Identification of the DNA methyltransferases establishing the methylome of the cyanobacterium Synechocystis sp. PCC 6803

Hagemann, Martin; Gärtner, Katrin; Scharnagl, Matthias; Bolay, Paul; Lott, Steffen C.; Fuß, Janina; Huettel, Bruno; Reinhardt, Richard; Klähn, Stephan; Hess, Wolfgang R.

doi:10.1093/dnares/dsy006

Cited by 26 publications

(43 citation statements)

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“…PCC 6803 (hereafter Synechocystis ), which does not express an active RM system. However, five different sites are methylated in the DNA of Synechocystis and the cognate methyltransferases were assigned (Scharnagl et al, 1998; Hagemann et al, 2018). Three DNA methyltransferases are encoded on the Synechocystis chromosome, M.Ssp6803I responsible for m5 CGATCG methylation, M.Ssp6803II for GG 4m CC, and M.Ssp6803III for the dam-like G m6 ATC methylation.…”

Section: Introductionmentioning

confidence: 99%

Cytosine N4-Methylation via M.Ssp6803II Is Involved in the Regulation of Transcription, Fine- Tuning of DNA Replication and DNA Repair in the Cyanobacterium Synechocystis sp. PCC 6803

et al. 2019

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DNA methylation plays a crucial role for gene regulation among eukaryotes, but its regulatory function is less documented in bacteria. In the cyanobacterium Synechocystis sp. PCC 6803 five DNA methyltransferases have been identified. Among them, M.Ssp6803II is responsible for the specific methylation of the first cytosine in the frequently occurring motif GGCC, leading to N4-methylcytosine (GG m4 CC). The mutation of the corresponding gene sll0729 led to lowered chlorophyll/phycocyanin ratio and slower growth. Transcriptomics only showed altered expression of sll0470 and sll1526 , two genes encoding hypothetical proteins. Moreover, prolonged cultivation revealed instability of the initially obtained phenotype. Colonies with normal pigmentation and wild-type-like growth regularly appeared on agar plates. These colonies represent suppressor mutants, because the sll0729 gene was still completely inactivated and the GGCC sites remained unmethylated. The suppressor strains showed smaller cell size, lowered DNA content per cell, and decreased tolerance against UV compared to wild type. Promoter assays revealed that the transcription of the sll0470 gene was still stimulated in the suppressor clones. Proteomics identified decreased levels of DNA topoisomerase 4 subunit A in suppressor cells. Collectively, these results indicate that GG m4 CC methylation is involved in the regulation of gene expression, in the fine-tuning of DNA replication, and DNA repair mechanisms.

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Section: Introductionmentioning

confidence: 99%

Cytosine N4-Methylation via M.Ssp6803II Is Involved in the Regulation of Transcription, Fine- Tuning of DNA Replication and DNA Repair in the Cyanobacterium Synechocystis sp. PCC 6803

et al. 2019

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“…The first genome-wide study of m 5 C at base resolution was carried out by applying WGBS into E. coli and found cytosine methylation may take part in regulation of gene expression in stationary phase as a regulator ( Kahramanoglou et al, 2012 ). With respect to cyanobacteria, SMRT sequencing showed the existence of m 6 A in Microcystis ( Zhao et al, 2017 ), and Hagemann et al (2018) profiled the global DNA methylation (including m 6 A, m 4 C, and m 5 C) in Synechocystis by using combination of SMRT sequencing and WGBS, which indicated 5-methylcytosine and m 4 C in Synechocystis were in the context of m 5 CGATCG and GGm 4 CC, respectively. All these studies were conducted to determine the specificity of methyltransferases.…”

Section: Discussionmentioning

confidence: 99%

“…A similar situation for the differential influence of base outside of the target motif was found in E. coli K12 of mid-exponential phase, where the methylation level for CmCCWGG was lower than [ATG]mCCWGG (mCCWGG was the methyltransferase target motif) ( Kahramanoglou et al, 2012 ). Due to the partially resistance of m 4 C to the bisulfite-mediated deamination, the methylation level of GGm 4 CC context is much lower than that of m 5 CGATCG ( Hagemann et al, 2018 ). Consistent with this, our study also showed the methylation level of mCG methylation was higher than those of mCHG and mCHH.…”

Section: Discussionmentioning

confidence: 99%

“…Enzyme digestion experiments in two Anabaena species indicates that DNA from both species is methylated, but that no gross change in methylation occurs during heterocyst formation ( Adams, 1988 ). Recently, global DNA methylation pattern study has been conducted in Synechocystis and more methyltransferases were identified ( Hagemann et al, 2018 ).…”

Section: Introductionmentioning

confidence: 99%

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Transgenerational Epigenetic Inheritance Under Environmental Stress by Genome-Wide DNA Methylation Profiling in Cyanobacterium

Xiao

Jiang

et al. 2018

Front. Microbiol.

