A Deg-protease family protein in marine Synechococcus is involved in outer membrane protein organization

Rhona K Stuart,Bianca Brahamsha,Brian Palenik

doi:10.3389/fmars.2014.00016

Rhona K Stuart, Bianca Brahamsha + Show 1 more

Open Access

https://doi.org/10.3389/fmars.2014.00016

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Abstract

Deg-family proteases are a periplasm-associated group of proteins that are known to be involved in envelope stress responses and are found in most microorganisms. Orthologous genes SYNW2176 (in strain WH8102) and sync_2523 (strain CC9311) are predicted members of the Deg-protease family and are among the few genes induced by copper stress in both open ocean and coastal marine Synechococcus strains. In contrast to the lack of a phenotype in a similar knockout in Synechocystis PCC6803, a SYNW2176 knockout mutant in strain WH8102 was much more resistant to copper than the wild-type. The mutant also exhibited a significantly altered outer membrane protein composition which may contribute to copper resistance, longer lag phase after transfer, low-level consistent alkaline phosphatase activity, and an inability to induce high alkaline phosphatase activity in response to phosphate stress. This phenotype suggests a protein-quality-control role for SYNW2176, the absence of which leads to a constitutively activated stress response. Deg-protease family proteins in this ecologically important cyanobacterial group thus help to determine outer membrane responses to both nutrients and toxins.

Highlights

Marine picocyanobacteria including Synechococcus and its sister taxon Prochlorococcus are found throughout the world oceans and contribute significantly to primary production and carbon cycling (Li, 1994; Richardson and Jackson, 2007)
In our previous work we found a few similarities in the transcriptional response to elevated copper, including a shared osmoregulatory-like response (Stuart et al, 2009)
One gene that was up-regulated in both Synechococcus strains was a predicted serine protease (SYNW2176 in WH8102 and sync_2523 in CC9311), which is a member of the Deg-family of serine proteases

Summary

Introduction

Marine picocyanobacteria including Synechococcus and its sister taxon Prochlorococcus are found throughout the world oceans and contribute significantly to primary production and carbon cycling (Li, 1994; Richardson and Jackson, 2007). Strain CC9311 (CC9311), we found striking differences in sensitivity to copper and in the transcriptional response to elevated copper (Stuart et al, 2009). Despite the diversity in response within the group, marine Synechococcus species in general are quite sensitive to elevated copper levels, when compared to other phytoplankton groups (Brand et al, 1986). One gene that was up-regulated in both Synechococcus strains was a predicted serine protease (SYNW2176 in WH8102 and sync_2523 in CC9311), which is a member of the Deg-family of serine proteases. This family is characterized by a protease domain and one or more C-terminal PDZ domains. DegQ is perhaps the least well-characterized of the three in E. coli, but overexpression has been shown to partially rescue a DegP null phenotype and DegQ exhibits higher chaperone and lower protease activity in vitro than DegP, indicating overlapping functions for these two (Waller and Sauer, 1996; Bai et al, 2011)

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