#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Ras GTPase-Like Protein MglA, a Controller of Bacterial Social-Motility in Myxobacteria, Has Evolved to Control Bacterial Predation by


Bacterial cell polarity control is important for maintaining asymmetry of polar components such as flagella and pili. Bdellovibrio bacteriovorus is a predatory deltaproteobacterium which attaches to, and invades, other bacteria using Type IV pili (T4P) extruded from the specialised, invasive, non-flagellar pole of the cell. It was not known how that invasive pole is specified and regulated. Here we discover that a regulatory protein-hub, including Ras-GTPase-like protein MglA and cyclic-di-GMP receptor-protein CdgA, control prey-invasion. In the deltaproteobacterium, Myxococcus xanthus, MglA, with MglB and RomR, was found by others to regulate switching of T4P in social ‘swarming’ surface motility by swapping the pole at which T4P are found. In contrast, in B. bacteriovorus MglA regulates the process of prey-invasion and RomR, which is required for surface motility regulation in Myxococcus, is essential for growth and viability in Bdellovibrio. During evolution, B. bacteriovorus has lost mglB, possibly as T4P-pole-switching is not required; pili are only required at the invasive pole. A previously unidentified tetratricopeptide repeat (TPR) protein interacts with MglA and is essential for prey-invasion. This regulatory protein hub allows prey-invasion, likely integrating cyclic-di-GMP signals, pilus assembly and TamAB secretion in B. bacteriovorus.


Vyšlo v časopise: Ras GTPase-Like Protein MglA, a Controller of Bacterial Social-Motility in Myxobacteria, Has Evolved to Control Bacterial Predation by. PLoS Genet 10(4): e32767. doi:10.1371/journal.pgen.1004253
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004253

Souhrn

Bacterial cell polarity control is important for maintaining asymmetry of polar components such as flagella and pili. Bdellovibrio bacteriovorus is a predatory deltaproteobacterium which attaches to, and invades, other bacteria using Type IV pili (T4P) extruded from the specialised, invasive, non-flagellar pole of the cell. It was not known how that invasive pole is specified and regulated. Here we discover that a regulatory protein-hub, including Ras-GTPase-like protein MglA and cyclic-di-GMP receptor-protein CdgA, control prey-invasion. In the deltaproteobacterium, Myxococcus xanthus, MglA, with MglB and RomR, was found by others to regulate switching of T4P in social ‘swarming’ surface motility by swapping the pole at which T4P are found. In contrast, in B. bacteriovorus MglA regulates the process of prey-invasion and RomR, which is required for surface motility regulation in Myxococcus, is essential for growth and viability in Bdellovibrio. During evolution, B. bacteriovorus has lost mglB, possibly as T4P-pole-switching is not required; pili are only required at the invasive pole. A previously unidentified tetratricopeptide repeat (TPR) protein interacts with MglA and is essential for prey-invasion. This regulatory protein hub allows prey-invasion, likely integrating cyclic-di-GMP signals, pilus assembly and TamAB secretion in B. bacteriovorus.


Zdroje

1. IidaY, HobleyL, LambertC, FentonAK, SockettRE, et al. (2009) Roles of multiple flagellins in flagellar formation and flagellar growth post bdelloplast lysis in Bdellovibrio bacteriovorus. J Mol Biol 394: 1011–1021.

2. LambertC, EvansKJ, TillR, HobleyL, CapenessM, et al. (2006) Characterizing the flagellar filament and the role of motility in bacterial prey-penetration by Bdellovibrio bacteriovorus. Mol Microbiol 60: 274–286.

3. LambertC, FentonAK, HobleyL, SockettRE (2011) Predatory Bdellovibrio bacteria use gliding motility to scout for prey on surfaces. J Bacteriol 193: 3139–3141.

4. EvansKJ, LambertC, SockettRE (2007) Predation by Bdellovibrio bacteriovorus HD100 requires type IV pili. J Bacteriol 189: 4850–4859.

