#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Functional Organization of a Multimodular Bacterial Chemosensory Apparatus


Myxococcus xanthus is a social bacterium that exhibits a complex life cycle including biofilm formation, microbial predation and the formation of multicellular fruiting bodies. Genomic analyses indicate that M. xanthus produces an unusual number of chemosensory proteins: eight chemosensory systems (CSS) and 21 chemoreceptors, 13 of which are orphans located outside operons. In this paper we used genetic, phylogenetic and cell biology techniques to analyze the organization of the chemoreceptors and their functions in the regulation of M. xanthus social behaviors. Results indicate the existence of one large and three small chemosensory modules that occupy different positions within cells. This organization is consistent with in vivo protein interaction assays. Our analyses revealed the presence of a complex network of regulators that might integrate different stimuli to modulate bacterial social behaviors. Such networks might be conserved in other bacterial species with a life cycle of similar complexity and whose genome carries multiple CSS encoding operons.


Vyšlo v časopise: Functional Organization of a Multimodular Bacterial Chemosensory Apparatus. PLoS Genet 10(3): e32767. doi:10.1371/journal.pgen.1004164
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004164

Souhrn

Myxococcus xanthus is a social bacterium that exhibits a complex life cycle including biofilm formation, microbial predation and the formation of multicellular fruiting bodies. Genomic analyses indicate that M. xanthus produces an unusual number of chemosensory proteins: eight chemosensory systems (CSS) and 21 chemoreceptors, 13 of which are orphans located outside operons. In this paper we used genetic, phylogenetic and cell biology techniques to analyze the organization of the chemoreceptors and their functions in the regulation of M. xanthus social behaviors. Results indicate the existence of one large and three small chemosensory modules that occupy different positions within cells. This organization is consistent with in vivo protein interaction assays. Our analyses revealed the presence of a complex network of regulators that might integrate different stimuli to modulate bacterial social behaviors. Such networks might be conserved in other bacterial species with a life cycle of similar complexity and whose genome carries multiple CSS encoding operons.


Zdroje

1. WuichetK, ZhulinIB (2010) Origins and diversification of a complex signal transduction system in prokaryotes. Sci Signal 3: ra50 doi:10.1126/scisignal.2000724

2. PorterSL, WadhamsGH, ArmitageJP (2011) Signal processing in complex chemotaxis pathways. Nat Rev Microbiol 9: 153–165 doi:10.1038/nrmicro2505

3. RobertsMAJ, PapachristodoulouA, ArmitageJP (2010) Adaptation and control circuits in bacterial chemotaxis. Biochem Soc Trans 38: 1265–1269 doi:10.1042/BST0381265

4. SourjikV, BergHC (2002) Binding of the Escherichia coli response regulator CheY to its target measured in vivo by fluorescence resonance energy transfer. Proc Natl Acad Sci USA 99: 12669–12674 doi:10.1073/pnas.192463199

5. KirbyJR (2009) Chemotaxis-Like Regulatory Systems: Unique Roles in Diverse Bacteria. Annual Review of Microbiology 63: 45–59 doi:10.1146/annurev.micro.091208.073221

6. 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

7. GüvenerZT, HarwoodCS (2007) Subcellular location characteristics of the Pseudomonas aeruginosa GGDEF protein, WspR, indicate that it produces cyclic-di-GMP in response to growth on surfaces. Mol Microbiol 66: 1459–1473 doi:10.1111/j.1365-2958.2007.06008.x

8. AmesP, StuddertCA, ReiserRH, ParkinsonJS (2002) Collaborative signaling by mixed chemoreceptor teams in Escherichia coli. Proc Natl Acad Sci USA 99: 7060–7065 doi:10.1073/pnas.092071899

9. SourjikV, BergHC (2004) Functional interactions between receptors in bacterial chemotaxis. Nature 428: 437–441 doi:10.1038/nature02406

10. ScottKA, PorterSL, BaggEAL, HamerR, HillJL, et al. (2010) Specificity of localization and phosphotransfer in the CheA proteins of Rhodobacter sphaeroides. Mol Microbiol 76: 318–330 doi:10.1111/j.1365-2958.2010.07095.x

11. WadhamsGH, WarrenAV, MartinAC, ArmitageJP (2003) Targeting of two signal transduction pathways to different regions of the bacterial cell. Mol Microbiol 50: 763–770.

