Applications of Serine/Threonine Protein Kinases (STPK): A Bus for Dormancy Exit

  • Bhagwan Rekadwad


As the response to unfavorable growth conditions, bacteria transform into the dormant state with the concomitant formation of the specialized dormant forms/structure characterized by low metabolic activity and resistance to hostile conditions. Such dormant cells can be reactivated under the influence of several factors including proteins of such as muropeptides, Resuscitation promoting factor (Rpf) and STPKs family, which possess peptidoglycan hydrolase activity were considered to belong to the group of the autocrine growth factors of the bacteria. Remarkable interest toward Rpf-STPKs family is determined by its participation in resuscitation of the dormant forms of various bacteria and their genes, what in turn into its application in microbial processes and in biotechnology such as breaking bacterial/endospore dormancy, in host pathogen interaction, in depression of neurons, in cell shape control and cell division etc.


  1. Alber T (2009) Signaling mechanisms of the Mycobacterium tuberculosis receptor Ser/Thr protein kinases. Curr Opin Struct Biol 19:650–657. Scholar
  2. Arora G, Sajid A, Virmani R, Singhal A, Santosh Kumar CM, Dhasmana N, Khanna T, Maji A, Misra R, Molle V, Becher D, Gerth U, Mande SC, Singh Y (2017) Ser/Thr protein kinase PrkC-mediated regulation of GroEL is critical for biofilm formation in Bacillus anthracis. Biofilms Microbiomes 3:7. Scholar
  3. Bazire A, Dufour A (2014) The Pseudomonas aeruginosa rhlG and rhlAB genes are inversely regulated and RhlG is not required for rhamnolipid synthesis. BMC Microbiol 14:160. Scholar
  4. Beltramini AM, Mukhopadhyay CD, Pancholi V (2009) Modulation of cell wall structure and antimicrobial susceptibility by a Staphylococcus aureus eukaryote-like serine/threonine kinase and phosphatase. Infect Immun 77:1406–1416. Scholar
  5. Boone T, Driks A (2016) Protein synthesis during germination: shedding new light on a classical question. J Bacteriol 198:3251–3253. Scholar
  6. Boudreau MA, Fisher JF, Mobashery S (2012) Messenger functions of the bacterial cell wall-derived muropeptides. Biochemistry 51:2974–2990. Scholar
  7. Canova MJ, Molle V (2014) Bacterial serine/threonine protein kinases in host-pathogen interactions. J Biol Chem 289:9473–9479. Scholar
  8. Cousin C, Derouiche A, Shi L, Pagot Y, Poncet S, Mijakovic I (2013) Protein-serine/threonine/tyrosine kinases in bacterial signalling and regulation. FEMS Microbiol Lett 346:11–19. Scholar
  9. Donato V, Ayala FR, Cogliati S, Bauman C, Costa GB, Leñini C, Grau R (2017) Bacillus subtilis biofilm extends Caenorhabditis elegans longevity through down regulation of the insulin-like signalling pathway. Nat Comm 8:14332. Scholar
  10. Donovan C, Bramkamp M (2014) Cell division in Corynebacterineae. Front Microbiol 5:132. Scholar
  11. Dworkin J, Shah IM (2010) Exit from dormancy in microbial organisms. Nat Rev Microbiol 8:890–896. Scholar
  12. Echenique J, Kadioglu A, Romao S, Andrew PW, Trombe MC (2004) Protein serine/threonine kinase StkP positively controls virulence and competence in Streptococcus pneumoniae. Infect Immun 72:2434–2437. Scholar
  13. Errington J (2017) Cell wall-deficient, L-form bacteria in the 21st century: a personal perspective. Biochem Soc Trans 45:287–295. Scholar
  14. Fatima Q, Zahin M, Khan MSA, Ahemad I (2010) Modulation of quorum sensing controlled behaviour of bacteria by growing seedling, seed and seedling extracts of leguminous plants. Indian J Microbiol 50:238–242. Scholar
  15. Fischer GJ, Bacon W, Yang J, Palmer JM, Dagenais T, Hammock BD, Keller NP (2017) Lipoxygenase activity accelerates programmed spore germination in Aspergillus fumigates. Front Microbiol 8:831. Scholar
