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. 2021 Apr 30:12:657821.
doi: 10.3389/fpls.2021.657821. eCollection 2021.

Carbon Dioxide Concentration Mechanisms in Natural Populations of Marine Diatoms: Insights From Tara Oceans

Juan José Pierella Karlusich  1   2 , Chris Bowler  1   2 , Haimanti Biswas  3
Affiliations

Carbon Dioxide Concentration Mechanisms in Natural Populations of Marine Diatoms: Insights From Tara Oceans

Juan José Pierella Karlusich et al. Front Plant Sci. .

Abstract

Marine diatoms, the most successful photoautotrophs in the ocean, efficiently sequester a significant part of atmospheric CO2 to the ocean interior through their participation in the biological carbon pump. However, it is poorly understood how marine diatoms fix such a considerable amount of CO2, which is vital information toward modeling their response to future CO2 levels. The Tara Oceans expeditions generated molecular data coupled with in situ biogeochemical measurements across the main ocean regions, and thus provides a framework to compare diatom genetic and transcriptional flexibility under natural CO2 variability. The current study investigates the interlink between the environmental variability of CO2 and other physicochemical parameters with the gene and transcript copy numbers of five key enzymes of diatom CO2 concentration mechanisms (CCMs): Rubisco activase and carbonic anhydrase (CA) as part of the physical pathway, together with phosphoenolpyruvate carboxylase, phosphoenolpyruvate carboxykinase, and malic enzyme as part of the potential C4 biochemical pathway. Toward this aim, we mined >200 metagenomes and >220 metatranscriptomes generated from samples of the surface layer of 66 globally distributed sampling sites and corresponding to the four main size fractions in which diatoms can be found: 0.8-5 μm, 5-20 μm, 20-180 μm, and 180-2,000 μm. Our analyses revealed that the transcripts for the enzymes of the putative C4 biochemical CCM did not in general display co-occurring profiles. The transcripts for CAs were the most abundant, with an order of magnitude higher values than the other enzymes, thus implying the importance of physical CCMs in diatom natural communities. Among the different classes of this enzyme, the most prevalent was the recently characterized iota class. Consequently, very little information is available from natural diatom assemblages about the distribution of this class. Biogeographic distributions for all the enzymes show different abundance hotspots according to the size fraction, pointing to the influence of cell size and aggregation in CCMs. Environmental correlations showed a complex pattern of responses to CO2 levels, total phytoplankton biomass, temperature, and nutrient concentrations. In conclusion, we propose that biophysical CCMs are prevalent in natural diatom communities.

Keywords: Tara Oceans; carbon dioxide concentration mechanisms; carbon metabolism; diatoms; metagenomics; metatranscriptomics.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The reviewer YM declared a past co-authorship with one of the authors CB to the handling editor.

