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Antonie van Leeuwenhoek

, Volume 111, Issue 5, pp 753–760 | Cite as

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

  • Janani Ravi
  • Vivek Anantharaman
  • L. Aravind
  • Maria Laura Gennaro
Original Paper

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.

Keywords

Actinobacteria Evolution Genomic context/neighborhood Phage shock protein Phylogeny PspA 

Notes

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.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10482_2018_1053_MOESM1_ESM.xlsx (156 kb)
Supplementary material 1 (XLSX 156 kb)

References

  1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aravind L, Anantharaman V, Balaji S, Babu MM, Iyer LM (2005) The many faces of the helix-turn-helix domain: transcription regulation and beyond. FEMS Microbiol Rev 29:231–262CrossRefPubMedGoogle Scholar
  3. Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2013) GenBank. Nucleic Acids Res 41:D36–D42CrossRefPubMedGoogle Scholar
  4. Brissette JL, Russel M, Weiner L, Model P (1990) Phage shock protein, a stress protein of Escherichia coli. Proc Natl Acad Sci USA 87:862–866CrossRefPubMedPubMedCentralGoogle Scholar
  5. Cole C, Barber JD, Barton GJ (2008) The Jpred 3 secondary structure prediction server. Nucleic Acids Res 36:W197–W201CrossRefPubMedPubMedCentralGoogle Scholar
  6. Darwin AJ (2005) The phage-shock-protein response. Mol Microbiol 57:621–628CrossRefPubMedGoogle Scholar
  7. Datta P, Ravi J, Guerrini V, Chauhan R, Neiditch MB, Shell SS, Fortune SM, Hancioglu B, Igoshin OA, Gennaro ML (2015) The Psp system of Mycobacterium tuberculosis integrates envelope stress-sensing and envelope-preserving functions. Mol Microbiol 97:408–422CrossRefPubMedPubMedCentralGoogle Scholar
  8. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797CrossRefPubMedPubMedCentralGoogle Scholar
  9. Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:W29–W37CrossRefPubMedPubMedCentralGoogle Scholar
  10. Flores-Kim J, Darwin AJ (2015) Activity of a bacterial cell envelope stress response is controlled by the interaction of a protein binding domain with different partners. J Biol Chem 290:11417–11430CrossRefPubMedPubMedCentralGoogle Scholar
  11. Flores-Kim J, Darwin AJ (2016) The phage shock protein response. Annu Rev Microbiol.  https://doi.org/10.1146/annurev-micro-102215-095359 PubMedGoogle Scholar
  12. Hutchings MI, Hoskisson PA, Chandra G, Buttner MJ (2004) Sensing and responding to diverse extracellular signals? Analysis of the sensor kinases and response regulators of Streptomyces coelicolor A3(2). Microbiology 150:2795–2806CrossRefPubMedGoogle Scholar
  13. Huvet M, Toni T, Sheng X, Thorne T, Jovanovic G, Engl C, Buck M, Pinney JW, Stumpf MP (2011) The evolution of the phage shock protein response system: interplay between protein function, genomic organization, and system function. Mol Biol Evol 28:1141–1155CrossRefPubMedGoogle Scholar
  14. Huynen M, Snel B, Lathe W, Bork P (2000) Predicting protein function by genomic context: quantitative evaluation and qualitative inferences. Genome Res 10:1204–1210CrossRefPubMedPubMedCentralGoogle Scholar
  15. Joly N, Engl C, Jovanovic G, Huvet M, Toni T, Sheng X, Stumpf MP, Buck M (2010) Managing membrane stress: the phage shock protein (Psp) response, from molecular mechanisms to physiology. FEMS Microbiol Rev 34:797–827CrossRefPubMedGoogle Scholar
  16. Kall L, Krogh A, Sonnhammer EL (2004) A combined transmembrane topology and signal peptide prediction method. J Mol Biol 338:1027–1036CrossRefPubMedGoogle Scholar
