Non-coding RNAs in marine <i>Synechococcus</i> and their regulation under environmentally relevant stress conditions

Gierga, Gregor; Voß, Björn; Hess, Wolfgang R.

doi:10.1038/ismej.2011.215

Cited by 37 publications

(24 citation statements)

References 55 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Six known structural RNA elements were identified (using RFAM) within IMS101 intergenic regions (Table S2). We also used a pipeline that has previously identified cyanobacterial noncoding RNAs (ncRNAs) (63,64) to look for Trichodesmium structural conservation between intergenic regions among IMS101 and 2175 and their in situ counterparts within metagenomic reads (SI Materials and Methods). For an in situ sympatric comparison, the same procedure was done with either Prochlorococcus (n = 5) or Synechococcus (n = 6) genomes, along with all of the assembled Sargasso Sea sequences from the Global Ocean Sampling dataset (65).…”

Section: Significancementioning

confidence: 99%

Trichodesmium genome maintains abundant, widespread noncoding DNA in situ, despite oligotrophic lifestyle

Walworth

Pfreundt

Nelson

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Understanding the evolution of the free-living, cyanobacterial, diazotroph Trichodesmium is of great importance because of its critical role in oceanic biogeochemistry and primary production. Unlike the other >150 available genomes of free-living cyanobacteria, only 63.8% of the Trichodesmium erythraeum (strain IMS101) genome is predicted to encode protein, which is 20-25% less than the average for other cyanobacteria and nonpathogenic, free-living bacteria. We use distinctive isolates and metagenomic data to show that low coding density observed in IMS101 is a common feature of the Trichodesmium genus, both in culture and in situ. Transcriptome analysis indicates that 86% of the noncoding space is expressed, although the function of these transcripts is unclear. The density of noncoding, possible regulatory elements predicted in Trichodesmium, when normalized per intergenic kilobase, was comparable and twofold higher than that found in the gene-dense genomes of the sympatric cyanobacterial genera Synechococcus and Prochlorococcus, respectively. Conserved Trichodesmium noncoding RNA secondary structures were predicted between most culture and metagenomic sequences, lending support to the structural conservation. Conservation of these intergenic regions in spatiotemporally separated Trichodesmium populations suggests possible genus-wide selection for their maintenance. These large intergenic spacers may have developed during intervals of strong genetic drift caused by periodic blooms of a subset of genotypes, which may have reduced effective population size. Our data suggest that transposition of selfish DNA, low effective population size, and high-fidelity replication allowed the unusual "inflation" of noncoding sequence observed in Trichodesmium despite its oligotrophic lifestyle. marine microbiology | oligotrophic | evolution genomics | nitrogen fixation T he low availability of N (and fixed carbon) in the midlatitude upper oceans provides an important niche for autotrophic organisms that can fix atmospheric nitrogen, which can exert control over global primary production (1-3). Nitrogen fixation is a prokaryotic process with a high-energy demand, and oceanic cyanobacteria are known to be significant sources of this "new" nitrogen (nitrogen that is fixed from the atmosphere or NO 3 advected from depth) (4, 5). Molecular field data have shown that a handful of cyanobacterial diazotrophs responsible for oligotrophic nitrogen fixation can reach relatively high cell numbers (6-12) and be of significant biogeochemical importance (13-16). These include photosynthetic free-living forms, such as the filamentous Trichodesmium and the unicellular Crocosphaera and Cyanothece, and photosynthetic and nonphotosynthetic symbiotic forms, such as heterocystous Richelia and Candidatus Atelocyanobacterium thalassa (3,5,17).Trichodesmium cells can grow either as trichomes (i.e., filaments) or aggregates and form three types of classically described colonies, including radial puffs, vertically aligned fusiform tufts, and bowties (...

show abstract

Section: Significancementioning

confidence: 99%

Trichodesmium genome maintains abundant, widespread noncoding DNA in situ, despite oligotrophic lifestyle

Walworth

Pfreundt

Nelson

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

show abstract

“…Although their regulatory targets are not well understood, sRNAs have been also been found in marine metatranscriptomes (Shi et al, 2009). Among cultured marine bacteria, only a few have been examined for sRNA control over gene expression (Steglich et al, 2008;Gierga et al, 2012;Rivers et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Small RNAs expressed during dimethylsulfoniopropionate degradation by a model marine bacterium

