The Evolution of an Osmotically Inducible dps in the Genus Streptomyces

Abstract

Dps proteins are found almost ubiquitously in bacterial genomes and there is now an appreciation of their multifaceted roles in various stress responses. Previous studies have shown that this family of proteins assemble into dodecamers and their quaternary structure is entirely critical to their function. Moreover, the numbers of dps genes per bacterial genome is variable; even amongst closely related species - however, for many genera this enigma is yet to be satisfactorily explained. We reconstruct the most probable evolutionary history of Dps in Streptomyces genomes. Typically, these bacteria encode for more than one Dps protein. We offer the explanation that variation in the number of dps per genome among closely related Streptomyces can be explained by gene duplication or lateral acquisition, and the former preceded a subsequent shift in expression patterns for one of the resultant paralogs. We show that the genome of S. coelicolor encodes for three Dps proteins including a tailless Dps. Our in vivo observations show that the tailless protein, unlike the other two Dps in S. coelicolor, does not readily oligomerise. Phylogenetic and bioinformatic analyses combined with expression studies indicate that in several Streptomyces species at least one Dps is significantly over-expressed during osmotic shock, but the identity of the ortholog varies. In silico analysis of dps promoter regions coupled with gene expression studies of duplicated dps genes shows that paralogous gene pairs are expressed differentially and this correlates with the presence of a sigB promoter. Lastly, we identify a rare novel clade of Dps and show that a representative of these proteins in S. coelicolor possesses a dodecameric quaternary structure of high stability.

Translational control plays an important role in the adaptive heat-shock response of Streptomyces coelicolor

“…Functional enrichment analysis of the 74 translationally-induced genes using DAVID software v 6.8 revealed three clusters with enrichment score (E.S.) >1.3 (equivalent to non-log scale of 0.005): ( 1 ) Cold-shock protein (CSP)/DNA binding domain (E.S. = 6.32); Universal stress protein A (E.S.…”

“…They are characterized by a complex mycelial life cycle and by their ability to produce a vast array of secondary metabolites, most notably antibiotics. Like unicellular free living organisms they have a versatile and robust metabolism which allows them to adapt to life in different environments and to quickly adjust to environmental fluctuations such as temperature or pH-changes, scarce nutrient or oxygen availability and exposure to antibiotics commonly occurring in the soil environment ( 1–4 ). Their ability to fine tune gene expression at multiple levels (transcriptional, post-transcriptional, translational, post-translational and protein decay) facilitates rapid changes to their proteome in response to extracellular or intracellular signals.…”

Developmental biology ofStreptomycesfrom the perspective of 100 actinobacterial genome sequences

“…DpsB (SCO5756) is represented in most streptomycetes and many other actinobacteria, but DpsA (SCO0596) is less universally present, and DpsC (SCO1050) is absent from most. An intriguing interplay between the Dps proteins of S. coelicolor , indicated by surprising differences in the nucleoid compaction phenotypes of various single and double mutants (Facey et al ., 2009 ), therefore does not seem to be generalisable among streptomycetes; and an extended analysis of the evolution of the three proteins (Facey et al ., 2013 ) does not clarify this interplay. Contributions to spore nucleoid partitioning and compaction are also made by the Smc protein and its partner proteins ScpA and ScpB (Dedrick et al ., 2009 ; Kois et al ., 2009 ), and by sIHF (SCO1480: Yang et al ., 2012 ; Swiercz et al ., 2013 ).…”

A sporulation‐specific, sigF‐dependent protein, SspA, affects septum positioning in Streptomyces coelicolor

“…Chromosome compaction in the spores relies on nucleoid-associated proteins, such as HupS ( Salerno et al , 2009 ) and the Dps proteins ( Facey et al. , 2009 ; 2013 ;, 2011 ,).…”