Comparative transcriptomics of two environmentally relevant cyanobacteria reveals unexpected transcriptome diversity

Abstract

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.

Transcriptional response of Prochlorococcus to co-culture with a marine Alteromonas: differences between strains and the involvement of putative infochemicals

“…Differential expression (DE) analysis was performed using the Rockhopper program (McClure et al, 2013). Similar to previous studies (Waldbauer et al, 2012;Voigt et al, 2014), we observed antisense expression in most of the genes (766/1716 genes in MED4 and 2060/2274 genes in MIT9313). Little is currently known about the function of these antisense RNAs, and thus we focused our analysis on protein-coding genes.…”

“…However, many of the predicted CCRG-2 core peptides do not contain cysteine residues and thus cannot be modified by the ProcM enzyme to form the lanthionine ring that is one of the hallmarks of lanthipeptides (Figure 5e). Notably, in some prochlorosin genes, transcription may start downstream of the predicted open reading frame, leading to translated proteins which lack much of the N'-terminal leader sequence (Voigt et al, 2014). It is unclear whether these truncated prochlorosins can be recognized and modified by the ProcM enzyme.…”

Torn apart and reunited: impact of a heterotroph on the transcriptome of Prochlorococcus

“…After 48 h, both the NrdR transcription factor (involved in regulating ribonucleotide reductase expression (Torrents et al, 2007)) and a putative AbrB-family regulator were both transcriptionally enriched in the co-cultures, and a putative GntR-like transcription factor was found to be depleted after 24 h (Supplementary Table S2). Antisense RNAs have an important role in Prochlorococcus transcriptional regulation (Steglich et al, 2008;Voigt et al, 2014), and while they have not yet been characterized in this particular strain, we expect that they likely contributed to at least some of the changes observed.…”

Techniques for Quantifying Phytoplankton Biodiversity

“…Indeed, for many microbial populations, functional activity is regulated at the transcriptional level, so there is a strong relationship between transcripts and functionality. Furthermore, noncoding RNA is emerging as a major component of functional regulation, thus providing significant insight into physiological diversity (Voigt et al 2014). However, other functions-and, in particular, many functions associated with eukaryotic phytoplankton species-are not necessarily regulated at the transcriptional level, so care must be taken in interpretation.…”