Burns

Bullock

Smith

et al. 2016

Environ Microbiol Rep

View full text Add to dashboard Cite

The fate of the sulfur moiety of dimethylsulfoniopropionate (DMSP) depends on the 'bacterial switch', a regulatory point between two metabolic pathways with different biogeochemical endpoints. Studies have focused on transcriptional patterns of known genes to determine physiological and environmental factors affecting this switch, but post-transcriptional regulation has been under-studied. Here we use a model bacterium containing both pathways to look for transcription of non-coding regulatory small RNAs (sRNAs) during DMSP metabolism. RNA-seq analysis of Ruegeria pomeroyi DSS-3 grown with DMSP, metabolic intermediates of DMSP degradation (MMPA or acetate), or methionine revealed 182 putative sRNAs, with 46 showing differential expression during growth on DMSP. A knockout mutant constructed for an upregulated sRNA had a phenotype that differed in its use of the two degradation pathways. Because transcription patterns of many differentially expressed sRNAs were not correlated with the transcription of their putative target gene, their effects on DMSP degradation would not be observable in the transcriptome. Overall, our results indicate that sRNAs are crucial but largely cryptic actors in regulating DMSP metabolism in this model marine bacterium and potentially other bacterial groups involved in the surface ocean sulfur cycle.

show abstract

“…Differentially expressed sRNAs in response to fluctuating environmental conditions are already known in some prokaryotes such as marine strains of the cyanobacterium Synechococcus [15]. In eukaryotes, RNAi is believed to be an ancient process that probably evolved before the basal split of the major supergroups [16], [17].…”

Section: Introductionmentioning

confidence: 99%

Evidence for Widespread Exonic Small RNAs in the Glaucophyte Alga Cyanophora paradoxa

et al. 2013

View full text Add to dashboard Cite

RNAi (RNA interference) relies on the production of small RNAs (sRNAs) from double-stranded RNA and comprises a major pathway in eukaryotes to restrict the propagation of selfish genetic elements. Amplification of the initial RNAi signal by generation of multiple secondary sRNAs from a targeted mRNA is catalyzed by RNA-dependent RNA polymerases (RdRPs). This phenomenon is known as transitivity and is particularly important in plants to limit the spread of viruses. Here we describe, using a genome-wide approach, the distribution of sRNAs in the glaucophyte alga Cyanophora paradoxa. C. paradoxa is a member of the supergroup Plantae (also known as Archaeplastida) that includes red algae, green algae, and plants. The ancient (>1 billion years ago) split of glaucophytes within Plantae suggests that C. paradoxa may be a useful model to learn about the early evolution of RNAi in the supergroup that ultimately gave rise to plants. Using next-generation sequencing and bioinformatic analyses we find that sRNAs in C. paradoxa are preferentially associated with mRNAs, including a large number of transcripts that encode proteins arising from different functional categories. This pattern of exonic sRNAs appears to be a general trend that affects a large fraction of mRNAs in the cell. In several cases we observe that sRNAs have a bias for a specific strand of the mRNA, including many instances of antisense predominance. The genome of C. paradoxa encodes four sequences that are homologous to RdRPs in Arabidopsis thaliana. We discuss the possibility that exonic sRNAs in the glaucophyte may be secondarily derived from mRNAs by the action of RdRPs. If this hypothesis is confirmed, then transitivity may have had an ancient origin in Plantae.

show abstract

Non-coding RNAs in marine Synechococcus and their regulation under environmentally relevant stress conditions

Cited by 37 publications

References 55 publications

Trichodesmium genome maintains abundant, widespread noncoding DNA in situ, despite oligotrophic lifestyle

Trichodesmium genome maintains abundant, widespread noncoding DNA in situ, despite oligotrophic lifestyle

Small RNAs expressed during dimethylsulfoniopropionate degradation by a model marine bacterium

Evidence for Widespread Exonic Small RNAs in the Glaucophyte Alga Cyanophora paradoxa

Contact Info

Product

Resources

About