Spo0M: structure and function beyond regulation of sporulation

  • Luz Adriana Vega-Cabrera
  • Christopher D. Wood
  • Liliana Pardo-López
Review

Abstract

In this mini-review, we present a perspective on the recent findings relating Spo0M structure and function that will stimulate and guide further studies in the characterization of this interesting protein. Cell division and sporulation constitute two of the best studied processes in the model organism Bacillus subtilis; however, there are many missing pieces in the giant regulatory puzzle that governs the independent and shared networks between them. Spo0M is a little studied protein that has been related to both, cell division and sporulation, but its biochemical function and its direct interactions have not been yet defined. Structural analysis of Spo0M revealed the presence of an arrestin-like domain and an FP domain (a dimerization domain present in proteasome elements), motifs more commonly found in eukaryotic proteins. The aim of this perspective is to present open questions regarding the functional and structural features of Spo0M that make this protein a good candidate for the ancestor of arrestins in bacteria and an important element in developmental and differentiation processes of Bacillus subtilis.

Keywords

Spo0M Bacillus subtilis Sporulation Cell division Arrestins Stress response 

References

  1. Al-Hinai MA, Jones SW, Papoutsakis ET (2015) The Clostridium sporulation programs: diversity and preservation of endospore differentiation. Microbiol Mol Biol Rev 79:19–37. doi:10.1128/MMBR.00025-14 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aubry L, Klein G (2013) True arrestins and arrestin-fold proteins: a structure-based appraisal. In: Khalil RA (ed) Progress in molecular biology and translational science, vol 118. Elsevier Inc, London, UK, pp 21–56Google Scholar
  3. Battesti A, Gottesman S (2013) Roles of adaptor proteins in regulation of bacterial proteolysis. Curr Opin Microbiol 16:140–147. doi:10.1038/jid.2014.371 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Benson AK, Haldenwang WG (1993) Bacillus subtilis SigmaB is regulated by a binding protein (RsbW) that blocks its association with core RNA polymerase. Proc Natl Acad Sci USA 90:2330–2334CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bramkamp M, van Baarle S (2009) Division site selection in rod-shaped bacteria. Curr Opin Microbiol 12:683–688. doi:10.1016/j.mib.2009.10.002 CrossRefPubMedGoogle Scholar
  6. Claessen D, Emmins R, Hamoen LW et al (2008) Control of the cell elongation-division cycle by shuttling of PBP1 protein in Bacillus subtilis. Mol Microbiol 68:1029–1046. doi:10.1111/j.1365-2958.2008.06210.x CrossRefPubMedGoogle Scholar
  7. De Hoon MJL, Eichenberger P, Vitkup D (2010) Hierarchical evolution of the bacterial sporulation network. Curr Biol. doi:10.1016/j.cub.2010.06.031 PubMedPubMedCentralGoogle Scholar
  8. Derouiche A, Shi L, Kalantari A, Mijakovic I (2016) Evolution and tinkering: what do a protein kinase, a transcriptional regulator and chromosome segregation/cell division proteins have in common? Curr Genet 62:67–70. doi:10.1007/s00294-015-0513-y CrossRefPubMedGoogle Scholar
  9. Driks A, Eichenberger P (2016) The spore coat. Microbiol Spectr 4(2). doi:10.1128/microbiolspec.TBS-0023-2016
  10. Eswaramoorthy P, Erb ML, Gregory JA et al (2011) Cellular architecture mediates DivIVA ultrastructure and regulates min activity in Bacillus subtilis. MBio. doi:10.1128/mBio.00257-11 PubMedPubMedCentralGoogle Scholar
  11. Eswaramoorthy P, Winter PW, Wawrzusin P et al (2014) Asymmetric division and differential gene expression during a bacterial developmental program requires DivIVA. PLoS Genet. doi:10.1371/journal.pgen.1004526 PubMedPubMedCentralGoogle Scholar
