Integrated Transcriptome Sequencing (RNA-seq) and Proteomic Studies Reveal Resource Reallocation towards Energy Metabolism and Defense in Skeletonema marinoi in Response to CO2 Increase

Rising atmospheric CO2 concentrations are causing ocean acidification (OA) with significant consequences for marine organisms. Because CO2 is essential for photosynthesis, the effect of elevated CO2 on phytoplankton is more complex, and the mechanism is poorly understood. Here, we applied transcriptome sequencing (RNA-seq) and IRAQ proteomics to investigate the impacts of CO(2 )increase (from ca. 400 to 1,000 ppm) on the temperate coastal marine diatom Skeletonema marina. We identified 32,389 differentially expressed genes and 1,826 differentially expressed proteins from conditions where the CO, is elevated, accounting for 48.5% of the total genes and 25.9% of the total proteins we detected, respectively. Elevated partial CO2 pressure (pCO(2)) significantly inhibited the growth of S. marinoi, and the omic data suggested that this might be due to compromised photosynthesis in the chloroplast and raised mitochondrial energy metabolism. Furthermore, many genes/proteins associated with nitrogen metabolism, transcriptional regulation, and translational regulation were markedly upregulated, suggesting enhanced protein synthesis. In addition, S. marinoi exhibited higher capacity of reactive oxygen species production and resistance to oxidative stress. Overall, elevated pCO(2) seems to repress photosynthesis and growth of S. marinoi and, through massive gene expression reconfiguration, induce cells to increase investment in protein synthesis, energy metabolism, and antioxidative stress defense, likely to maintain pH homeostasis and population survival. This survival strategy may deprive this usually dominant diatom in temperate coastal waters of its competitive advantages in acidified environments. IMPORTANCE Rising atmospheric CO2 concentrations are causing ocean acidification with significant consequences for marine organisms. Chain-forming centric diatoms of Skeletonema is one of the most successful groups of eukaryotic primary producers with widespread geographic distribution. Among the recognized 28 species, Skeletonema marinoi can be a useful model for investigating the ecological, genetic, physiological, and biochemical characteristics of diatoms in temperate coastal regions. In this study, we found that the elevated pCO(2) level seems to repress photosynthesis and growth of S. marinoi and, through massive gene expression reconfiguration, induce cells to increase investment in protein synthesis, energy metabolism, and antioxidative stress defense, likely to maintain pH homeostasis and population survival. This survival strategy may deprive this usually dominant diatom in temperate coastal waters of its competitive advantages in acidified environments.

Automated summary

Research has shown that rising atmospheric CO2 concentrations are causing ocean acidification with significant consequences for marine organisms. Studies on the temperate coastal marine diatom Skeletonema marinoi suggest that elevated CO2 levels can inhibit photosynthesis and growth, but induce cells to invest more in protein synthesis, energy metabolism, and antioxidative stress defense.