Genomic and genetic analyses have demonstrated that many species contain multiple chemotaxis-like signal transduction cascades that likely control processes other than chemotaxis. The Che3 signal transduction cascade from Rhodospirillum centenum is one such example that regulates development of dormant cysts. This Che-like cascade contains two hybrid response regulator-histidine kinases, CheA3 and CheS3, and a single-domain response regulator CheY3. We demonstrate that cheS3 is epistatic to cheA3 and that only CheS3∼P can phosphorylate CheY3. We further show that CheA3 derepresses cyst formation by phosphorylating a CheS3 receiver domain. These results demonstrate that the flow of phosphate as defined by the paradigm E. coli chemotaxis cascade does not necessarily hold true for non-chemotactic Che-like signal transduction cascades.
Vyšlo v časopise: Phosphate Flow between Hybrid Histidine Kinases CheA and CheS Controls Cyst Formation. PLoS Genet 9(12): e32767. doi:10.1371/journal.pgen.1004002 Kategorie: Research Article prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004002
1. SteenhoudtO, VanderleydenJ (2000) Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. Fems Microbiol Rev 24 : 487–506.
2. DoddIC, Ruiz-LozanoJM (2012) Microbial enhancement of crop resource use efficiency. Curr Opin Biotechnol 23 : 236–242 doi:10.1016/j.copbio.2011.09.005
3. OkonY, ItzigsohnR (1995) The development of Azospirillum as a commercial inoculant for improving crop yields. Biotechnol Adv 13 : 415–424 doi: http://dx.doi.org/10.1016/0734-9750(95)02004-M
4. SadasivanL, NeyraCA (1985) Flocculation in Azospirillum brasilense and Azospirillum lipoferum: exopolysaccharides and cyst formation. J Bacteriol 163 : 716–723.
5. BerlemanJE, BauerCE (2004) Characterization of cyst cell formation in the purple photosynthetic bacterium Rhodospirillum centenum. Microbiology (Reading, Engl) 150 : 383–390.
6. StadtwalddemchickR, StadtwalddemchickR, TurnerFR, TurnerFR, GestH, et al. (1990) Physiological properties of the thermotolerant photosynthetic bacterium, Rhodospirillum centenum. Fems Microbiol Lett 67 : 139–143.
7. WillettJW, KirbyJR (2011) CrdS and CrdA comprise a two-component system that is cooperatively regulated by the Che3 chemosensory system in Myxococcus xanthus. MBio 2: e00110–11–e00110–11 doi:10.1128/mBio.00110-11
8. BerlemanJE, BauerCE (2005) Involvement of a Che-like signal transduction cascade in regulating cyst cell development in Rhodospirillum centenum. Molecular Microbiology 56 : 1457–1466 doi:10.1111/j.1365-2958.2005.04646.x
9. RagatzL, JiangZY, JiangZY, BauerCE, BauerCE, et al. (1995) Macroscopic phototactic behavior of the purple photosynthetic bacterium Rhodospirillum centenum. Arch Microbiol 163 : 1–6.
10. BerlemanJE, BauerCE (2004) Characterization of cyst cell formation in the purple photosynthetic bacterium Rhodospirillum centenum. Microbiology (Reading, Engl) 150 : 383–390.
11. FavingerJ, StadtwaldR, GestH (1989) Rhodospirillum centenum, sp. nov., a thermotolerant cyst-forming anoxygenic photosynthetic bacterium. Antonie Van Leeuwenhoek 55 : 291–296.
12. DuttaR, InouyeM (1996) Reverse phosphotransfer from OmpR to EnvZ in a kinase−/phosphatase+ mutant of EnvZ (EnvZ.N347D), a bifunctional signal transducer of Escherichia coli. J Biol Chem 271 : 1424–1429 Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=8576133&retmode=ref&cmd=prlinks.
13. GeorgellisD, KwonO, De WulfP, LinE (1998) Signal decay through a reverse phosphorelay in the arc two-component signal transduction system. J Biol Chem 273 : 32864–32869 Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=9830034&retmode=ref&cmd=prlinks.
14. HessJF, OosawaK, KaplanN, SimonMI (1988) Phosphorylation of three proteins in the signaling pathway of bacterial chemotaxis. Cell 53 : 79–87.
15. LukatGS, StockAM, StockJB (1990) Divalent metal ion binding to the CheY protein and its significance to phosphotransfer in bacterial chemotaxis. Biochemistry-Us 29 : 5436–5442 Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=2201404&retmode=ref&cmd=prlinks.
16. WuichetK, CantwellBJ, ZhulinIB (2010) Evolution and phyletic distribution of two-component signal transduction systems. Curr Opin Microbiol 13 : 219–225 Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=20133179&retmode=ref&cmd=prlinks.
