Type 4 pili are dispensable for biofilm development in the cyanobacterium <i>Synechococcus elongatus</i>

Nagar, Elad; Zilberman, Shaul; Sendersky, Eleonora; Simkovsky, Ryan; Shimoni, Eyal; Gershtein, Diana; Herzberg, Moshe; Golden, Susan S.; Schwarz, Rakefet

doi:10.1111/1462-2920.13814

Cited by 42 publications

(81 citation statements)

References 66 publications

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“…microcins, often precedes their secretion (Michiels et al, ; Bobeica et al, ) and, therefore, we examined whether the putative microcin‐processing peptidase encoded by Synpcc7942_1127 affects extracellular levels of these proteins. Exoproteome analysis revealed higher levels of each of the EbfG proteins in extracellular culture fluids of T2SEΩ compared with WT (Nagar et al, ). In contrast, inactivation of Synpcc7942_1127 in combination with T2SEΩ significantly reduced the extracellular levels of EbfG proteins (Fig.…”

Section: Resultsmentioning

confidence: 99%

A microcin processing peptidase‐like protein of the cyanobacterium Synechococcus elongatus is essential for secretion of biofilm‐promoting proteins

Parnasa

Sendersky

Simkovsky

et al. 2019

Environ Microbiol Rep

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Summary Small secreted compounds, e.g. microcins, are characterized by a double‐glycine (GG) secretion motif that is cleaved off upon maturation. Genomic analysis suggests that small proteins that possess a GG motif are widespread in cyanobacteria; however, the roles of these proteins are largely unknown. Using a biofilm‐proficient mutant of the cyanobacterium Synechococcus elongatus PCC 7942 in which the constitutive biofilm self‐suppression mechanism is inactivated, we previously demonstrated that four small proteins, Enable biofilm formation with a GG motif (EbfG1‐4), each with a GG motif, enable biofilm formation. Furthermore, a peptidase belonging to the C39 family, Peptidase transporter enabling Biofilm (PteB), is required for secretion of these proteins. Here, we show that the microcin processing peptidase‐like protein encoded by gene Synpcc7942_1127 is also required for biofilm development – inactivation of this gene in the biofilm‐proficient mutant abrogates biofilm development. Additionally, this peptidase‐like protein (denoted EbfE – enables biofilm formation peptidase) is required for secretion of the EbfG biofilm‐promoting small proteins. Given their protein‐domain characteristics, we suggest that PteB and EbfE take part in a maturation‐secretion system, with PteB being located to the cell membrane while EbfE is directed to the periplasmic space via its secretion signal.

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Section: Resultsmentioning

confidence: 99%

A microcin processing peptidase‐like protein of the cyanobacterium Synechococcus elongatus is essential for secretion of biofilm‐promoting proteins

Parnasa

Sendersky

Simkovsky

et al. 2019

Environ Microbiol Rep

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“…, our data preclude PilC-mediated secretion of released factors 295 analogous to biofilm enhancers and inhibitors secreted by S. elongatus[62][63][64].…”

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confidence: 77%

“…This mutation is proposed to block an unidentified 118molecule that inhibits secretion of biofilm enhancing proteins in WT S. elongatus [63]. 119 A subsequent study found certain piliated S. elongatus mutants also underwent a degree 120 of sedimentation, adhesion, and biofilm formation compared to WT, indicating that loss 121 of Type IV pili is not a prerequisite for biofilm formation in S. elongatus [64].…”

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confidence: 99%

“…Interestingly, 115 knockout of a putative pilC homolog pcc7942 2069 enhances biofilm-forming phenotype 116 to Synechococcus elongatus PCC 7942 [62] (hereafter S. elongatus), due to the role of 117 PilC in secreting small proteins that inhibit biofilm formation by WT strains [63]. A 118subsequent study found certain piliated S. elongatus mutants also underwent a degree of 119 sedimentation, adhesion, and biofilm formation compared to WT, so loss of pili is not a 120 prerequisite for biofilm formation in S. elongatus [64].…”

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confidence: 99%

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Axenic Biofilm Formation and Aggregation bySynechocystisPCC 6803 is Induced by Changes in Nutrient Concentration, and Requires Cell Surface Structures

