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A Specific Single Nucleotide Polymorphism in the ATP Synthase Gene Significantly Improves Environmental Stress Tolerance of Synechococcus elongatus PCC 7942.

ABSTRACT: In response to a broad range of habitats and environmental stresses, cyanobacteria have evolved various effective acclimation strategies, which will be helpful for improving the stress tolerances of photosynthetic organisms, including higher plants. Synechococcus elongatus UTEX 2973 and PCC 7942 possess genomes that are 99.8% identical but exhibit significant differences in cell growth and stress tolerance. In this study, we found that a single amino acid substitution at FoF1 ATP synthase subunit ? (AtpA), C252Y, is the primary contributor to the improved stress tolerance of S. elongatus UTEX 2973. Site-saturation mutagenesis experiments showed that point mutations of cysteine 252 to any of the four conjugated amino acids could significantly improve the stress tolerance of S. elongatus PCC 7942. We further confirmed that the C252Y mutation increases AtpA protein levels, intracellular ATP synthase activity, intracellular ATP abundance, transcription of psbA genes (especially psbA2), photosystem II activity, and glycogen accumulation in S. elongatus PCC 7942. This work highlights the importance of AtpA in improving the stress tolerance of cyanobacteria and provides insight into how cyanobacteria evolve via point mutations in the face of environmental selection pressures.IMPORTANCE Two closely related Synechococcus strains showed significantly different tolerances to high light and high temperature but limited genomic differences, providing us opportunities to identify key genes responsible for stress acclimation by a gene complementation approach. In this study, we confirmed that a single point mutation in the ? subunit of FoF1 ATP synthase (AtpA) contributes mainly to the improved stress tolerance of Synechococcus elongatus UTEX 2973. The point mutation of AtpA, the important ATP-generating complex of photosynthesis, increases AtpA protein levels, intracellular ATP synthase activity, and ATP concentrations under heat stress, as well as photosystem II activity. This work proves the importance of ATP synthase in cyanobacterial stress acclimation and provides a good target for future improvement of cyanobacterial stress tolerance by metabolic engineering.

SUBMITTER: Lou W

PROVIDER: S-EPMC6121992 | biostudies-literature | 2018 Sep

REPOSITORIES: biostudies-literature

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A Specific Single Nucleotide Polymorphism in the ATP Synthase Gene Significantly Improves Environmental Stress Tolerance of Synechococcus elongatus PCC 7942.

Lou Wenjing W Tan Xiaoming X Song Kuo K Zhang Shanshan S Luan Guodong G Li Cheng C Lu Xuefeng X

Applied and environmental microbiology 20180831 18

In response to a broad range of habitats and environmental stresses, cyanobacteria have evolved various effective acclimation strategies, which will be helpful for improving the stress tolerances of photosynthetic organisms, including higher plants. <i>Synechococcus elongatus</i> UTEX 2973 and PCC 7942 possess genomes that are 99.8% identical but exhibit significant differences in cell growth and stress tolerance. In this study, we found that a single amino acid substitution at F<sub>o</sub>F<su ...[more]

PMID: 30006407

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Project description:Cyanobacteria are excellent autotrophic photosynthetic chassis employed in synthetic biology, and previous studies have suggested that they have alkaline tolerance but low acid tolerance, significantly limiting their productivity as photosynthetic chassis and necessitating investigations into the acid stress resistance mechanism. In this study, differentially expressed genes were obtained by RNA sequencing-based comparative transcriptomic analysis under long-term acidic stress conditions and acidic shock treatment, in the model cyanobacterium Synechococcus elongatus PCC 7942. A pathway enrichment analysis revealed the upregulated and downregulated pathways during long-term acidic and shock stress treatment. The subsequent single gene knockout and phenotype analysis showed that under acidic stress conditions, the strains with chlL, chlN, pex, synpcc7942_2038, synpcc7942_1890, or synpcc7942_2547 knocked out grew worse than the wild type, suggesting their involvement in acid tolerance. This finding was further confirmed by introducing the corresponding genes back into the knockout mutant individually. Moreover, individual overexpression of the chlL and chlN genes in the wild type successfully improved the tolerance of S. elongatus PCC 7942 to acidic stress. This work successfully identified six genes involved in acidic stress responses, and overexpressing chIL or chIN individually successfully improved acid tolerance in S. elongatus PCC 7942, providing valuable information to better understand the acid resistance mechanism in S. elongatus PCC 7942 and novel insights into the robustness and tolerance engineering of cyanobacterial chassis. KEY POINTS: • DEGs were identified by RNA-seq based transcriptomics analysis in response to acidic stress in S. elongatus PCC 7942. • Six genes were identified to be involved in acid tolerance in S. elongatus PCC 7942. • Overexpression of chIL or chIN individually successfully improved the acid tolerance of S. elongatus PCC 7942.

Dataset Information

A Specific Single Nucleotide Polymorphism in the ATP Synthase Gene Significantly Improves Environmental Stress Tolerance of Synechococcus elongatus PCC 7942.

Publications

A Specific Single Nucleotide Polymorphism in the ATP Synthase Gene Significantly Improves Environmental Stress Tolerance of Synechococcus elongatus PCC 7942.

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