  17. Kleine B, Chattopadhyay A, Polen T, Pinto D, Mascher T, Bott M, Brocker M, Freudl R (2017) The three-component system EsrISR regulates a cell envelope stress response in Corynebacterium glutamicum. Mol Microbiol 106(5):719–741CrossRefPubMedGoogle Scholar
  18. Koonin EV, Wolf YI (2008) Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Res 36:6688–6719CrossRefPubMedPubMedCentralGoogle Scholar
  19. Korbel JO, Jensen LJ, von Mering C, Bork P (2004) Analysis of genomic context: prediction of functional associations from conserved bidirectionally transcribed gene pairs. Nat Biotechnol 22:911–917CrossRefPubMedGoogle Scholar
  20. Lassmann T, Frings O, Sonnhammer EL (2009) Kalign2: high-performance multiple alignment of protein and nucleotide sequences allowing external features. Nucleic Acids Res 37:858–865CrossRefPubMedGoogle Scholar
  21. Manganelli R, Gennaro ML (2016) Protecting from envelope stress: variations on the phage-shock-protein theme. Trends Microbiol.  https://doi.org/10.1016/j.tim.2016.11.010 PubMedCentralGoogle Scholar
  22. Mascher T, Zimmer SL, Smith TA, Helmann JD (2004) Antibiotic-inducible promoter regulated by the cell envelope stress-sensing two-component system LiaRS of Bacillus subtilis. Antimicrob Agents Chemother 48:2888–2896CrossRefPubMedPubMedCentralGoogle Scholar
  23. Mistry J, Finn R (2007) Pfam: a domain-centric method for analyzing proteins and proteomes. Methods Mol Biol 396:43–58CrossRefPubMedGoogle Scholar
  24. Nielsen H (2017) Predicting secretory proteins with SignalP. Methods Mol Biol 1611:59–73CrossRefPubMedGoogle Scholar
  25. Overmars L, Kerkhoven R, Siezen RJ, Francke C (2013) MGcV: the microbial genomic context viewer for comparative genome analysis. BMC Genom 14:209CrossRefGoogle Scholar
  26. Price MN, Dehal PS, Arkin AP (2010) FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490CrossRefPubMedPubMedCentralGoogle Scholar
  27. Rogozin IB, Makarova KS, Wolf YI, Koonin EV (2004) Computational approaches for the analysis of gene neighbourhoods in prokaryotic genomes. Brief Bioinform 5:131–149CrossRefPubMedGoogle Scholar
  28. Soding J, Biegert A, Lupas AN (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33:W244–W248CrossRefPubMedPubMedCentralGoogle Scholar
  29. Sonnhammer EL, Eddy SR, Durbin R (1997) Pfam: a comprehensive database of protein domain families based on seed alignments. Proteins 28:405–420CrossRefPubMedGoogle Scholar
  30. Sonnhammer EL, Eddy SR, Birney E, Bateman A, Durbin R (1998) Pfam: multiple sequence alignments and HMM-profiles of protein domains. Nucleic Acids Res 26:320–322CrossRefPubMedPubMedCentralGoogle Scholar
  31. Vothknecht UC, Otters S, Hennig R, Schneider D (2012) Vipp1: a very important protein in plastids?! J Exp Bot 63:1699–1712CrossRefPubMedGoogle Scholar
  32. Vrancken K, van Mellaert L, Anne J (2008) Characterization of the Streptomyces lividans PspA response. J Bacteriol 190:3475–3481CrossRefPubMedPubMedCentralGoogle Scholar
  33. Wattam AR, Abraham D, Dalay O, Disz TL, Driscoll T, Gabbard JL, Gillespie JJ, Gough R, Hix D, Kenyon R, Machi D, Mao C, Nordberg EK, Olson R, Overbeek R, Pusch GD, Shukla M, Schulman J, Stevens RL, Sullivan DE, Vonstein V, Warren A, Will R, Wilson MJ, Yoo HS, Zhang C, Zhang Y, Sobral BW (2014) PATRIC, the bacterial bioinformatics database and analysis resource. Nucleic Acids Res 42:D581–D591CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Public Health Research Institute, New Jersey Medical School, RutgersThe State University of New JerseyNewarkUSA
  2. 2.National Center for Biotechnology Information, National Library of Medicine, National Institutes of HealthBethesdaUSA

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