Leaderless genes in bacteria: clue to the evolution of translation initiation mechanisms in prokaryotes

Zheng, Xiaobin; Hu, Gangqing; She, Zhen‐Su; Zhu, Huaiqiu

doi:10.1186/1471-2164-12-361

Cited by 107 publications

(101 citation statements)

References 57 publications

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“…Together, our data indicate that S1 protein-mediated and leaderless translation constitute mechanisms for translation initiation, whereas Shine-Dalgarno sequence-dependent translation initiation plays a secondary role (if at all) in Prochlorococcus. Zheng et al (2011) determined cyanobacterial-specific sequence signatures in the 5 0 UTR and suggested that other so far unknown mechanisms of translation initiation must exist, which is in total agreement with our results.…”

Section: Utrs In Prochlorococcussupporting

confidence: 91%

“…Here we found in both strains B8% of all gTSS to be located within the first 10 nt to the initiation codon of translation, suggesting that leaderless translation occurs in Prochlorococcus. This is in agreement with computational predictions based on 953 bacterial and 72 archaeal genomes, which suggested that leaderless transcription is widespread among bacteria (207 of the 953 genomes) although not dominant (Zheng et al, 2011). Transcription starts for 30 MED4 ORFs and 41 MIT9313 ORFs on the first nucleotide of the start codon.…”

Section: Utrs In Prochlorococcussupporting

confidence: 89%

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Comparative transcriptomics of two environmentally relevant cyanobacteria reveals unexpected transcriptome diversity

et al. 2014

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Prochlorococcus is a genus of abundant and ecologically important marine cyanobacteria. Here, we present a comprehensive comparison of the structure and composition of the transcriptomes of two Prochlorococcus strains, which, despite their similarities, have adapted their gene pool to specific environmental constraints. We present genome-wide maps of transcriptional start sites (TSS) for both organisms, which are representatives of the two most diverse clades within the two major ecotypes adapted to high-and low-light conditions, respectively. Our data suggest antisense transcription for three-quarters of all genes, which is substantially more than that observed in other bacteria. We discovered hundreds of TSS within genes, most notably within 16 of the 29 prochlorosin genes, in strain MIT9313. A direct comparison revealed very little conservation in the location of TSS and the nature of non-coding transcripts between both strains. We detected extremely short 5 0 untranslated regions with a median length of only 27 and 29 nt for MED4 and MIT9313, respectively, and for 8% of all protein-coding genes the median distance to the start codon is only 10 nt or even shorter. These findings and the absence of an obvious Shine-Dalgarno motif suggest that leaderless translation and ribosomal protein S1-dependent translation constitute alternative mechanisms for translation initiation in Prochlorococcus. We conclude that genomewide antisense transcription is a major component of the transcriptional output from these relatively small genomes and that a hitherto unrecognized high degree of complexity and variability of gene expression exists in their transcriptional architecture.

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Section: Utrs In Prochlorococcussupporting

confidence: 91%

Section: Utrs In Prochlorococcussupporting

confidence: 89%

Comparative transcriptomics of two environmentally relevant cyanobacteria reveals unexpected transcriptome diversity

et al. 2014

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“…Leaderless initiation has been observed in many species of bacteria and archaea (37,38). The binding sequence of AveT extends from positions Ϫ58 to Ϫ24 nt relative to the aveT TSS and from positions Ϫ90 to Ϫ56 nt relative to the pepD2 TSS (Fig.…”

Section: Resultsmentioning

confidence: 95%

Increasing Avermectin Production in Streptomyces avermitilis by Manipulating the Expression of a Novel TetR-Family Regulator and Its Target Gene Product

Liu

Zhang

Guo

et al. 2015

Appl Environ Microbiol

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Avermectins produced by Streptomyces avermitilis are commercially important anthelmintic agents. The detailed regulatory mechanisms of avermectin biosynthesis remain unclear. Here, we identified SAV3619, a TetR-family transcriptional regulator designated AveT, to be an activator for both avermectin production and morphological differentiation in S. avermitilis. AveT was shown to indirectly stimulate avermectin production by affecting transcription of the cluster-situated activator gene aveR. AveT directly repressed transcription of its own gene (aveT), adjacent gene pepD2 (sav_3620), sav_7490 (designated aveM), and sav_7491 by binding to an 18-bp perfect palindromic sequence (CGAAACGKTKYCGTTTCG, where K is T or G and Y is T or C and where the underlining indicates inverted repeats) within their promoter regions. aveM (which encodes a putative transmembrane efflux protein belonging to the major facilitator superfamily [MFS]), the important target gene of AveT, had a striking negative effect on avermectin production and morphological differentiation. Overexpression of aveT and deletion of aveM in wild-type and industrial strains of S. avermitilis led to clear increases in the levels of avermectin production. In vitro gel-shift assays suggested that C-5-O-B1, the late pathway precursor of avermectin B1, acts as an AveT ligand. Taken together, our findings indicate positive-feedback regulation of aveT expression and avermectin production by a late pathway intermediate and provide the basis for an efficient strategy to increase avermectin production in S. avermitilis by manipulation of AveT and its target gene product, AveM. Soil-dwelling species of Streptomyces produce about half of currently known antibiotics (including antibacterial, anticancer, anthelmintic, and immunosuppressive agents) during their complex morphological differentiation cycle (1) and have many important medical and commercial applications. Antibiotic biosynthesis is controlled by large gene clusters, usually including cluster-situated regulators (CSRs). These CSRs are at the lowest level of the complex regulatory network for antibiotic biosynthesis and are controlled by various higher-level pleiotropic regulators in response to developmental state, population density, environmental signals, and physiological signals (2-4).The species Streptomyces avermitilis produces avermectins, a series of 16-membered macrocyclic lactones (termed A1a, A1b, A2a, A2b, B1a, B1b, B2a, and B2b) that are excellent anthelmintic agents with high potency, broad-spectrum activity against various arthropod and nematode parasites, and a low level of side effects on the host (5, 6). Of the eight avermectin components, B1a has the highest insecticidal activity (7). Avermectins are a commercially important group of antibiotics with annual worldwide sales of ϳ$850 million (8) and are widely applied in the agricultural, veterinary, and medical fields. The 82-kb ave gene cluster that controls avermectin biosynthesis includes 18 open reading frames (ORFs) (9). The gene aveR, loc...