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Epigenetic modifications such as DNA methylation are well known as connected with many important biological processes. Rapid accumulating evidence shows environmental stress can generate particular defense epigenetic changes across generations in eukaryotes. This transgenerational epigenetic inheritance in animals and plants has gained interest over the last years. Cyanobacteria play very crucial role in the earth, and as the primary producer they can adapt to nearly all diverse environments. However, few knowledge about the genome wide epigenetic information such as methylome information in cyanobacteria, especially under any environment stress, was reported so far. In this study we profiled the genome-wide cytosine methylation from a model cyanobacterium Synechocystis sp. PCC 6803, and explored the possibility of transgenerational epigenetic process in this ancient single-celled prokaryote by comparing the DNA methylomes among normal nitrogen medium cultivation, nitrogen starvation for 72 h and nitrogen recovery for about 12 generations. Our results shows that DNA methylation patterns in nitrogen starvation and nitrogen recovery are much more similar with each other, significantly different from that of the normal nitrogen. This study reveals the difference in global DNA methylation pattern of cyanobacteria between normal and nutrient stress conditions and reports the evidence of transgenerational epigenetic process in cyanobacteria. The results of this study may contribute to a better understanding of epigenetic regulation in prokaryotic adaptation to and survive in the ever changing environment.

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“…Top hits always included the highly iterative palindrome 1 (HIP1, 5′-GGCGATCGCC-3′) sequence. This sequence is a target of methylation in other cyanobacteria and may be involved in modes of DNA repair ( 48 , 49 ). However, its role in PCC 7002 remains unexplained.…”

Section: Methodsmentioning

confidence: 99%

Genome-Wide Analysis of RNA Decay in the Cyanobacterium Synechococcus sp. Strain PCC 7002

et al. 2020

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RNA degradation is an important process that influences the ultimate concentration of individual proteins inside cells. While the main enzymes that facilitate this process have been identified, global maps of RNA turnover are available for only a few species. Even in these cases, there are few sequence elements that are known to enhance or destabilize a native transcript; even fewer confer the same effect when added to a heterologous transcript. To address this knowledge gap, we assayed genome-wide RNA degradation in the cyanobacterium Synechococcus sp. strain PCC 7002 by collecting total RNA samples after stopping nascent transcription with rifampin. We quantified the abundance of each position in the transcriptome as a function of time using RNA-sequencing data and later analyzed the global mRNA decay map using machine learning principles. Half-lives, calculated on a per-ORF (open reading frame) basis, were extremely short, with a median half-life of only 0.97 min. Despite extremely rapid turnover of most mRNA, transcripts encoding proteins involved in photosynthesis were both highly expressed and highly stable. Upon inspection of these stable transcripts, we identified an enriched motif in the 3′ untranslated region (UTR) that had similarity to Rho-independent terminators. We built statistical models for half-life prediction and used them to systematically identify sequence motifs in both 5′ and 3′ UTRs that correlate with stabilized transcripts. We found that transcripts linked to a terminator containing a poly(U) tract had a longer half-life than both those without a poly(U) tract and those without a terminator. IMPORTANCE RNA degradation is an important process that affects the final concentration of individual mRNAs, affecting protein expression and cellular physiology. Studies of how RNA is degraded increase our knowledge of this fundamental process as well as enable the creation of genetic tools to manipulate RNA stability. By studying global transcript turnover, we searched for sequence elements that correlated with transcript (in)stability and used these sequences to guide tool design. This study probes global RNA turnover in a cyanobacterium, Synechococcus sp. strain PCC 7002, that both has a unique array of RNases that facilitate RNA degradation and is an industrially relevant strain that could be used to convert CO2 and sunlight into useful products.

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Identification of the DNA methyltransferases establishing the methylome of the cyanobacterium Synechocystis sp. PCC 6803

Cited by 26 publications

References 55 publications

Cytosine N4-Methylation via M.Ssp6803II Is Involved in the Regulation of Transcription, Fine- Tuning of DNA Replication and DNA Repair in the Cyanobacterium Synechocystis sp. PCC 6803

Cytosine N4-Methylation via M.Ssp6803II Is Involved in the Regulation of Transcription, Fine- Tuning of DNA Replication and DNA Repair in the Cyanobacterium Synechocystis sp. PCC 6803

Transgenerational Epigenetic Inheritance Under Environmental Stress by Genome-Wide DNA Methylation Profiling in Cyanobacterium

Genome-Wide Analysis of RNA Decay in the Cyanobacterium Synechococcus sp. Strain PCC 7002

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