17. CapraEJ, PerchukBS, AshenbergO, SeidCA, SnowHR, et al. (2012) Spatial tethering of kinases to their substrates relaxes evolutionary constraints on specificity. Molecular Microbiology 86 : 1393–1403 doi:10.1111/mmi.12064
18. TownsendGE, RaghavanV, ZwirI, GroismanEA (2013) Intramolecular arrangement of sensor and regulator overcomes relaxed specificity in hybrid two-component systems. Proc Natl Acad Sci USA 110: E161–E169 doi:10.1073/pnas.1212102110
19. Wegener-FeldbrüggeS, Søgaard-AndersenL (2009) The atypical hybrid histidine protein kinase RodK in Myxococcus xanthus: spatial proximity supersedes kinetic preference in phosphotransfer reactions. J Bacteriol 191 : 1765–1776 Available: http://jb.asm.org/cgi/content/abstract/191/6/1765.
20. FujitakiJM, SmithRA (1984) Techniques in the detection and characterization of phosphoramidate-containing proteins. Meth Enzymol 107 : 23–36 Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=6438441&retmode=ref&cmd=prlinks.
21. KoshlandDE (1952) Effect of Catalysts on the Hydrolysis of Acetyl Phosphate. Nucleophilic Displacement Mechanisms in Enzymatic Reactions 74 : 2286–2292 Available: http://dx.doi.org/10.1021/ja01129a035.
22. FeherVA, ZapfJW, HochJA, DahlquistFW, WhiteleyJM, et al. (1995) 1H, 15N, and 13C backbone chemical shift assignments, secondary structure, and magnesium-binding characteristics of the Bacillus subtilis response regulator, Spo0F, determined by heteronuclear high-resolution NMR. Protein Sci 4 : 1801–1814 doi: 10.1002/pro.5560040915
23. GuilletV (2002) Crystallographic and Biochemical Studies of DivK Reveal Novel Features of an Essential Response Regulator in Caulobacter crescentus. J Biol Chem 277 : 42003–42010 doi: 10.1074/jbc.M204789200
24. NeedhamJV, ChenTY, FalkeJJ (1993) Novel ion specificity of a carboxylate cluster Mg(II) binding site: strong charge selectivity and weak size selectivity. Biochemistry-Us 32 : 3363–3367 Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=8461299&retmode=ref&cmd=prlinks.
25. SourjikV, SchmittR (1998) Phosphotransfer between CheA, CheY1, and CheY2 in the chemotaxis signal transduction chain of Rhizobium meliloti. Biochemistry-Us 37 : 2327–2335 Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=9485379&retmode=ref&cmd=prlinks.
26. LukatGS, LEEBH, MOTTONENJM, StockAM, StockJB (1991) Roles of the Highly Conserved Aspartate and Lysine Residues in the Response. Regulator of Bacterial Chemotaxis 266 : 8348–8354 Available: http://eutils.ncbi.nlm.nih.gov/ entrez/eutils/elink.fcgi?dbfrom=pubmed&id=1902474&retmode=ref&cmd=prlinks.
27. Jiménez-PearsonM-A, DelanyI, ScarlatoV, BeierD (2005) Phosphate flow in the chemotactic response system of Helicobacter pylori. Microbiology (Reading, Engl) 151 : 3299–3311 doi:10.1099/mic.0.28217-0
28. WuichetK, ZhulinIB (2010) Origins and diversification of a complex signal transduction system in prokaryotes. Sci Signal 3: ra50 doi:10.1126/scisignal.2000724
29. BerlemanJE, BauerCE (2005) Involvement of a Che-like signal transduction cascade in regulating cyst cell development in Rhodospirillum centenum. Molecular Microbiology 56 : 1457–1466 doi: 10.1111/j.1365-2958.2005.04646.x
30. KirbyJR, ZusmanDR (2003) Chemosensory regulation of developmental gene expression in Myxococcus xanthus. Proc Natl Acad Sci USA 100 : 2008–2013 doi: 10.1073/pnas.0330944100
31. HickmanJW, TifreaDF, HarwoodCS (2005) A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci USA 102 : 14422–14427 doi: 10.1073/pnas.0507170102
32. BlackWP, SchubotFD, LiZ, YangZ (2010) Phosphorylation and dephosphorylation among Dif chemosensory proteins essential for exopolysaccharide regulation in Myxococcus xanthus. J Bacteriol 192 : 4267–4274 doi: 10.1128/JB.00403-10
33. BibleAN, StephensBB, OrtegaDR, XieZ, AlexandreG (2008) Function of a chemotaxis-like signal transduction pathway in modulating motility, cell clumping, and cell length in the alphaproteobacterium Azospirillum brasilense. J Bacteriol 190 : 6365–6375 doi:10.1128/JB.00734-08