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“…and of adnA and adnB in Rhodococcus erythropolis, both actinomycetes. Interestingly, the promoter motifs are positioned only 7 nucleotides upstream from the predicted translational start codon of adnB in both S. coelicolor and S. ambofaciens, suggesting that these genes may be leaderless genes that are widespread in actinobacteria (45).…”

Section: Resultsmentioning

confidence: 99%

The adnAB Locus, Encoding a Putative Helicase-Nuclease Activity, Is Essential in Streptomyces

et al. 2014

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bHomologous recombination is a crucial mechanism that repairs a wide range of DNA lesions, including the most deleterious ones, double-strand breaks (DSBs). This multistep process is initiated by the resection of the broken DNA ends by a multisubunit helicase-nuclease complex exemplified by Escherichia coli RecBCD, Bacillus subtilis AddAB, and newly discovered Mycobacterium tuberculosis AdnAB. Here we show that in Streptomyces, neither recBCD nor addAB homologues could be detected. The only putative helicase-nuclease-encoding genes identified were homologous to M. tuberculosis adnAB genes. These genes are conserved as a single copy in all sequenced genomes of Streptomyces. The disruption of adnAB in Streptomyces ambofaciens and Streptomyces coelicolor could not be achieved unless an ectopic copy was provided, indicating that adnAB is essential for growth. Both adnA and adnB genes were shown to be inducible in response to DNA damage (mitomycin C) and to be independently transcribed. Introduction of S. ambofaciens adnAB genes in an E. coli recB mutant restored viability and resistance to UV light, suggesting that Streptomyces AdnAB could be a functional homologue of RecBCD and be involved in DNA damage resistance. Cells are under constant genotoxic pressure from both endogenous and exogenous sources. DNA damage needs to be repaired to avoid the formation of deleterious mutations, abortion of replication, and lethal chromosomal breakage. Homologous recombination (HR) is a crucial mechanism that repairs a variety of DNA lesions, including DNA double-strand breaks (DSBs), single-strand DNA gaps, and interstrand cross-links.DSBs are probably the most deleterious DNA damage that a cell can encounter. They are induced in cells by physical agents such as ionizing radiation or UV light, chemical agents, and natural products such as mitomycin C (MMC) or bleomycin. DSBs also result from replication fork collapse during chromosomal replication (1). The failure to repair DSBs can lead to cell death and, in the case of disrepair, can trigger large-scale chromosome rearrangements, favoring the generation of genetic diversity.In bacteria, DSBs are for the most part processed through HR, which requires a homologous DNA template to carry out faithful repair of the damaged DNA duplex. In intensively replicating cells (vegetative growth phase) or immediately after the passing of the replication fork, the sister chromatid can be used as an intact template. In nonreplicating phases, such as late stationary phase or in spores (which contain a single copy of the chromosome), DSBs are more likely repaired by an illegitimate repair pathway. Indeed, illegitimate recombination (IR) does not require an intact homologous sequence but as a consequence has reduced fidelity.The involvement of DSB repair by HR in a range of fundamental cellular processes (e.g., chromosome integrity, replication, segregation, etc.) reveals that HR is conserved in all living organisms. The initiating step of the repair mechanism consists of the resection of the DSB...

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Leaderless genes in bacteria: clue to the evolution of translation initiation mechanisms in prokaryotes

Cited by 107 publications

References 57 publications

Comparative transcriptomics of two environmentally relevant cyanobacteria reveals unexpected transcriptome diversity

Comparative transcriptomics of two environmentally relevant cyanobacteria reveals unexpected transcriptome diversity

Increasing Avermectin Production in Streptomyces avermitilis by Manipulating the Expression of a Novel TetR-Family Regulator and Its Target Gene Product

The adnAB Locus, Encoding a Putative Helicase-Nuclease Activity, Is Essential in Streptomyces

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