  12. Gallon M, Clairfeuille T, Steinberg F et al (2014) A unique PDZ domain and arrestin-like fold interaction reveals mechanistic details of endocytic recycling by SNX27-retromer. Proc Natl Acad Sci USA 111:E3604–E3613. doi:10.1073/pnas.1410552111 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Grau RR, De Oña P, Kunert M et al (2015) A duo of potassium-responsive histidine kinases govern the multicellular destiny of Bacillus subtilis. MBio. doi:10.1128/mBio.00581-15 Google Scholar
  14. Gurevich VV, Gurevich EV (2013) Structural determinants of arrestin function. In: Khalil RA (ed) Progress in molecular biology and translational science, vol 118. Elsevier Inc, London, UK, pp 57–92Google Scholar
  15. Haeusser DP, Schwartz RL, Smith AM et al (2004) EzrA prevents aberrant cell division by modulating assembly of the cytoskeletal protein FtsZ. Mol Microbiol 52:801–814. doi:10.1111/j.1365-2958.2004.04016.x CrossRefPubMedGoogle Scholar
  16. Han W-D, Kawamoto S, Hosoya Y et al (1998) A novel sporulation-control gene (spo0M) of Bacillus subtilis with a σH-regulated promoter. Gene 217:31–40. doi:10.1016/S0378-1119(98)00378-3 CrossRefPubMedGoogle Scholar
  17. Hecker M, Pané-Farré J, Uwe V (2007) SigB-dependent general stress response in Bacillus subtilis and related gram-positive bacteria. Annu Rev Microbiol 61:215–236. doi:10.1146/annurev.micro.61.080706.093445 CrossRefPubMedGoogle Scholar
  18. Jastrab JB, Darwin KH (2016) Bacterial proteasomes. Annu Rev Microbiol 69:109–127. doi:10.1038/nbt.3121.ChIP-nexus CrossRefGoogle Scholar
  19. Jeleń F, Oleksy A, Śmietana K (2003) PDZ domains—common players in the cell signaling. Acta Biochim Pol 50(4):985–1017Google Scholar
  20. Kloosterman TG, Lenarcic R, Willis CR et al (2016) Complex polar machinery required for proper chromosome segregation in vegetative and sporulating cells of Bacillus subtilis. Mol Microbiol 101:333–350. doi:10.1111/mmi.13393 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Land AD, Luo Q, Levin PA (2014) Functional domain analysis of the cell division inhibitor EzrA. PLoS One 9:e102616. doi:10.1371/journal.pone.0102616 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Lee H-J, Zheng JJ (2010) PDZ domains and their binding partners: structure, specificity, and modification. Cell Commun Signal 8:8. doi:10.1186/1478-811X-8-8 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Lefkowitz RJ (2013) Arrestins come of age: a personal historical perspective. In: Khalil RA (ed) Progress in molecular biology and translational science, vol 118. Elsevier Inc, London, UK, pp 3–18Google Scholar
  24. Livneh I, Cohen-kaplan V, Cohen-rosenzweig C et al (2016) The life cycle of the 26S proteasome: from birth, through regulation and function, and onto its death. Cell Res 26:869–885. doi:10.1038/cr.2016.86 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Mastny M, Heuck A, Kurzbauer R et al (2013) XCtpB assembles a gated protease tunnel regulating cell–cell signaling during spore formation in Bacillus subtilis. Cell. doi:10.1016/j.cell.2013.09.050 PubMedPubMedCentralGoogle Scholar
  26. Meeske AJ, Rodrigues CDA, Brady J et al (2016) High-throughput genetic screens identify a large and diverse collection of new sporulation genes in Bacillus subtilis. PLoS Biol. doi:10.1371/journal.pbio.1002341 PubMedPubMedCentralGoogle Scholar