5. MahmoudKK, KovalSF (2010) Characterization of type IV pili in the life cycle of the predator bacterium Bdellovibrio. Microbiology 156: 1040–1051.

6. LeonardyS, MiertzschkeM, BulyhaI, SperlingE, WittinghoferA, et al. (2010) Regulation of dynamic polarity switching in bacteria by a Ras-like G-protein and its cognate GAP. Embo J 29: 2276–2289.

7. ZhangY, FrancoM, DucretA, MignotT (2010) A bacterial Ras-like small GTP-binding protein and its cognate GAP establish a dynamic spatial polarity axis to control directed motility. PLoS Biol 8: e1000430.

8. MaurielloEM, NanB, ZusmanDR (2009) AglZ regulates adventurous (A-) motility in Myxococcus xanthus through its interaction with the cytoplasmic receptor, FrzCD. Mol Microbiol 72: 964–977.

9. YangR, BartleS, OttoR, StassinopoulosA, RogersM, et al. (2004) AglZ is a filament-forming coiled-coil protein required for adventurous gliding motility of Myxococcus xanthus. J Bacteriol 186: 6168–6178.

10. KaiserD (1979) Social Gliding Is Correlated with the Presence of Pili in Myxococcus xanthus. Proc Natl Acad Sci U S A 76: 5952–5956.

11. NanB, MaurielloEM, SunIH, WongA, ZusmanDR (2010) A multi-protein complex from Myxococcus xanthus required for bacterial gliding motility. Mol Microbiol 76: 1539–1554.

12. MaurielloEM, MouhamarF, NanB, DucretA, DaiD, et al. (2010) Bacterial motility complexes require the actin-like protein, MreB and the Ras homologue, MglA. Embo J 29: 315–326.

13. SunMZ, WartelM, CascalesE, ShaevitzJW, MignotT (2011) Motor-driven intracellular transport powers bacterial gliding motility. P Natl Acad Sci USA 108: 7559–7564.

14. DucretA, ValignatMP, MouhamarF, MignotT, TheodolyO (2012) Wet-surface-enhanced ellipsometric contrast microscopy identifies slime as a major adhesion factor during bacterial surface motility. P Natl Acad Sci USA 109: 10036–10041.

15. WartelM, DucretA, ThutupalliS, CzerwinskiF, Le GallAV, et al. (2013) A Versatile Class of Cell Surface Directional Motors Gives Rise to Gliding Motility and Sporulation in Myxococcus xanthus. PLoS Biol 11: e1001728.

16. BulyhaI, SchmidtC, LenzP, JakovljevicV, HoneA, et al. (2009) Regulation of the type IV pili molecular machine by dynamic localization of two motor proteins. Mol Microbiol 74: 691–706.

17. LucianoJ, AgrebiR, Le GallAV, WartelM, FiegnaF, et al. (2011) Emergence and modular evolution of a novel motility machinery in bacteria. PLoS Genet 7: e1002268.

18. MedinaAA, ShanksRM, KadouriDE (2008) Development of a novel system for isolating genes involved in predator-prey interactions using host independent derivatives of Bdellovibrio bacteriovorus 109J. BMC Microbiol 8: 33.

19. CotterTW, ThomashowMF (1992) Identification of a Bdellovibrio bacteriovorus genetic locus, hit, associated with the host-independent phenotype. J Bacteriol 174: 6018–6024.

20. HorowitzAT, KesselM, ShiloM (1974) Growth cycle of predacious Bdellovibrios in a host-free extract system and some properties of the host extract. Journal of Bacteriology 117: 270–282.

21. KaiserD (2003) Coupling cell movement to multicellular development in myxobacteria. Nat Rev Microbiol 1: 45–54.

22. BlackhartBD, ZusmanDR (1985) “Frizzy” genes of Myxococcus xanthus are involved in control of frequency of reversal of gliding motility. Proc Natl Acad Sci U S A 82: 8767–8770.