Figures

FIGURE 1
FIGURE 1
Overview of ocean carbon cycle and diatom carbon dioxide concentration mechanisms. (A) Schematic representation of the ocean carbon cycle depicting the role of marine diatoms in the biological carbon pump. The anthropogenic CO2 emission to the atmosphere (mainly generated by fossil fuel burning and deforestation) is nearly 11 Gigaton carbon (GtC) per year, of which almost 2.5 GtC is taken up by the surface ocean. In surface seawater (pH 8.1–8.4), bicarbonate (HCO3–) and carbonate ions (CO32–) constitute nearly 90 and <10% of dissolved inorganic carbon (DIC) respectively, while dissolved CO2 (CO2 aqueous) contributes <1%. Despite this low level of CO2 in the ocean and its slow diffusion rate in water, diatoms fix 10–20 GtC annually via photosynthesis thanks to their carbon dioxide concentration mechanisms (CCMs), allowing them to sustain food chains. In addition, 0.1–1% of this organic material produced in the euphotic layer sinks down as particles, thus transferring the surface carbon toward the deep ocean and sequestering atmospheric CO2 for thousands of years or longer. The remaining organic matter is remineralized through respiration. Thus, diatoms are one of the main players in this biological carbon pump, which is arguably the most important biological mechanism in the Earth System allowing CO2 to be removed from the carbon cycle for very long period. Based on data from Friedlingstein et al., 2020. (B) Schematic representation of the CCMs in diatoms. The low levels of CO2 in the ocean and its slow diffusion rate in water have led diatoms and other photosynthetic organisms to evolve CCMs that utilize the higher concentrations of HCO3–. The biophysical CCM consists of various bicarbonate transporters and carbonic anhydrases (CAs) that serve to increase the CO2 flux balance toward the pyrenoid, a low CO2-permeable subcellular compartment in the chloroplast containing most of the Rubisco. In addition, some diatoms may also have a biochemical (C4-like) CCM involving phosphoenolpyruvate carboxylase (PEPC), phosphoenolpyruvate carboxykinase (PEPCK) and/or malic enzyme (ME). (C) Schematic presentation of Rubisco activation by CbbX in diatoms and other phototrophs with red-type Rubisco. CbbX functions as a mechanochemical motor protein and uses the energy from ATP hydrolysis to modify the structure of Rubisco. This process facilitates the dissociation of inhibitory sugar phosphates [ribulose-1,5-bisphosphate (RuBP) and others] from the active site of Rubisco.
FIGURE 2
FIGURE 2
Tara Oceans sampling sites relevant to the current study. (A) Station labels. (B) Ocean regions. (C) Temperature measurements. (D) pH measurements. (E) CO2 partial pressure measurements. The sampling covers almost all main ecogeographic locations. Complete contextual data is available in Supplementary Table 1. IO, Indian Ocean; MS, Mediterranean Sea; NAO, North Atlantic Ocean; NPO, North Pacific Ocean; SAO, South Atlantic Ocean; SO, Southern Ocean; SPO, South Pacific Ocean.
FIGURE 3
FIGURE 3
Abundance of genes and transcripts potentially involved in diatom carbon dioxide concentration mechanisms across the different size-fractionated seawater samples collected during the Tara Oceans transect. (A) Gene and transcript abundances for the five enzymes under study. Barplots show the sum of normalized abundances for all samples in a given size fraction. Boxplots show the gene expression levels based on the abundance ratio in metatranscriptomes and metagenomes (metaT/metaG), and are displayed in logarithmic scale. Abbreviations: carbonic anhydrase (CA), Rubisco activase (CbbX), malic enzyme (ME), phosphoenolpyruvate carboxylase (PEPC), and phosphoenolpyruvate carboxykinase (PEPCK). (B) Gene and transcript abundances for the different types of CAs. Barplots and boxplots are displayed as indicated in panel (A).
FIGURE 4
FIGURE 4
Correlation analysis between the diatom genes and transcripts potentially involved in carbon dioxide concentration mechanisms. Circle size and color intensity are proportional to the Spearman’s rho correlation coefficients. Empty spaces refer to non-significant correlation values (two.tailed p-value > 0.05). carbonic anhydrase (CA), Rubisco activase (CbbX), malic enzyme (ME), phosphoenolpyruvate carboxylase (PEPC), and phosphoenolpyruvate carboxykinase (PEPCK).
FIGURE 5
FIGURE 5
Biogeography of genes and transcripts potentially involved in diatom carbon dioxide concentration mechanisms. Circle sizes are proportional to the gene or transcript abundance (% of total diatom gene or transcript read abundance), while crosses indicate absence of detection. Color code varies according to the size fractions. CA, carbonic anhydrase; CbbX, Rubisco activase; ME, malic enzyme; PEPC, phosphoenolpyruvate carboxylase, PEPCK, phosphoenolpyruvate carboxykinase.
FIGURE 6
FIGURE 6
Biogeographical patterns for the diatom genes and transcripts encoding carbonic anhydrases. Circle sizes are proportional to the gene or transcript abundance (% of total diatom gene or transcript abundance), while crosses indicate absence of detection.
FIGURE 7
FIGURE 7
Environmental distribution of genes and transcript potentially involved in diatom carbon dioxide concentration mechanisms. (A) Pairwise correlation of the matrix of contextual parameters. (B) Correlations of nutrients, chlorophyll a and temperature with gene and transcript abundances for the enzymes under study. (C) Correlations of carbonate chemistry measurements with gene and transcript abundances for the enzymes under study. Circle color varies according to Spearman rho’s correlation coefficient, while size varies according to the absolute value of the coefficient. Only statistically significant correlations are displayed (two-tailed test, p < 0.05). PAR, photosynthetically active radiation; CA, carbonic anhydrase; CbbX, Rubisco activase; ME, malic enzyme; PEPC, phosphoenolpyruvate carboxylase, PEPCK, phosphoenolpyruvate carboxykinase.
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References

    1. Alberti A., Poulain J., Engelen S., Labadie K., Romac S., Ferrera I., et al. (2017). Viral to metazoan marine plankton nucleotide sequences from the Tara Oceans expedition. Sci. Data 4:170093. - PMC - PubMed
    1. Aminot A., Kérouel R., Coverly S. C. (2009). “Nutrients in seawater using segmented flow analysis,” in Practical Guidelines for the Analysis of Seawater, ed. Wurl O. (Boca Raton, FL: CRC Press; ), 143–178.
    1. Armbrust E. V. (2009). The life of diatoms in the world’s oceans. Nature 459 185–192. 10.1038/nature08057 - DOI - PubMed
    1. Aumont O., Ethé C., Tagliabue A., Bopp L., Gehlen M. (2015). PISCES-v2: an ocean biogeochemical model for carbon and ecosystem studies. Geosci. Model Dev. 8 2465–2513. 10.5194/gmd-8-2465-2015 - DOI
    1. Badger M. (2003). The roles of carbonic anhydrases in photosynthetic CO2 concentrating mechanisms. Photosynth. Res. 77:83. - PubMed

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