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Comparative genome-wide identification of transcriptional start sites in two environmentally relevant cyanobacteria reveals unexpected diversity in the transcriptome architecture

ABSTRACT: Prochlorococcus is a genus of abundant and ecologically important marine cyanobacteria. Here, we present the comprehensive comparison of the structure and composition of the transcriptomes of two closely related Prochlorococcus strains, which, despite their similarities, have adapted their gene pool to specific environmental constraints. We used large-scale strand-specific cDNA sequencing, microarray RNA profiling and computational analyses to characterize the transcriptomes of Prochlorococcus sp. MED4 and Prochlorococcus sp. MIT9313, representatives of the two major ecotypes adapted to high and low light conditions, respectively. We present genome-wide maps of transcriptional start sites (TSS) for both organisms. Our data suggest antisense transcription for three quarters of all genes. A direct comparison revealed very little conservation in the use of TSS and the nature of non-coding transcripts between both strains. We conclude that the major transcriptional output from these highly streamlined genomes consists of antisense RNA and that a hitherto unrecognized high degree of variability exists in the transcriptional architecture of these rapidly evolving prokaryotes. Furthermore, we detected extremely short 5’ untranslated regions with a median length of only 27 nt and 29 nt for MED4 and MIT9313, respectively, and noticed the absence of the Shine-Dalgarno motif, which is suggestive of alternative mechanisms for the initiation of translation. For 8 % of all protein-coding genes, the median length to the initiator codon is 10 nt or shorter, suggesting that leaderless translation and ribosomal protein S1-dependent translation constitute the primary avenues for protein synthesis in Prochlorococcus.

ORGANISM(S): Prochlorococcus marinus str. MIT 9313 Tiamatvirus PSSP7 Prochlorococcus marinus subsp. pastoris str. CCMP1986 Prochlorococcus phage P-SSM4

PROVIDER: GSE53065 | GEO | 2013/12/07

SECONDARY ACCESSION(S): PRJNA230785

REPOSITORIES: GEO

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Project description:Prochlorococcus is a genus of abundant and ecologically important marine cyanobacteria. Here, we present the comprehensive comparison of the structure and composition of the transcriptomes of two closely related Prochlorococcus strains, which, despite their similarities, have adapted their gene pool to specific environmental constraints. We used large-scale strand-specific cDNA sequencing, microarray RNA profiling and computational analyses to characterize the transcriptomes of Prochlorococcus sp. MED4 and Prochlorococcus sp. MIT9313, representatives of the two major ecotypes adapted to high and low light conditions, respectively. We present genome-wide maps of transcriptional start sites (TSS) for both organisms. Our data suggest antisense transcription for three quarters of all genes. A direct comparison revealed very little conservation in the use of TSS and the nature of non-coding transcripts between both strains. We conclude that the major transcriptional output from these highly streamlined genomes consists of antisense RNA and that a hitherto unrecognized high degree of variability exists in the transcriptional architecture of these rapidly evolving prokaryotes. Furthermore, we detected extremely short 5M-bM-^@M-^Y untranslated regions with a median length of only 27 nt and 29 nt for MED4 and MIT9313, respectively, and noticed the absence of the Shine-Dalgarno motif, which is suggestive of alternative mechanisms for the initiation of translation. For 8 % of all protein-coding genes, the median length to the initiator codon is 10 nt or shorter, suggesting that leaderless translation and ribosomal protein S1-dependent translation constitute the primary avenues for protein synthesis in Prochlorococcus. Prochlorococcus cells were either grown under standard growth conditions or various stress conditions (darkness, high light, iron or nitrogen depletion, cold or heat stress). Stress conditions were subsequently pooled and hybridized on one microarray.

Project description:We compared changes induced by the addition of 100 nM and 5 mM glucose on the proteome and metabolome complements in Synechococcus sp. strains WH8102, WH7803, and BL107 and Prochlorococcus sp. strains MED4, SS120, and MIT9313, grown either under standard light conditions or in darkness. Our results suggested that glucose is metabolized by these cyanobacteria, using primarily the oxidative pentoses and Calvin pathways, while no proof was found for the involvement of the Entner-Doudoroff pathway in this process. We observed differences in the effects of glucose availability, both between genera and between Prochlorococcus MED4 and SS120 strains, which might be related to their specific adaptations to the environment. We found evidence for fermentation in Prochlorococcus sp. strain SS120 and Synechococcus sp. strain WH8102 after 5 mM glucose addition. Our results additionally suggested that marine cyanobacteria can detect nanomolar glucose concentrations in the environment and that glucose might be used to sustain metabolism under darkness. Furthermore, the KaiB and KaiC proteins were also affected in Synechococcus sp. WH8102, pointing to a direct link between glucose assimilation and circadian rhythms in marine cyanobacteria. In conclusion, our study provides a wide overview on the metabolic effects induced by glucose availability in representative strains of the diverse marine picocyanobacteria, providing further evidence for the importance of mixotrophy in marine picocyanobacteria. The Prochlorococcus sp. strain PCC 9511 is genetically identical to MED4IMPORTANCE Glucose uptake by marine picocyanobacteria has been previously described and strongly suggests they are mixotrophic organisms (capable of using energy from the sun to make organic matter, but also to directly use organic matter from the environment when available). However, a detailed analysis of the effects of glucose addition on the proteome and metabolome of these microorganisms had not been carried out. Here, we analyzed three Prochlorococcus sp. and three Synechococcus sp. strains which were representative of several marine picocyanobacterial clades. We observed differential features in the effects of glucose availability, depending on both the genus and strain; our study illuminated the strategies utilized by these organisms to metabolize glucose and showed unexpected links to other pathways, such as circadian regulation. Furthermore, we found glucose addition had profound effects in the microbiome, favoring the growth of coexisting heterotrophic bacteria.

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Comparative genome-wide identification of transcriptional start sites in two environmentally relevant cyanobacteria reveals unexpected diversity in the transcriptome architecture

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