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Variations on a theme: evolution of the phage-shock-protein system in Actinobacteria

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Abstract

The phage shock protein (Psp) stress-response system protects bacteria from envelope stress through a cascade of interactions with other proteins and membrane lipids to stabilize the cell membrane. A key component of this multi-gene system is PspA, an effector protein that is found in diverse bacterial phyla, archaea, cyanobacteria, and chloroplasts. Other members of the Psp system include the cognate partners of PspA that are part of known operons: pspF||pspABC in Proteobacteria, liaIHGFSR in Firmicutes, and clgRpspAMN in Actinobacteria. Despite the functional significance of the Psp system, the conservation of PspA and other Psp functions, as well as the various genomic contexts of PspA, remain poorly characterized in Actinobacteria. Here we utilize a computational evolutionary approach to systematically identify the variations of the Psp system in ~450 completed actinobacterial genomes. We first determined the homologs of PspA and its cognate partners (as reported in Escherichia coli, Bacillus subtilis, and Mycobacterium tuberculosis) across Actinobacteria. This survey revealed that PspA and most of its functional partners are prevalent in Actinobacteria. We then found that PspA occurs in four predominant genomic contexts within Actinobacteria, the primary context being the clgRpspAM system previously identified in Mycobacteria. We also constructed a phylogenetic tree of PspA homologs (including paralogs) to trace the conservation and evolution of PspA across Actinobacteria. The genomic context revealed that PspA shows changes in its gene-neighborhood. The presence of multiple PspA contexts or of other known Psp members in genomic neighborhoods that do not carry pspA suggests yet undiscovered functional implications in envelope stress response mechanisms.

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Acknowledgements

This work was supported in part by a grant from the National Institutes of Health (R01AI104615) to MLG. We thank members of the Gennaro and Aravind laboratories for valuable discussions.

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Authors and Affiliations

  1. Public Health Research Institute, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark, NJ, 07103, USA

    Janani Ravi & Maria Laura Gennaro

  2. National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, 20892, USA

    Vivek Anantharaman & L. Aravind

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  1. Janani Ravi
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  2. Vivek Anantharaman
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  3. L. Aravind
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  4. Maria Laura Gennaro
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Correspondence to Maria Laura Gennaro.

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Ravi, J., Anantharaman, V., Aravind, L. et al. Variations on a theme: evolution of the phage-shock-protein system in Actinobacteria. Antonie van Leeuwenhoek 111, 753–760 (2018). https://doi.org/10.1007/s10482-018-1053-5

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