Allen

Rittmann

Curtiss

2018

Preprint

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Phototrophic biofilms are key to nutrient cycling in natural environments and bioremediation technologies, but few studies describe biofilm formation by pure (axenic) cultures of a phototrophic microbe. The cyanobacterium Synechocystis sp. PCC 6803 (hereafter Synechocystis) is a model micro-organism for the study of oxygenic photosynthesis and biofuel production. We report here that wild-type (WT) Synechocystis caused extensive biofilm formation in a 2000 liter outdoor non-axenic photobioreactor under conditions attributed to nutrient limitation. We developed a biofilm assay and found that axenic Synechocystis forms biofilms of cells and extracellular material, but only when induced by an environmental signal, such as by reducing the concentration of growth medium BG11. Mutants lacking cell surface structures, namely type IV pili and the S-layer, do not form biofilms.To further characterize the molecular mechanisms of cell-cell binding by Synechocystis, we also developed a rapid (8 hour) axenic aggregation assay. Mutants lacking Type IV pili were unable to aggregate, but mutants lacking a homolog to Wza, a protein required for Type 1 exopolysaccharide export in Escherichia coli, had a super-binding phenotype. In WT cultures, 1.2x BG11 induced aggregation to the same degree as 0.8x BG11. Overall, our data support that Wza-dependant exopolysaccharide is essential to maintain stable, uniform suspensions of WT Synechocystis cells in unmodified growth medium, and this mechanism is counter-acted in a pili-dependent manner under altered BG11 concentrations. ImportanceMicrobes can exist as suspensions of individual cells in liquids, and also commonly form multicellular communities attached to surfaces. Surface-attached communities, called biofilms, can confer antibiotic resistance to pathogenic bacteria during infections, and establish food webs for global nutrient cycling in the environment. Phototrophic biofilm formation is one of the earliest phenotypes visible in the fossil record, dating back over 3 billion years. Despite the importance and ubiquity of phototrophic biofilms, most of what we know about the molecular mechanisms, genetic regulation, and October 22, 2018 1/33 (E. coli ). This includes Type I capsular polysaccharide, which requires proteins 45 including Wzx, Wzy, Wza, and Wzc for the later stages of EPS synthesis and export 46 [30]. Wza and Wzc proteins act as a gating mechanism / polymerase, and an outer 47 membrane porin of Type I capsule in E. coli, respectively [31]. In many heterotrophic 48 bacterial species, mutants lacking Wza do not synthesize capsule [32] and are also 49 impaired for biofilm formation [33-35]. The Synechocystis protein Sll1581 is a putative 50 homolog to Wza (28% identity, 42% similarity), consistent with its localization to the 51 outer membrane of Synechocystis [36]. In a previous study, Synechocystis mutants 52 lacking Sll1581 had EPS levels less than 25% that of wild-type (42). Compared to WT 53 cells, this mutant showed spontaneous auto-sedimentation without aggregation in ...

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“…The time course experiment has allowed us to assign the production of these proteins to nutrient-rich conditions with a peak of SynWH7803_1795 detection at day 7 (25.7%) and an average detection of 8.1% over the 100 days, whereas the detection was low (< 0.1%) in natural SW conditions. The remarkable ecological and physiological roles of the pili need further characterization although a recent study in Synechococcus elongatus suggests this structure may be involved in cell buoyancy (Nagar et al, 2017). Interestingly, both alkaline phosphatases were detected in the exoproteome of Synechococcus sp.…”

Section: Correlation Between Culture Growth and Exoproteomesmentioning

confidence: 99%

100 Days of marine Synechococcus–Ruegeria pomeroyi interaction: A detailed analysis of the exoproteome

Kaur

Hernández-Fernaud

Aguiló-Ferretjans

et al. 2017

Environmental Microbiology

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SummaryMarine phototroph and heterotroph interactions are vital in maintaining the nutrient balance in the oceans as essential nutrients need to be rapidly cycled before sinking to aphotic layers. The aim of this study was to highlight the molecular mechanisms that drive these interactions. For this, we generated a detailed exoproteomic time‐course analysis of a 100‐day co‐culture between the model marine picocyanobacterium Synechococcus sp. WH7803 and the Roseobacter strain Ruegeria pomeroyi DSS‐3, both in nutrient‐enriched and natural oligotrophic seawater. The proteomic data showed a transition between the initial growth phase and stable‐state phase that, in the case of the heterotroph, was caused by a switch in motility attributed to organic matter availability. The phototroph adapted to seawater oligotrophy by reducing its selective leakiness, increasing the acquisition of essential nutrients and secreting conserved proteins of unknown function. We also report a surprisingly high abundance of extracellular superoxide dismutase produced by Synechococcus and a dynamic secretion of potential hydrolytic enzyme candidates used by the heterotroph to cleave organic groups and hydrolase polymeric organic matter produced by the cyanobacterium. The time course dataset we present here will become a reference for understanding the molecular processes underpinning marine phototroph‐heterotroph interactions.

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

Cited by 42 publications

References 66 publications

A microcin processing peptidase‐like protein of the cyanobacterium Synechococcus elongatus is essential for secretion of biofilm‐promoting proteins

A microcin processing peptidase‐like protein of the cyanobacterium Synechococcus elongatus is essential for secretion of biofilm‐promoting proteins

Axenic Biofilm Formation and Aggregation bySynechocystisPCC 6803 is Induced by Changes in Nutrient Concentration, and Requires Cell Surface Structures

100 Days of marine Synechococcus–Ruegeria pomeroyi interaction: A detailed analysis of the exoproteome

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