12. AlexanderRP, ZhulinIB (2007) Evolutionary genomics reveals conserved structural determinants of signaling and adaptation in microbial chemoreceptors. Proc Natl Acad Sci USA 104: 2885–2890 doi:10.1073/pnas.0609359104

13. TranHT, KrushkalJ, AntommatteiFM, LovleyDR, WeisRM (2008) Comparative genomics of Geobacter chemotaxis genes reveals diverse signaling function. BMC Genomics 9: 471 doi:10.1186/1471-2164-9-471

14. Tindall MJ, Porter SL, Maini PK, Armitage JP (2010) Modeling chemotaxis reveals the role of reversed phosphotransfer and a bi-functional kinase-phosphatase. PLoS Comput Biol 6. Available: http://www.ncbi.nlm.nih.gov/pubmed/20808885. Accessed 31 January 2012.

15. GoldmanBS, NiermanWC, KaiserD, SlaterSC, DurkinAS, et al. (2006) Evolution of sensory complexity recorded in a myxobacterial genome. Proc Natl Acad Sci USA 103: 15200–15205 doi:10.1073/pnas.0607335103

16. ShiX, Wegener-FeldbrüggeS, HuntleyS, HamannN, HedderichR, et al. (2008) Bioinformatics and experimental analysis of proteins of two-component systems in Myxococcus xanthus. J Bacteriol 190: 613–624 doi:10.1128/JB.01502-07

17. BerlemanJE, ScottJ, ChumleyT, KirbyJR (2008) Predataxis behavior in Myxococcus xanthus. Proc Natl Acad Sci USA 105: 17127–17132 doi:10.1073/pnas.0804387105

18. KaiserD (2006) A microbial genetic journey. Annu Rev Microbiol 60: 1–25 doi:10.1146/annurev.micro.60.080805.142209

19. KaiserD (2003) Coupling cell movement to multicellular development in myxobacteria. Nat Rev Microbiol 1: 45–54 doi:10.1038/nrmicro733

20. ShimketsLJ (1990) Social and developmental biology of the myxobacteria. Microbiol Rev 54: 473–501.

21. LiY, SunH, MaX, LuA, LuxR, et al. (2003) Extracellular polysaccharides mediate pilus retraction during social motility of Myxococcus xanthus. Proc Natl Acad Sci U S A 100: 5443–5448.

22. WallD, KaiserD (1999) Type IV pili and cell motility. Mol Microbiol 32: 1–10.

23. DucretA, ThéodolyO, MignotT (2013) Single cell microfluidic studies of bacterial motility. Methods Mol Biol 966: 97–107 doi:_10.1007/978-1-62703-245-2_6

24. LucianoJ, AgrebiR, Le GallAV, WartelM, FiegnaF, et al. (2011) Emergence and modular evolution of a novel motility machinery in bacteria. PLoS Genet 7: e1002268 doi:10.1371/journal.pgen.1002268

25. NanB, ChenJ, NeuJC, BerryRM, OsterG, et al. (2011) Myxobacteria gliding motility requires cytoskeleton rotation powered by proton motive force. Proc Natl Acad Sci USA 108: 2498–2503 doi:10.1073/pnas.1018556108

26. NanB, BandariaJN, MoghtaderiA, SunI-H, YildizA, et al. (2013) Flagella stator homologs function as motors for myxobacterial gliding motility by moving in helical trajectories. Proc Natl Acad Sci USA 110: E1508–E1513 doi:10.1073/pnas.1219982110

27. SunM, WartelM, CascalesE, ShaevitzJW, MignotT (2011) Motor-driven intracellular transport powers bacterial gliding motility. Proc Natl Acad Sci USA 108: 7559–7564 doi:10.1073/pnas.1101101108

28. BlackWP, XuQ, YangZ (2006) Type IV pili function upstream of the Dif chemotaxis pathway in Myxococcus xanthus EPS regulation. Mol Microbiol 61: 447–456 doi:10.1111/j.1365-2958.2006.05230.x

29. VlamakisHC, KirbyJR, ZusmanDR (2004) The Che4 pathway of Myxococcus xanthus regulates type IV pilus-mediated motility. Mol Microbiol 52: 1799–1811 doi:10.1111/j.1365-2958.2004.04098.x

30. McBrideMJ, WeinbergRA, ZusmanDR (1989) “Frizzy” aggregation genes of the gliding bacterium Myxococcus xanthus show sequence similarities to the chemotaxis genes of enteric bacteria. Proc Natl Acad Sci USA 86: 424–428.

