Multi-Omics Profiling Reveals Resource Allocation and Acclimation Strategies to Temperature Changes in a Marine Dinoflagellate

Zhang，Hao1; Gu，Bowei1; Zhou，Youping2,3,4; Ma，Xiao1; Liu，Tianqi5; Xu，Hongkai6; Xie，Zhangxian5; Liu，Kailin7; Wang，Dazhi5; Xia，Xiaomin1,8

2022-09-13

10.1128/aem.01213-22

Applied and environmental microbiology   Impact Factor & Quartile

1098-5336

Temperature is a critical environmental factor that affects the cell growth of dinoflagellates and bloom formation. To date, the molecular mechanisms underlying the physiological responses to temperature variations are poorly understood. Here, we applied quantitative proteomic and untargeted metabolomic approaches to investigate protein and metabolite expression profiles of a bloom-forming dinoflagellate Prorocentrum shikokuense at different temperatures. Of the four temperatures (19, 22, 25, and 28°C) investigated, P. shikokuense at 25°C exhibited the maximal cell growth rate and maximum quantum efficiency of photosystem II (Fv/Fm) value. The levels of particulate organic carbon (POC) and nitrogen (PON) decreased with increasing temperature, while the POC/PON ratio increased and peaked at 25°C. Proteomic analysis showed proteins related to photoreaction, light harvesting, and protein homeostasis were highly expressed at 28°C when cells were under moderate heat stress. Metabolomic analysis further confirmed reallocated amino acids and soluble sugars at this temperature. Both omic analyses showed glutathione metabolism that scavenges the excess reactive oxygen species, and transcription and lipid biosynthesis that compensate for the low translation efficiency and plasma membrane fluidity were largely upregulated at suboptimal temperature. Higher accumulations of glutathione, glutarate semialdehyde, and 5-KETE at 19°C implied their important roles in low-temperature acclimation. The strikingly active nitrate reduction and nitrogen flux into asparagine, glutamine, and aspartic acid at 19°C indicated these three amino acids may serve as nitrogen storage pools and help cells cope with low temperature. Our study provides insights into the effects of temperature on dinoflagellate resource allocation and advances our knowledge of dinoflagellate bloom formation in marine environments. IMPORTANCE Marine phytoplankton is one of the most important nodes in global biogeochemical cycle. Deciphering temperature-associated marine phytoplankton cell stoichiometric changes and the underlying molecular mechanisms are therefore of great ecological concerns. However, knowledge of how phytoplankton adjust the cell stoichiometry to sustain growth under temperature changes is still lacking. This study investigates the variations of protein and metabolite profiles in a marine dinoflagellate across temperatures at which the field blooms usually occur and highlights the temperature-dependent molecular traits and key metabolites that may be associated with rapid cell growth and temperature stress acclimation.

dinoflagellate harmful algal blooms metabolomics phytoplankton stoichiometry quantitative proteomics temperature

SCI ; EI

English

Others

China Postdoctoral Science Foundation[2019M663152];Times Higher Education[Y8SL031001];

WOS:000846759300001

20224613120795

Amino acids ; Biochemistry ; Cell membranes ; Cell proliferation ; Efficiency ; Metabolites ; Molecular biology ; Nitrogen ; Organic carbon ; Peptides ; Physiological models ; Resource allocation

Biological Materials and Tissue Engineering:461.2 ; Biology:461.9 ; Thermodynamics:641.1 ; Biochemistry:801.2 ; Chemical Products Generally:804 ; Organic Compounds:804.1 ; Management:912.2 ; Production Engineering:913.1

2-s2.0-85138449435

Scopus

1.CAS Key Laboratory of Tropical Marine Bio-Resources and Ecology,South China Sea Institute of Oceanology,Chinese Academy of Sciences,Guangzhou,China
2.Department of Ocean Science and Engineering,Southern University of Science and Technology (SUSTech),Shenzhen,China
3.Isotopoimics in Chemical Biology (ICB),School of Chemistry and Chemical Engineering,Shaanxi University of Science and Technology,Xi'an,China
4.Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai),Zhuhai,China
5.State Key Laboratory of Marine Environmental Science/College of the Environment and Ecology,Xiamen,China
6.BGI-Shenzhen,Shenzhen,China
7.Department of Mathematics and Statistics,University of Strathclyde,Glasgow,United Kingdom
8.Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou),Guangzhou,China

Zhang，Hao,Gu，Bowei,Zhou，Youping,et al. Multi-Omics Profiling Reveals Resource Allocation and Acclimation Strategies to Temperature Changes in a Marine Dinoflagellate[J]. Applied and environmental microbiology,2022,88(17).

Zhang，Hao.,Gu，Bowei.,Zhou，Youping.,Ma，Xiao.,Liu，Tianqi.,...&Xia，Xiaomin.(2022).Multi-Omics Profiling Reveals Resource Allocation and Acclimation Strategies to Temperature Changes in a Marine Dinoflagellate.Applied and environmental microbiology,88(17).

Zhang，Hao,et al."Multi-Omics Profiling Reveals Resource Allocation and Acclimation Strategies to Temperature Changes in a Marine Dinoflagellate".Applied and environmental microbiology 88.17(2022).