosynthesis, respiration, and carbon-concentrating mechanisms (CCMs) (Ashworth et al, 2013; Hennon et al, 2015), which are utilized by many diatoms (Badger et al, 1998; Crawfurd et al, 2011) to grow in the CO2-limited oceans of today (

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Results

Conclusion