Blooms of the dinitrogen-fixing marine cyanobacterium Trichodesmium considerably contribute to new nitrogen inputs into tropical oceans. Intriguingly, only 60% of the Trichodesmium erythraeum IMS101 genome sequence codes for protein, compared with ∼85% in other sequenced cyanobacterial genomes. The extensive non-coding genome fraction suggests space for an unusually high number of unidentified, potentially regulatory non-protein-coding RNAs (ncRNAs). To identify the transcribed fraction of the genome, here we present a genome-wide map of transcriptional start sites (TSS) at single nucleotide resolution, revealing the activity of 6,080 promoters. We demonstrate that T. erythraeum has the highest number of actively splicing group II introns and the highest percentage of TSS yielding ncRNAs of any bacterium examined to date. We identified a highly transcribed retroelement that serves as template repeat for the targeted mutation of at least 12 different genes by mutagenic homing. Our findings explain the non-coding portion of the T. erythraeum genome by the transcription of an unusually high number of non-coding transcripts in addition to the known high incidence of transposable elements. We conclude that riboregulation and RNA maturation-dependent processes constitute a major part of the Trichodesmium regulatory apparatus.
Bibliographical noteFunding Information:
This work was supported by the BMBF JOINT GERMAN-ISRAELI RESEARCH PROJECTS, project number GR2378/03F0640A, the GERMAN-ISRAELI RESEARCH FOUNDATION (GIF), project number 1133-13.8/2011 to W.R.H. and I.B.F. and by the EU project MaCuMBA (Marine Microorganisms: Cultivation Methods for Improving their Biotechnological Applications; grant agreement no: 311975 to W.R.H.). We thank Edward F. DeLong for permission to study a metagenomic dataset obtained from Trichodesmium natural colonies off the coast at Oahu, Hawaii (IMG Submission ID 8735).
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