A comparative analysis of the calcification transcriptome and proteome of Emiliania huxleyi

Abstract

Calcium carbonate precipitation by marine organisms is an acknowledged contributor to the global carbon cycle. Coccolithophores are unicellular marine phytoplankton, that by excreting calcium scales and performing photosynthesis, contribute largely to the flux of atmospheric carbon to the surface and deeper oceans. The impact of elevated future ocean temperature and ocean acidity on the mechanism and rates, by which coccolithophores secret their calcium carbonate scales internally and contribute to the global carbon cycle, has been widely studied. However, biomineralisation in coccolithophores, the expression of molecular pathways, and the timing of gene expression related to calcification are still poorly understood. To better understand the process of calcification the transcriptome and proteome of calcifying G1-phase Emiliania huxleyi cells were investigated in the light and dark using next generation techniques. The results showed clear differences in both the transcriptomic and proteomic profiles between the photosynthetically enhanced calcification and the dark calcification phase. Interestingly, the bulk of the biomineralisation genes were higher expressed in the dark calcification phase at low calcification rates, suggesting that a large proportion of the molecular calcification machinery is bound to the Golgi apparatus and endoplasmic reticulum, which are complemented in the early G1-phase following cytokinesis. Furthermore, the results suggest that a set of biomineralisation genes exhibits continuous expression in both conditions of the G1 phase, whereas other genes are more abundantly expressed in the calcification phase. The importance of the calcium binding proteins calreticulin, calnexin, and calmodulin in the calcification phase was confirmed by transcriptomic and proteomic data. Proton pumping V-type ATPases were found higher expressed in dark phase but was still highly expressed in the enhanced calcification phase in the light. Calcium transport related gene expression of members of the NCKX (Na+/Ca2+-K+ exchanger), NCX (Na+/Ca2+exchanger), and CAX (calcium exchanger) were stronger in the low calcification phase, whereas SERCA-type calcium transporting ATPases were nearly equally expressed in both condition but originating from different genes that were expressed in either the light or the dark. Furthermore, transcriptome exploration suggested syntaxin and synaptobrevin could play an important role in calcification related vesicle fusion. The results have important implications for better understanding the timing of calcification related gene expression throughout the E. huxleyi cell cycle and for potential transcriptomic plasticity in response to changing environmental conditions.

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ORCID for Chris Hauton: orcid.org/0000-0002-2313-4226

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