  16. Fiuza M, Canova MJ, Zanella-Cle’on I, Becchi M, Cozzone J, Mateos LM, Kremer L, Gil JA, Molle V (2008) From the characterization of the four serine/threonine protein kinases (PknA/B/G/L) of Corynebacterium glutamicum toward the role of PknA and PknB in cell division. J Biol Chem 283:18099–18112. Scholar
  17. Goldová J, Ulrych A, Hercík K, Branny P (2011) A eukaryotic-type signalling system of Pseudomonas aeruginosa contributes to oxidative stress resistance, intracellular survival and virulence. BMC Genomics 12:437. Scholar
  18. Grandchamp GM, Caro L, Shank EA (2017) Pirated siderophores promote sporulation in Bacillus subtilis. Appl Environ Microbiol 83:e03293–e03216. Scholar
  19. Greenstein AE, Grundner C, Echols N, Gay LM, Lombana TN, Miecskowski CA, Pullen KE, Sung PY, Alber T (2005) Structure/function studies of Ser/Thr and Tyr protein phosphorylation in Mycobacterium tuberculosis. J Mol Microbiol Biotechnol 9:167–181. Scholar
  20. Hussain H, Branny P, Allan E (2006) A eukaryotic-type serine/threonine protein kinase is required for biofilm formation, genetic competence, and acid resistance in Streptococcus mutans. J Bacteriol 188:1628–1632. Scholar
  21. Kalia VC (2014) Microbes, antimicrobials and resistance: the battle goes on. Indian J Microbiol 54:1–2. Scholar
  22. Kalia VC (2015) Microbes: the most friendly beings? In: Kalia VC (ed) Quorum sensing vs quorum quenching: a battle with no end in sight. Springer, India, pp 1–5. Scholar
  23. Kalia VC, Kumar P (2015) Genome wide search for biomarkers to diagnose Yersinia infections. Indian J Microbiol 55:366. Scholar
  24. Kalia VC, Kumar P, Pandian STK, Sharma P (2015) Biofouling control by quorum quenching. Hb_25. In: Kim SK (ed) Springer handbook of marine biotechnology, vol 15. Springer, Berlin/Heidelberg, pp 431–440Google Scholar
  25. Kalia VC, Prakash J, Koul S, Ray S (2017) Simple and rapid method for detecting biofilm forming bacteria. Indian J Microbiol 57:109–111. Scholar
  26. Kaur G, Rajesh S, Princy SA (2015) Plausible drug targets in the Streptococcus mutans quorum sensing pathways to combat dental biofilms and associated risks. Indian J Microbiol 55:349. Scholar
  27. Kobir A, Shi L, Boskovic A, Grangeasse C, Franjevic D, Mijakovic I (2011) Protein phosphorylation in bacterial signal transduction. Biochim Biophys Acta 18:989–994. Scholar
  28. Korza G, Setlow B, Rao L, Li Q, Setlow P (2016) Changes in Bacillus spore small molecules, rRNA, germination, and outgrowth after extended sublethal exposure to various temperatures: evidence that protein synthesis is not essential for spore germination. J Bacteriol 198:3254–3264. Scholar
  29. Koul S, Prakash J, Mishra A, Kalia VC (2016) Potential emergence of multi-quorum sensing inhibitor resistant (MQSIR) bacteria. Indian J Microbiol 56:1–18. Scholar
  30. Koul S, Kalia VC (2017) Multiplicity of quorum quenching enzymes: a potential mechanism to limit quorum sensing bacterial population. Indian J Microbiol 57:100–108.
  31. Kristich CJ, Wells CL, Dunny GM (2007) A eukaryotic-type Ser/Thr kinase in Enterococcus faecalis mediates antimicrobial resistance and intestinal persistence. Proc Natl Acad Sci U S A 104:3508–3513. Scholar
  32. Kysela DT, Randich AM, Caccamo PD, Brun YV (2016) Diversity takes shape: understanding the mechanistic and adaptive basis of bacterial morphology. PLoS Biol 14:e1002565. Scholar
  33. Makhnovskii DA, Tretyakova MS, Murzina GB, Pivovarov AS (2011) Endocytosis of cholinoreceptors in the mechanism of depression of the cholinosensitivity of common snail neurons in a cellular model of habituation. Neurosci Behav Physiol 41:617.
