Small secreted proteins enable biofilm development in the cyanobacterium Synechococcus elongatus

Parnasa, Rami; Nagar, Elad; Sendersky, Eleonora; Reich, Ziv; Simkovsky, Ryan; Golden, Susan S.; Schwarz, Rakefet

doi:10.1038/srep32209

Cited by 50 publications

(97 citation statements)

References 51 publications

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“…It is possible that release of the protein encoded by Synpcc7942_0122 to the medium allows intracellular accumulation of c‐di‐GMP and, thus, stimulation of biofilm formation by T2SEΩ. Three small proteins recently designated EbfG (enable biofilm formation with a GG secretion motif), previously shown to be important for biofilm development by T2SEΩ (Parnasa et al ., ), are enriched in the T2SEΩ exo‐proteome: EbfG1 and EbfG2 are more abundant in T2SEΩ than in the WT, and EbfG4 (Synpcc7942_1134) was not detected in the WT exo‐proteome at all (Fig. B).…”

Section: Resultsmentioning

confidence: 99%

Type 4 pili are dispensable for biofilm development in the cyanobacterium Synechococcus elongatus

Nagar

Zilberman

Sendersky

et al. 2017

Environmental Microbiology

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The hair-like cell appendages denoted as type IV pili are crucial for biofilm formation in diverse eubacteria. The protein complex responsible for type IV pilus assembly is homologous with the type II protein secretion complex. In the cyanobacterium Synechococcus elongatus PCC 7942, the gene Synpcc7942_2071 encodes an ATPase homologue of type II/type IV systems. Here, we report that inactivation of Synpcc7942_2071 strongly affected the suite of proteins present in the extracellular milieu (exo-proteome) and eliminated pili observable by electron microscopy. These results support a role for this gene product in protein secretion as well as in pili formation. As we previously reported, inactivation of Synpcc7942_2071 enables biofilm formation and suppresses the planktonic growth of S. elongatus. Thus, pili are dispensable for biofilm development in this cyanobacterium, in contrast to their biofilm-promoting function in type IV pili-producing heterotrophic bacteria. Nevertheless, pili removal is not required for biofilm formation as evident by a piliated mutant of S. elongatus that develops biofilms. We show that adhesion and timing of biofilm development differ between the piliated and non-piliated strains. The study demonstrates key differences in the process of biofilm formation between cyanobacteria and well-studied type IV pili-producing heterotrophic bacteria.

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Section: Resultsmentioning

confidence: 99%

Type 4 pili are dispensable for biofilm development in the cyanobacterium Synechococcus elongatus

Nagar

Zilberman

Sendersky

et al. 2017

Environmental Microbiology

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“…A particular group of small proteins are toxic due to their integration into the cell membrane as peptide component of a type I toxin-antitoxin system [69–71]. In the cyanobacterium Synechococcus elongatus , four small secreted proteins have been suggested to be involved in biofilm development [72]. Small proteins of the type II toxin-antitoxin category in Synechocystis 6803 have been catalogued separately [73] but the majority of them are somewhat larger than the here considered μ-proteins.…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2016

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BackgroundDespite their versatile functions in multimeric protein complexes, in the modification of enzymatic activities, intercellular communication or regulatory processes, proteins shorter than 80 amino acids (μ-proteins) are a systematically underestimated class of gene products in bacteria. Photosynthetic cyanobacteria provide a paradigm for small protein functions due to extensive work on the photosynthetic apparatus that led to the functional characterization of 19 small proteins of less than 50 amino acids. In analogy, previously unstudied small ORFs with similar degrees of conservation might encode small proteins of high relevance also in other functional contexts.ResultsHere we used comparative transcriptomic information available for two model cyanobacteria, Synechocystis sp. PCC 6803 and Synechocystis sp. PCC 6714 for the prediction of small ORFs. We found 293 transcriptional units containing candidate small ORFs ≤80 codons in Synechocystis sp. PCC 6803, also including the known mRNAs encoding small proteins of the photosynthetic apparatus. From these transcriptional units, 146 are shared between the two strains, 42 are shared with the higher plant Arabidopsis thaliana and 25 with E. coli. To verify the existence of the respective μ-proteins in vivo, we selected five genes as examples to which a FLAG tag sequence was added and re-introduced them into Synechocystis sp. PCC 6803. These were the previously annotated gene ssr1169, two newly defined genes norf1 and norf4, as well as nsiR6 (nitrogen stress-induced RNA 6) and hliR1(high light-inducible RNA 1) , which originally were considered non-coding. Upon activation of expression via the Cu2+.responsive petE promoter or from the native promoters, all five proteins were detected in Western blot experiments.ConclusionsThe distribution and conservation of these five genes as well as their regulation of expression and the physico-chemical properties of the encoded proteins underline the likely great bandwidth of small protein functions in bacteria and makes them attractive candidates for functional studies.

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“…Furthermore, a significant number of the genes differentially expressed encode for proteins of unknown functions (Imanaka et al, 2010). Compared with heterotrophic bacteria, there is little information about biofilm formation in cyanobacteria (Parnasa et al, 2016). However, recent studies have shown that Synechocystis and Synechococcus elongatus PCC 7942 also exhibit variations in gene expression pattern when grown on a solid surface or in liquid (Nakasugi and Neilan, 2005;Schatz et al, 2013;Agostoni et al, 2016).…”

Section: Is Stationary Phase Reached Because Of Metabolic/ Nutrient Lmentioning

confidence: 99%

A Novel Mechanism, Linked to Cell Density, Largely Controls Cell Division in Synechocystis

et al. 2017

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ORCID IDs: 0000-0001-7618-4748 (M.I.); 0000-0001-8931-7722 (T.O.); 0000-0002-6113-9570 (R.S.).Many studies have investigated the various genetic and environmental factors regulating cyanobacterial growth. Here, we investigated the growth and metabolism of Synechocystis sp. PCC 6803 under different nitrogen sources, light intensities, and CO 2 concentrations. Cells grown on urea showed the highest growth rates. However, for all conditions tested, the daily growth rates in batch cultures decreased steadily over time, and stationary phase was obtained with similar cell densities. Unexpectedly, metabolic and physiological analyses showed that growth rates during log phase were not controlled primarily by the availability of photoassimilates. Further physiological investigations indicated that nutrient limitation, quorum sensing, light quality, and light intensity (self-shading) were not the main factors responsible for the decrease in the growth rate and the onset of the stationary phase. Moreover, cell division rates in fed-batch cultures were positively correlated with the dilution rates. Hence, not only light, CO 2 , and nutrients can affect growth but also a cell-cell interaction. Accordingly, we propose that cell-cell interaction may be a factor responsible for the gradual decrease of growth rates in batch cultures during log phase, culminating with the onset of stationary phase.

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Small secreted proteins enable biofilm development in the cyanobacterium Synechococcus elongatus

Cited by 50 publications

References 51 publications

Type 4 pili are dispensable for biofilm development in the cyanobacterium Synechococcus elongatus

Type 4 pili are dispensable for biofilm development in the cyanobacterium Synechococcus elongatus

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

A Novel Mechanism, Linked to Cell Density, Largely Controls Cell Division in Synechocystis

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