31. ZusmanDR, ScottAE, YangZ, KirbyJR (2007) Chemosensory pathways, motility and development in Myxococcus xanthus. Nat Rev Microbiol 5: 862–872 doi:10.1038/nrmicro1770

32. Willett JW, Kirby JR (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. Available: http://www.ncbi.nlm.nih.gov/pubmed/21810965. Accessed 30 January 2012.

33. YangZ, GengY, XuD, KaplanHB, ShiW (1998) A new set of chemotaxis homologues is essential for Myxococcus xanthus social motility. Mol Microbiol 30: 1123–1130.

34. MuffTJ, FosterRM, LiuPJY, OrdalGW (2007) CheX in the three-phosphatase system of bacterial chemotaxis. J Bacteriol 189: 7007–7013 doi:10.1128/JB.00896-07

35. BerlemanJE, BauerCE (2005) Involvement of a Che-like signal transduction cascade in regulating cyst cell development in Rhodospirillum centenum. Mol Microbiol 56: 1457–1466 doi:10.1111/j.1365-2958.2005.04646.x

36. WhitchurchCB, LeechAJ, YoungMD, KennedyD, SargentJL, et al. (2004) Characterization of a complex chemosensory signal transduction system which controls twitching motility in Pseudomonas aeruginosa. Mol Microbiol 52: 873–893 doi:10.1111/j.1365-2958.2004.04026.x

37. BustamanteVH, Martinez-FloresI, VlamakisHC, ZusmanDR (2004) Analysis of the Frz signal transduction system of Myxococcus xanthus shows the importance of the conserved C-terminal region of the cytoplasmic chemoreceptor FrzCD in sensing signals. Mol Microbiol 53: 1501–1513.

38. YangZ, MaX, TongL, KaplanHB, ShimketsLJ, et al. (2000) Myxococcus xanthus dif genes are required for biogenesis of cell surface fibrils essential for social gliding motility. J Bacteriol 182: 5793–5798.

39. Del CampoAM, BalladoT, de la MoraJ, PoggioS, CamarenaL, et al. (2007) Chemotactic control of the two flagellar systems of Rhodobacter sphaeroides is mediated by different sets of CheY and FliM proteins. J Bacteriol 189: 8397–8401 doi:10.1128/JB.00730-07

40. YangY, SourjikV (2012) Opposite responses by different chemoreceptors set a tunable preference point in Escherichia coli pH taxis. Mol Microbiol 86: 1482–9 doi:10.1111/mmi.12070

41. VuA, WangX, ZhouH, DahlquistFW (2012) The receptor-CheW binding interface in bacterial chemotaxis. J Mol Biol 415: 759–767 doi:10.1016/j.jmb.2011.11.043

42. WangX, VuA, LeeK, DahlquistFW (2012) CheA-receptor interaction sites in bacterial chemotaxis. J Mol Biol 422: 282–290 doi:10.1016/j.jmb.2012.05.023

43. GüvenerZT, TifreaDF, HarwoodCS (2006) Two different Pseudomonas aeruginosa chemosensory signal transduction complexes localize to cell poles and form and remould in stationary phase. Mol Microbiol 61: 106–118 doi:10.1111/j.1365-2958.2006.05218.x

44. O'ConnorJR, KuwadaNJ, HuangyutithamV, WigginsPA, HarwoodCS (2012) Surface sensing and lateral subcellular localization of WspA, the receptor in a chemosensory-like system leading to c-di-GMP production. Mol Microbiol 86: 720–729 doi:10.1111/mmi.12013

45. MartinAC, WadhamsGH, ArmitageJP (2001) The roles of the multiple CheW and CheA homologues in chemotaxis and in chemoreceptor localization in Rhodobacter sphaeroides. Mol Microbiol 40: 1261–1272.

46. WadhamsGH, MartinAC, PorterSL, MaddockJR, MantottaJC, et al. (2002) TlpC, a novel chemotaxis protein in Rhodobacter sphaeroides, localizes to a discrete region in the cytoplasm. Mol Microbiol 46: 1211–1221.

47. HamblinPA, MaguireBA, GrishaninRN, ArmitageJP (1997) Evidence for two chemosensory pathways in Rhodobacter sphaeroides. Mol Microbiol 26: 1083–1096.

48. PorterSL, WarrenAV, MartinAC, ArmitageJP (2002) The third chemotaxis locus of Rhodobacter sphaeroides is essential for chemotaxis. Mol Microbiol 46: 1081–1094.

