Distinct and redundant functions of three homologs of RNase III in the cyanobacterium Synechococcus sp. strain PCC 7002

Gordon, Gina C.; Cameron, Jeffrey C.; Pfleger, Brian F.

doi:10.1093/nar/gky041

Cited by 10 publications

(13 citation statements)

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“…Recently, RNase III was also implicated in global gene expression in the cyanobacterium Synechococcus sp. strain PCC 7002 [ 68 ] whose genome harbours three RNase III homologs (A0061, A2542, A0384). A second L. indica RNase III-encoding gene, rnc1 (_30253) was repressed in P2 (FC > 2, FDR = 0.000) but not regulated in P6 cells in our original analysis prior to normalization ( Table S2 ), after which it was not withheld as a DEG ( Table S4 ).…”

Section: Resultsmentioning

confidence: 99%

“…The rnc1 and rnc2 products were 49% and 57% identical to A2542 and A0061, respectively, but a third homolog corresponding to the Synechococcus A0384 “Mini-RNase III” was not found in the L. indica PCC 8005 proteome (via BLASTp using A0384 as a query). It has been suggested that the Synechococcus A0061 and A2542 RNase III play a role in processing pre-23S-rRNA explaining the significant alterations in the genome-wide expression patterns of single and combined ΔA2542/Δ0061 mutants [ 68 ]. Seen in this context, the high induction of rnc2 in response to γ-radiation in both P2 and P6 might be related to switches and rerouting of global protein expression and hence increased needs in RNA degradation, maturation and processing.…”

Section: Resultsmentioning

confidence: 99%

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Genetic Responses of Metabolically Active Limnospira indica Strain PCC 8005 Exposed to γ-Radiation during Its Lifecycle

et al. 2021

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Two morphotypes of the cyanobacterial Limnospira indica (formerly Arthrospira sp.) strain PCC 8005, denoted as P2 (straight trichomes) and P6 (helical trichomes), were subjected to chronic gamma radiation from spent nuclear fuel (SNF) rods at a dose rate of ca. 80 Gy.h−1 for one mass doubling period (approximately 3 days) under continuous light with photoautotrophic metabolism fully active. Samples were taken for post-irradiation growth recovery and RNA-Seq transcriptional analysis at time intervals of 15, 40, and 71.5 h corresponding to cumulative doses of ca. 1450, 3200, and 5700 Gy, respectively. Both morphotypes, which were previously reported by us to display different antioxidant capacities and differ at the genomic level in 168 SNPs, 48 indels and 4 large insertions, recovered equally well from 1450 and 3200 Gy. However, while the P2 straight type recovered from 5700 Gy by regaining normal growth within 6 days, the P6 helical type took about 13 days to recover from this dose, indicating differences in their radiation tolerance and response. To investigate these differences, P2 and P6 cells exposed to the intermediate dose of gamma radiation (3200 Gy) were analyzed for differential gene expression by RNA-Seq analysis. Prior to batch normalization, a total of 1553 genes (887 and 666 of P2 and P6, respectively, with 352 genes in common) were selected based on a two-fold change in expression and a false discovery rate FDR smaller or equal to 0.05. About 85% of these 1553 genes encoded products of yet unknown function. Of the 229 remaining genes, 171 had a defined function while 58 genes were transcribed into non-coding RNA including 21 tRNAs (all downregulated). Batch normalization resulted in 660 differentially expressed genes with 98 having a function and 32 encoding RNA. From PCC 8005-P2 and PCC 8005-P6 expression patterns, it emerges that although the cellular routes used by the two substrains to cope with ionizing radiation do overlap to a large extent, both strains displayed a distinct preference of priorities.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Genetic Responses of Metabolically Active Limnospira indica Strain PCC 8005 Exposed to γ-Radiation during Its Lifecycle

et al. 2021

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“…In cyanobacteria, RNase III proteins are likely also dispensable. Loss of each of the two RNase III proteins, or of both, in Synechococcus PCC 7002 did not significantly affect cell growth, although it led to altered expression of hundreds of genes 47,63 . In Anabaena PCC 7120, at least one of the RNase III‐encoding genes, alr0280 , could be inactivated; however, the phenotype of the mutant was not mentioned 66 .…”

Section: Endoribonucleasesmentioning

confidence: 96%

“…Thus, maturing stable RNAs may be a common function of bacterial RNase III proteins. Disruption of the gene encoding A2542, the other RNase III family protein in Synechococcus PCC 7002, did not affect rRNA maturation but greatly increased the copy number of the endogenous plasmid pAQ3 63 . The mechanism of plasmid copy number control by A2542 remains unclear.…”

Section: Endoribonucleasesmentioning

confidence: 99%

“Life is short, and art is long”: RNA degradation in cyanobacteria and model bacteria

Zhang

Hess

Zhang

2022

mLife

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RNA turnover plays critical roles in the regulation of gene expression and allows cells to respond rapidly to environmental changes. In bacteria, the mechanisms of RNA turnover have been extensively studied in the models Escherichia coli and Bacillus subtilis, but not much is known in other bacteria. Cyanobacteria are a diverse group of photosynthetic organisms that have great potential for the sustainable production of valuable products using CO2 and solar energy. A better understanding of the regulation of RNA decay is important for both basic and applied studies of cyanobacteria. Genomic analysis shows that cyanobacteria have more than 10 ribonucleases and related proteins in common with E. coli and B. subtilis, and only a limited number of them have been experimentally investigated. In this review, we summarize the current knowledge about these RNA‐turnover‐related proteins in cyanobacteria. Although many of them are biochemically similar to their counterparts in E. coli and B. subtilis, they appear to have distinct cellular functions, suggesting a different mechanism of RNA turnover regulation in cyanobacteria. The identification of new players involved in the regulation of RNA turnover and the elucidation of their biological functions are among the future challenges in this field.

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“…Another reason motivating the study of RNA degradation in PCC 7002 is its unique array of RNases that facilitate both RNA maturation and degradation. The functions of three homologs of RNase III have been studied ( 22 ), but PCC 7002 also has both an essential homolog of RNase E (a hallmark of RNA degradation in E. coli ) and an essential homolog of RNase J (a hallmark of RNA degradation in B. subtilis ) ( 23 ). The impact of the presence of both essential enzymes on RNA turnover remains unexplained.…”

Section: Introductionmentioning

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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Distinct and redundant functions of three homologs of RNase III in the cyanobacterium Synechococcus sp. strain PCC 7002

Cited by 10 publications

References 61 publications

Genetic Responses of Metabolically Active Limnospira indica Strain PCC 8005 Exposed to γ-Radiation during Its Lifecycle

Genetic Responses of Metabolically Active Limnospira indica Strain PCC 8005 Exposed to γ-Radiation during Its Lifecycle

“Life is short, and art is long”: RNA degradation in cyanobacteria and model bacteria

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

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