34. BibleA, RussellMH, AlexandreG (2012) The Azospirillum brasilense Che1 chemotaxis pathway controls swimming velocity, which affects transient cell-to-cell clumping. J Bacteriol 194 : 3343–3355 doi:10.1128/JB.00310-12
35. BerlemanJE, BauerCE (2005) A che-like signal transduction cascade involved in controlling flagella biosynthesis in Rhodospirillum centenum. Molecular Microbiology 55 : 1390–1402 doi: 10.1111/j.1365-2958.2005.04489.x
36. RasmussenAA, Wegener-FeldbrüggeS, PorterSL, ArmitageJP, Søgaard-AndersenL (2006) Four signalling domains in the hybrid histidine protein kinase RodK of Myxococcus xanthus are required for activity. Molecular Microbiology 60 : 525–534 doi: 10.1111/j.1365-2958.2006.05118.x
37. RasmussenAA, PorterSL, ArmitageJP, Søgaard-AndersenL (2005) Coupling of multicellular morphogenesis and cellular differentiation by an unusual hybrid histidine protein kinase in Myxococcus xanthus. Molecular Microbiology 56 : 1358–1372 doi: 10.1111/j.1365-2958.2005.04629.x
38. HiggsPI, JagadeesanS, MannP, ZusmanDR (2008) EspA, an Orphan Hybrid Histidine Protein Kinase, Regulates the Timing of Expression of Key Developmental Proteins of Myxococcus xanthus. J Bacteriol 190 : 4416–4426 doi: 10.1128/JB.00265-08
39. KimuraY, NakanoH, TerasakaH, TakegawaK (2001) Myxococcus xanthus mokA encodes a histidine kinase-response regulator hybrid sensor required for development and osmotic tolerance. J Bacteriol 183 : 1140–1146 doi: 10.1128/JB.183.4.1140-1146.2001
40. DinN, ShoemakerCJ, AkinKL, FrederickC, BirdTH (2011) Two putative histidine kinases are required for cyst formation in Rhodospirillum centenum. Arch Microbiol 193 : 209–222 doi:10.1007/s00203-010-0664-7
41. TakedaS, FujisawaY, MatsubaraM, AibaH, MizunoT (2001) A novel feature of the multistep phosphorelay in Escherichia coli: a revised model of the RcsC→YojN→RcsB signalling pathway implicated in capsular synthesis and swarming behaviour. Molecular Microbiology 40 : 440–450 Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=11309126&retmode=ref&cmd=prlinks.
42. InclánYF, LaurentS, ZusmanDR (2008) The receiver domain of FrzE, a CheA-CheY fusion protein, regulates the CheA histidine kinase activity and downstream signalling to the A - and S-motility systems of Myxococcus xanthus. Molecular Microbiology 68 : 1328–1339 doi: 10.1111/j.1365-2958.2008.06238.x
43. WiseAA, FangF, LinY-H, HeF, LynnDG, et al. (2010) The receiver domain of hybrid histidine kinase VirA: an enhancing factor for vir gene expression in Agrobacterium tumefaciens. J Bacteriol 192 : 1534–1542 Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=20081031&retmode=ref&cmd=prlinks.
44. MardenJN, DongQ, RoychowdhuryS, BerlemanJE, BauerCE (2011) Cyclic GMP controls Rhodospirillum centenum cyst development. Molecular Microbiology 79 : 600–615 doi:10.1111/j.1365-2958.2010.07513.x
45. JiangZY, RushingBG, BaiY, GestH, BauerCE (1998) Isolation of Rhodospirillum centenum mutants defective in phototactic colony motility by transposon mutagenesis. J Bacteriol 180 : 1248–1255.
46. BerlemanJE, BauerCE (2004) Characterization of cyst cell formation in the purple photosynthetic bacterium Rhodospirillum centenum. Microbiology (Reading, Engl) 150 : 383–390.
47. SainiDK (2004) DevR-DevS is a bona fide two-component system of Mycobacterium tuberculosis that is hypoxia-responsive in the absence of the DNA-binding domain of DevR. Microbiology (Reading, Engl) 150 : 865–875 Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=15073296&retmode=ref&cmd=prlinks.
48. SchultzJ, MilpetzF, BorkP, PontingCP (1998) Colloquium Paper: SMART, a simple modular architecture research tool: Identification of signaling domains. Proc Natl Acad Sci USA 95 : 5857–5864 doi: 10.1073/pnas.95.11.5857
Zvýšte si kvalifikáciu online z pohodlia domova
Nemáte účet? Registrujte sa
Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
