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

Mei Zhang; Yu Zhen; Tiezhu Mi; Senjie Lin

doi:10.1128/AEM.02614-20

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

Appl Environ Microbiol. 2021 Mar 1;87(5):e02614-20. doi: 10.1128/AEM.02614-20. Epub 2020 Dec 18.

Authors

Mei Zhang^{1

2

3

4}, Yu Zhen^{5

2

3}, Tiezhu Mi^{1

2

3}, Senjie Lin⁶

Affiliations

¹ Key Laboratory of Marine Environment and Ecology, Ocean University of China, Ministry of Education, Qingdao 266100, China.
² Laboratory for Marine Ecology and Environmental Science, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China.
³ College of Environmental Science and Engineering, Ocean University of China, Qingdao 266100, China.
⁴ Department of marine science, University of Connecticut, Groton, CT 06340, USA.
⁵ Key Laboratory of Marine Environment and Ecology, Ocean University of China, Ministry of Education, Qingdao 266100, China zhenyu@ouc.edu.cn senjie.lin@uconn.edu.
⁶ Department of marine science, University of Connecticut, Groton, CT 06340, USA zhenyu@ouc.edu.cn senjie.lin@uconn.edu.

Abstract

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 RNA-seq and iTRAQ proteomics to investigate the impacts of CO₂ increase (from ∼400 to 1000 ppm) on the temperate coastal marine diatom Skeletonema marinoi We identified 32,389 differentially expressed genes (DEGs) and 1,826 differentially expressed proteins (DEPs) from elevated CO₂ conditions, accounting for 48.5% of total genes and 25.9% of total proteins we detected, respectively. Elevated pCO₂ 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 up-regulated, suggesting enhanced protein synthesis. In addition, S marinoi exhibited higher capacity of ROS production and resistance to oxidative stress. Overall, elevated pCO₂ 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, S. 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 pCO₂ 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.