49. WadhamsGH, MartinAC, ArmitageJP (2000) Identification and localization of a methyl-accepting chemotaxis protein in Rhodobacter sphaeroides. Mol Microbiol 36: 1222–1233.

50. MaurielloEMF, AstlingDP, SliusarenkoO, ZusmanDR (2009) Localization of a bacterial cytoplasmic receptor is dynamic and changes with cell-cell contacts. Proc Natl Acad Sci USA 106: 4852–4857 doi:10.1073/pnas.0810583106

51. HazelbauerGL, EngströmP (1981) Multiple forms of methyl-accepting chemotaxis proteins distinguished by a factor in addition to multiple methylation. J Bacteriol 145: 35–42.

52. WangEA, MowryKL, CleggDO, KoshlandDEJr (1982) Tandem duplication and multiple functions of a receptor gene in bacterial chemotaxis. J Biol Chem 257: 4673–4676.

53. MaurielloEMF, NanB, ZusmanDR (2009) AglZ regulates adventurous (A-) motility in Myxococcus xanthus through its interaction with the cytoplasmic receptor, FrzCD. Mol Microbiol 72: 964–977 doi:10.1111/j.1365-2958.2009.06697.x

54. ThiemS, KentnerD, SourjikV (2007) Positioning of chemosensory clusters in E. coli and its relation to cell division. EMBO J 26: 1615–1623 doi:10.1038/sj.emboj.7601610

55. AdlerJ, ParmrydI (2010) Quantifying colocalization by correlation: The Pearson correlation coefficient is superior to the Mander's overlap coefficient. Cytometry Part A 77A: 733–742 doi:10.1002/cyto.a.20896

56. GalperinMY, HigdonR, KolkerE (2010) Interplay of heritage and habitat in the distribution of bacterial signal transduction systems. Mol Biosyst 6: 721–728 doi:10.1039/b908047c

57. ShimketsLJ (1999) Intercellular signaling during fruiting-body development of Myxococcus xanthus. Annu Rev Microbiol 53: 525–549.

58. XuQ, BlackWP, CadieuxCL, YangZ (2008) Independence and interdependence of Dif and Frz chemosensory pathways in Myxococcus xanthus chemotaxis. Mol Microbiol 69: 714–723 doi:10.1111/j.1365-2958.2008.06322.x

59. PuntaM, CoggillPC, EberhardtRY, MistryJ, TateJ, et al. (2012) The Pfam protein families database. Nucleic Acids Res 40: D290–301 doi:10.1093/nar/gkr1065

60. BendtsenJD, NielsenH, von HeijneG, BrunakS (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783–795 doi:10.1016/j.jmb.2004.05.028

61. KroghA, LarssonB, von HeijneG, SonnhammerEL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567–580 doi:10.1006/jmbi.2000.4315

62. AltschulSF, MaddenTL, SchäfferAA, ZhangJ, ZhangZ, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402.

63. LarkinMA, BlackshieldsG, BrownNP, ChennaR, McGettiganPA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948 doi:10.1093/bioinformatics/btm404

64. PhilippeH (1993) MUST, a computer package of Management Utilities for Sequences and Trees. Nucleic Acids Res 21: 5264–5272.

65. GuindonS, GascuelO (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696–704.

66. HuelsenbeckJP, RonquistF (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755.

67. KunerJM, KaiserD (1982) Fruiting body morphogenesis in submerged cultures of Myxococcus xanthus. J Bacteriol 151: 458–461.

68. BattestiA, BouveretE (2012) The bacterial two-hybrid system based on adenylate cyclase reconstitution in Escherichia coli. Methods 58: 325–334 doi:10.1016/j.ymeth.2012.07.018

69. MignotT, MerlieJP, ZusmanDR (2005) Regulated pole-to-pole oscillations of a bacterial gliding motility protein. Science 310: 855–857.

70. DucretA, MaisonneuveE, NotareschiP, GrossiA, MignotT, et al. (2009) A microscope automated fluidic system to study bacterial processes in real time. PLoS ONE 4: e7282 doi:10.1371/journal.pone.0007282

71. SchindelinJ, Arganda-CarrerasI, FriseE, KaynigV, LongairM, et al. (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9: 676–682 doi:10.1038/nmeth.2019

72. LiY, LuxR, PellingAE, GimzewskiJK, ShiW (2005) Analysis of type IV pilus and its associated motility in Myxococcus xanthus using an antibody reactive with native pilin and pili. Microbiology 151: 353–360.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2014 Číslo 3
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#