Small proteins in cyanobacteria provide a paradigm for the functional analysis of the bacterial micro-proteome

Baumgartner, Desirée; Kopf, Matthias; Klähn, Stephan; Steglich, Claudia; Hess, Wolfgang R.

doi:10.1186/s12866-016-0896-z

Cited by 56 publications

(86 citation statements)

References 73 publications

(82 reference statements)

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“…However, several studies revealed the involvement of small proteins in essential regulatory and other processes (Storz et al, 2014 ). The detection and functional characterization of small proteins in cyanobacteria has received particular attention (Baumgartner et al, 2016 ). We therefore decided to add their genes, if they were conserved and had a minimum length of 50 amino acids, to the other two genomes, leading to the numbers presented in Figure 4 .…”

Section: Resultsmentioning

confidence: 99%

Comparative Genomics of the Baltic Sea Toxic Cyanobacteria Nodularia spumigena UHCC 0039 and Its Response to Varying Salinity

et al. 2018

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Salinity is an important abiotic factor controlling the distribution and abundance of Nodularia spumigena, the dominating diazotrophic and toxic phototroph, in the brackish water cyanobacterial blooms of the Baltic Sea. To expand the available genomic information for brackish water cyanobacteria, we sequenced the isolate Nodularia spumigena UHCC 0039 using an Illumina-SMRT hybrid sequencing approach, revealing a chromosome of 5,294,286 base pairs (bp) and a single plasmid of 92,326 bp. Comparative genomics in Nostocales showed pronounced genetic similarity among Nodularia spumigena strains evidencing their short evolutionary history. The studied Baltic Sea strains share similar sets of CRISPR-Cas cassettes and a higher number of insertion sequence (IS) elements compared to Nodularia spumigena CENA596 isolated from a shrimp production pond in Brazil. Nodularia spumigena UHCC 0039 proliferated similarly at three tested salinities, whereas the lack of salt inhibited its growth and triggered transcriptome remodeling, including the up-regulation of five sigma factors and the down-regulation of two other sigma factors, one of which is specific for strain UHCC 0039. Down-regulated genes additionally included a large genetic region for the synthesis of two yet unidentified natural products. Our results indicate a remarkable plasticity of the Nodularia salinity acclimation, and thus salinity strongly impacts the intensity and distribution of cyanobacterial blooms in the Baltic Sea.

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Section: Resultsmentioning

confidence: 99%

Comparative Genomics of the Baltic Sea Toxic Cyanobacteria Nodularia spumigena UHCC 0039 and Its Response to Varying Salinity

et al. 2018

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“…Knowledge about the functions of small proteins in bacteria is limited, but small proteins have recently achieved attention (reviewed in [ 15 , 18 ]). For instance, Baumgartner et al [ 67 ] confirmed five small proteins in Synechocystis by Western blot. Neuhaus et al [ 11 ] detected 72 novel small genes in the intergenic regions of the E .…”

Section: Discussionmentioning

confidence: 99%

Discovery of numerous novel small genes in the intergenic regions of the Escherichia coli O157:H7 Sakai genome

et al. 2017

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In the past, short protein-coding genes were often disregarded by genome annotation pipelines. Transcriptome sequencing (RNAseq) signals outside of annotated genes have usually been interpreted to indicate either ncRNA or pervasive transcription. Therefore, in addition to the transcriptome, the translatome (RIBOseq) of the enteric pathogen Escherichia coli O157:H7 strain Sakai was determined at two optimal growth conditions and a severe stress condition combining low temperature and high osmotic pressure. All intergenic open reading frames potentially encoding a protein of ≥ 30 amino acids were investigated with regard to coverage by transcription and translation signals and their translatability expressed by the ribosomal coverage value. This led to discovery of 465 unique, putative novel genes not yet annotated in this E. coli strain, which are evenly distributed over both DNA strands of the genome. For 255 of the novel genes, annotated homologs in other bacteria were found, and a machine-learning algorithm, trained on small protein-coding E. coli genes, predicted that 89% of these translated open reading frames represent bona fide genes. The remaining 210 putative novel genes without annotated homologs were compared to the 255 novel genes with homologs and to 250 short annotated genes of this E. coli strain. All three groups turned out to be similar with respect to their translatability distribution, fractions of differentially regulated genes, secondary structure composition, and the distribution of evolutionary constraint, suggesting that both novel groups represent legitimate genes. However, the machine-learning algorithm only recognized a small fraction of the 210 genes without annotated homologs. It is possible that these genes represent a novel group of genes, which have unusual features dissimilar to the genes of the machine-learning algorithm training set.

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“…Samples for protein and amino acid extraction were taken prior to and in short intervals after adding NH 4 Cl in a final concentration of 10 mM. Proteins were extracted from cells harvested by centrifugation, separated by SDS-PAGE and transferred to nitrocellulose membranes as described previously ( 52 ). Membranes were blocked with TBS-T containing 5% milk powder and probed with sera containing anti-IF17 (1:2000) or anti-TrxA (1:5000).…”

Section: Methodsmentioning

confidence: 99%

A glutamine riboswitch is a key element for the regulation of glutamine synthetase in cyanobacteria

Klähn

Bolay

Wright

et al. 2018

Nucleic Acids Research

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As the key enzyme of bacterial nitrogen assimilation, glutamine synthetase (GS) is tightly regulated. In cyanobacteria, GS activity is controlled by the interaction with inactivating protein factors IF7 and IF17 encoded by the genes gifA and gifB, respectively. We show that a glutamine-binding aptamer within the gifB 5′ UTR of Synechocystis sp. PCC 6803 is critical for the expression of IF17. Binding of glutamine induced structural re-arrangements in this RNA element leading to enhanced protein synthesis in vivo and characterizing it as a riboswitch. Mutagenesis showed the riboswitch mechanism to contribute at least as much to the control of gene expression as the promoter-mediated transcriptional regulation. We suggest this and a structurally related but distinct element, to be designated type 1 and type 2 glutamine riboswitches. Extended biocomputational searches revealed that glutamine riboswitches are exclusively but frequently found in cyanobacterial genomes, where they are primarily associated with gifB homologs. Hence, this RNA-based sensing mechanism is common in cyanobacteria and establishes a regulatory feedback loop that couples the IF17-mediated GS inactivation to the intracellular glutamine levels. Together with the previously described sRNA NsiR4, these results show that non-coding RNA is an indispensable component in the control of nitrogen assimilation in cyanobacteria.

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Small proteins in cyanobacteria provide a paradigm for the functional analysis of the bacterial micro-proteome

Cited by 56 publications

References 73 publications

Comparative Genomics of the Baltic Sea Toxic Cyanobacteria Nodularia spumigena UHCC 0039 and Its Response to Varying Salinity

Comparative Genomics of the Baltic Sea Toxic Cyanobacteria Nodularia spumigena UHCC 0039 and Its Response to Varying Salinity

Discovery of numerous novel small genes in the intergenic regions of the Escherichia coli O157:H7 Sakai genome

A glutamine riboswitch is a key element for the regulation of glutamine synthetase in cyanobacteria

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