  27. Mielich-Süss B, Schneider J, Lopez D (2013) Overproduction of flotillin influences cell differentiation and shape in Bacillus subtilis. MBio 4:e00719-13. doi:10.1128/mBio.00719-13 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Msadek T, Dartois V, Kunst F et al (1998) ClpP of Bacillus subtilis is required for competence development, motility, degradative enzyme synthesis, growth at high temperature and sporulation. Mol Microbiol 27:899–914. doi:10.1046/j.1365-2958.1998.00735.x CrossRefPubMedGoogle Scholar
  29. Patwari P, Chutkow WA, Cummings K et al (2009) Thioredoxin-independent regulation of metabolism by the α-arrestin proteins. J Biol Chem 284:24996–25003. doi:10.1074/jbc.M109.018093 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Piggot PJ, Hilbert DW (2004) Sporulation of Bacillus subtilis. Curr Opin Microbiol 7:579–586. doi:10.1016/j.mib.2004.10.001 CrossRefPubMedGoogle Scholar
  31. Pompeo F, Foulquier E, Serrano B et al (2015) Phosphorylation of the cell division protein GpsB regulates PrkC kinase activity through a negative feedback loop in Bacillus subtilis. Mol Microbiol 97:1–12. doi:10.1111/mmi.13015 CrossRefGoogle Scholar
  32. Shang J, Wang G, Yang Y et al (2014) Structure of the FP domain of Fbxo7 reveals a novel mode of protein–protein interaction. Acta Crystallogr Sect D Biol Crystallogr 70:155–164. doi:10.1107/S1399004713025820 CrossRefGoogle Scholar
  33. Sonoda Y, Mizutani K, Mikami B (2015) Structure of Spo0M, a sporulation-control protein from Bacillus subtilis. Acta Crystallogr Sect F Struct Biol Commun 71:1488–1497. doi:10.1107/S2053230X15020919 CrossRefGoogle Scholar
  34. Strahl H, Hamoen LW (2012) Finding the corners in a cell. Curr Opin Microbiol 15:731–736. doi:10.1016/j.mib.2012.10.006 CrossRefPubMedGoogle Scholar
  35. Sugimoto S, Saruwatari K, Higashi C, Sonomoto K (2008) The proper ratio of GrpE to DnaK is important for protein quality control by the DnaK–DnaJ–GrpE chaperone system and for cell division. Microbiology 154:1876–1885. doi:10.1099/mic.0.2008/017376-0 CrossRefPubMedGoogle Scholar
  36. Thi Nguyen HB, Schumann W (2012) The sporulation control gene spo0M of Bacillus subtilis is a target of the FtsH metalloprotease. Res Microbiol 163:114–118. doi:10.1016/j.resmic.2011.10.011 CrossRefPubMedGoogle Scholar
  37. Touzain F, Petit M-A, Schbath S, El Karoui M (2011) DNA motifs that sculpt the bacterial chromosome. Nat Rev Microbiol 9:15–26. doi:10.1038/nrmicro2477 CrossRefPubMedGoogle Scholar
  38. Vega-Cabrera LA, Guerrero A, Rodríguez-Mejía JL et al (2017) Analysis of Spo0M function in Bacillus subtilis. PLoS One 12:e0172737. doi:10.1371/journal.pone.0172737 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Wünsche A, Hammer E, Bartholomae M et al (2012) CcpA forms complexes with CodY and RpoA in Bacillus subtilis. FEBS J 279:2201–2214. doi:10.1111/j.1742-4658.2012.08604.x CrossRefPubMedGoogle Scholar
  40. Xiao K, Sun J, Kim J et al (2010) Global phosphorylation analysis of beta-arrestin-mediated signaling downstream of a seven transmembrane receptor (7TMR). Proc Natl Acad Sci USA 107:15299–15304. doi:10.1073/pnas.1008461107 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Yepes A, Schneider J, Mielich B et al (2012) The biofilm formation defect of a Bacillus subtilis flotillin-defective mutant involves the protease FtsH. Mol Microbiol 86:457–471. doi:10.1111/j.1365-2958.2012.08205.x CrossRefPubMedPubMedCentralGoogle Scholar
  42. Zweers JC, Nicolas P, Wiegert T et al (2012) Definition of the σW regulon of Bacillus subtilis in the absence of stress. PLoS One. doi:10.1371/journal.pone.0048471 PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Instituto de BiotecnologíaUniversidad Nacional Autónoma de MéxicoCuernavacaMexico
  2. 2.Laboratorio Nacional de Microscopía AvanzadaUniversidad Nacional Autónoma de MéxicoCuernavacaMexico

Personalised recommendations