  34. Makhnovskii DA, Murzina GB, Tretyakova MS, Pivovarov AS (2013) The role of serine/threonine and tyrosine protein kinases in depression of the cholinosensitivity of neurons in the common snail in a cellular analog of habituation. Neurosci Behav Physiol 43:22. Scholar
  35. Margolin W (2009) Sculpting the bacterial cell. Curr Biol 19:R812–R822. Scholar
  36. McKenney PT, Driks A, Eichenberger P (2013) The Bacillus subtilis endospore: assembly and functions of the multilayered coat. Nat Rev Microbiol 11:33–44. Scholar
  37. Molle V, Kremer L (2010) Division and cell envelope regulation by Ser/Thr phosphorylation: Mycobacterium shows the way. Mol Microbiol 75:1064–1077. Scholar
  38. Monteiro JM, Fernandes PB, Vaz F, Pereira A, Tavares AC, Ferreira MT, Pereira PM, Veiga H, Kuru E, VanNieuwenhze MS, Brun YV, Filipe SR, Pinhoa MG (2015) Cell shape dynamics during the staphylococcal cell cycle. Nat Commun 6:8055. Scholar
  39. Nikitushkin VD, Demina GR, Kaprelyants AS (2016) Rpf Proteins are the factors of reactivation of the dormant forms of actinobacteria. Biochemist 81:1719–1734. Scholar
  40. Pivovarov AS, Murzina GB, Tret’yakova MS, Makhnovskii DA (2014a) The role of serine/threonine and tyrosine protein phosphatases in common snail command neurons in a cellular analog of habituation. Neurosci Behav Physiol 44:640. Scholar
  41. Pivovarov AS, Murzina GB, Makhnovsky DA, Vasil’eva NA, Tret’yakova MS (2014b) The role of myosins in depression of neuron sensitivity to acetylcholine in a cellular analog of habituation in the common snail. Neurosci Behav Physiol 44:1039. Scholar
  42. Pompeo F, Foulquier E, Galinier A (2016) Impact of serine/threonine protein kinases on the regulation of sporulation in Bacillus subtilis. Front Microbiol 7:568. Scholar
  43. Pooja S, Pushpananthan M, Jayashree S, Gunasekaran P, Rajendhran J (2015) Identification of periplasmic a-amlyase from cow dung metagenome by product induced gene expression profiling (Pigex). Indian J Microbiol 55:57–65. Scholar
  44. Ray S, Kalia VC (2017) Biomedical applications of polyhydroxyalkanaotes. Indian J Microbiol 57:39–47. Scholar
  45. Rekadwad BN, Khobragade CN (2017a) Bacterial quorum sensing (QS) in rhizosphere (paddy soil): understanding soil signaling and N- recycling for increased crop production. In: Kalia VC (ed) Microbial applications vol.2 – biomedicine, agriculture and industry. Springer International Publishing, Switzerland., AG, Springer Nature, pp 119–131. Scholar
  46. Rekadwad BN, Khobragade CN (2017b) Microbial biofilm: role in crop productivity. In: KALIA VC (ed) Microbial applications vol.2 – biomedicine, agriculture and industry. Springer International Publishing, Switzerland., AG, Springer Nature, pp 107–118. Scholar
  47. Scott SR, Hasty J (2016) Quorum sensing communication modules for microbial consortia. ACS Synth Biol 5:969–977. Scholar
  48. Setlow P (2006) Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals. J Applied Microbiol 101:514–525. Scholar
  49. Setlow P (2008) Dormant spores receive an unexpected wake-up call. Cell 135:410–412. Scholar
  50. Shah IM, Laaberki MH, Popham DL, Dworkin J (2008) A eukaryotic-like Ser/Thr kinase signals bacteria to exit dormancy in response to peptidoglycan fragments. Cell 135:486–496. Scholar
  51. Shukla SK, Mangwani N, Rao TS, Das S (2014) Biofilm-mediated bioremediation of polycyclic aromatic hydrocarbons. In: Das S (ed) Microbial biodegradation and bioremediation. Elsevier, Oxford, pp 203–232. Scholar
  52. Siddiqui MF, Rzechowicz M, Harvey W, Zularisam AW, Anthony GF (2015) Quorum sensing based membrane biofouling control for water treatment: a review. J Water Proc Eng 30:112–122. Scholar
  53. Truong-Bolduc QC, Hooper DC (2010) Phosphorylation of MgrA and its effect on expression of the NorA and NorB efflux pumps of Staphylococcus aureus. J Bacteriol 192:2525–2534. Scholar
  54. Truong-Bolduc QC, Ding Y, Hooper DC (2008) Posttranslational modification influences the effects of MgrA on norA expression in Staphylococcus aureus. J Bacteriol 190:7375–7381. Scholar
  55. Ulrych A, Holečková N, Goldová J, Doubravová L, Benada O, Kofroňová O, Halada P, Branny P (2016) Characterization of pneumococcal Ser/Thr protein phosphatase phpP mutant and identification of a novel PhpP substrate, putative RNA binding protein Jag. BMC Microbiol 16:247. Scholar
  56. Vidal JE, Ludewick HP, Kunkel RM, Zähner D, Klugman KP (2011) The LuxS-dependent quorum-sensing system regulates early biofilm formation by Streptococcus pneumoniae strain D39. Infect Immun 79:4050–4060. Scholar
  57. Wehenkel A, Fernandez P, Bellinzoni M, Catherinot V, Barilone N, Labesse G, Jackson M, Alzari PM (2006) The structure of PknB in complex with mitoxantrone, an ATP-competitive inhibitor, suggests a mode of protein kinase regulation in mycobacteria. FEBS Lett 580:3018–3022. Scholar
  58. Wehenkel A, Bellinzoni M, Graña M, Duran R, Villarino A, Fernandez P, Andre-Leroux G, England P, Takiff H, Cerveñansky C, Cole ST, Alzari PM (2008) Mycobacterial Ser/Thr protein kinases and phosphatases: physiological roles and therapeutic potential. Biochim Biophys Acta 1784:193–202. Scholar
  59. Zhou X, Halladin DK, Theriot JA (2016) Fast mechanically driven daughter cell separation is widespread in actinobacteria. mBio 7:4e00952–4e00916. Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Bhagwan Rekadwad
    • 1
  1. 1.National Centre for Microbial Resource, National Centre for Cell SciencePuneIndia

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