Translating Divergent Environmental Stresses into a Common Proteome Response through the Histidine Kinase 33 (Hik33) in a Model Cyanobacterium.

Haitao Ge,Ye Liu,Yuanya Zhang,Qingfang He,Longfa Fang,Yingchun Wang,Wu Xu,Xiahe Huang,Xiaorong Wang,Weiyang Chen,Jinlong Wang

doi:10.1074/mcp.m116.068080

Haitao Ge, Ye Liu + Show 9 more

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https://doi.org/10.1074/mcp.m116.068080

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The histidine kinase Hik33 plays important roles in mediating cyanobacterial response to divergent types of abiotic stresses including cold, salt, high light (HL), and osmotic stresses. However, how these functions are regulated by Hik33 remains to be addressed. Using a hik33-deficient strain (Δhik33) of Synechocystis sp. PCC 6803 (Synechocystis) and quantitative proteomics, we found that Hik33 depletion induces differential protein expression highly like that induced by divergent types of stresses. This typically includes downregulation of proteins in photosynthesis and carbon assimilation that are necessary for cell propagation, and upregulation of heat shock proteins, chaperons, and proteases that are important for cell survival. This observation indicates that depletion of Hik33 alone mimics divergent types of abiotic stresses, and that Hik33 could be important for preventing abnormal stress response in the normal condition. Moreover, we found most proteins of plasmid origin were significantly upregulated in Δhik33, though their biological significance remains to be addressed. Together, the systematically characterized Hik33-regulated cyanobacterial proteome, which is largely involved in stress responses, builds the molecular basis for Hik33 as a general regulator of stress responses.

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From the ‡State Key Laboratory of Microbial Technology, College of Life Science, Shandong University, Jinan 250100, China; §State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, No.1 West Beichen Rd., Beijing 100101, China; ¶University of Chinese Academy of Sciences, Beijing, 100049, China; ʈDepartment of Chemistry, University of Louisiana at Lafayette, Lafayette, Louisiana 70504; **Department of Applied Science, University of Arkansas at Little Rock, Little Rock, Arkansas
Depletion of Hik33 Resulted in Differential Protein Expression in Synechocystis—The ⌬hik33 mutant was firstly confirmed for the complete depletion of hik33 and the repressed photoautotrophic growth [15] (Fig. 1A)
Proteins extracted from the whole cell lysate (WCL), the membrane fraction, and the soluble fraction from both the wild type (WT) and the mutant strains of Synechocystis were separated by sodium dodecyl sulfate (SDS)-PAGE and visualized with Coomassie blue staining

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In the downregulated proteins in ⌬hik33, genes downregulated in different types of stresses including cold, HL, osmotic, peroxide, salt, and UV irradiation were significantly enriched (Fig. 6A, upper panel, Fig. 6C– 6I, and supplemental Table S2). Determination of Hik33-regulated Common Stress-responsive (CSR) Proteins—To find proteins that are regulated by Hik33 and commonly involved in different types of stresses, we selected only differentially expressed proteins in ⌬hik33 whose coding genes are concordantly upregulated or downregulated in at least three out of the eight stress conditions, either in transcription or translation (Fig. 6).

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