23. KeilbergD, WuichetK, DrescherF, Sogaard-AndersenL (2012) A response regulator interfaces between the Frz chemosensory system and the MglA/MglB GTPase/GAP module to regulate polarity in Myxococcus xanthus. PLoS Genet 8: e1002951.

24. ZhangY, GuzzoM, DucretA, LiYZ, MignotT (2012) A dynamic response regulator protein modulates G-protein-dependent polarity in the bacterium Myxococcus xanthus. PLoS Genet 8: e1002872.

25. HobleyL, FungRK, LambertC, HarrisMA, DabhiJM, et al. (2012) Discrete Cyclic di-GMP-Dependent Control of Bacterial Predation versus Axenic Growth in Bdellovibrio bacteriovorus. PLoS Pathog 8: e1002493.

26. CapenessMJ, LambertC, LoveringAL, TillR, UchidaK, et al. (2013) Activity of Bdellovibrio Hit Locus Proteins, Bd0108 and Bd0109, Links Type IVa Pilus Extrusion/Retraction Status to Prey-Independent Growth Signalling. PLoS One 8: e79759.

27. FentonAK, KannaM, WoodsRD, AizawaSI, SockettRE (2010) Shadowing the Actions of a Predator: Backlit Fluorescent Microscopy Reveals Synchronous Nonbinary Septation of Predatory Bdellovibrio inside Prey and Exit through Discrete Bdelloplast Pores. J Bacteriol 192: 6329–6335.

28. FremgenSA, BurkeNS, HartzellPL (2010) Effects of site-directed mutagenesis of mglA on motility and swarming of Myxococcus xanthus. BMC Microbiol 10: 295.

29. MiertzschkeM, KoernerC, VetterIR, KeilbergD, HotE, et al. (2011) Structural analysis of the Ras-like G protein MglA and its cognate GAP MglB and implications for bacterial polarity. Embo J 30: 4185–4197.

30. SeiS, MussioJK, YangQE, NagashimaK, ParchmentRE, et al. (2009) Synergistic antitumor activity of oncolytic reovirus and chemotherapeutic agents in non-small cell lung cancer cells. Mol Cancer 8: 47.

31. HartzellP, KaiserD (1991) Upstream gene of the mgl operon controls the level of MglA protein in Myxococcus xanthus. J Bacteriol 173: 7625–7635.

32. HobleyL, LernerTR, WilliamsLE, LambertC, TillR, et al. (2012) Genome analysis of a simultaneously predatory and prey-independent, novel Bdellovibrio bacteriovorus from the River Tiber, supports in silico predictions of both ancient and recent lateral gene transfer from diverse bacteria. BMC Genomics 13: 670.

33. SnyderAR, WilliamsHN, BaerML, WalkerKE, StineOC (2002) 16S rDNA sequence analysis of environmental Bdellovibrio-and-like organisms (BALO) reveals extensive diversity. Int J Syst Evol Microbiol 52: 2089–2094.

34. KarimovaG, PidouxJ, UllmannA, LadantD (1998) A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci U S A 95: 5752–5756.

35. KarpenahalliMR, LupasAN, SodingJ (2007) TPRpred: a tool for prediction of TPR-, PPR- and SEL1-like repeats from protein sequences. BMC Bioinformatics 8: 2.

36. PetersenTN, BrunakS, von HeijneG, NielsenH (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785–786.

37. LeonardyS, FreymarkG, HebenerS, EllehaugeE, Sogaard-AndersenL (2007) Coupling of protein localization and cell movements by a dynamically localized response regulator in Myxococcus xanthus. Embo J 26: 4433–4444.

38. SeidlerRJ, StarrMP (1969) Isolation and characterisation of host-independent Bdellovibrios. J Bacteriol 100: 769–785.

39. SelkrigJ, MosbahiK, WebbCT, BelousoffMJ, PerryAJ, et al. (2012) Discovery of an archetypal protein transport system in bacterial outer membranes. Nat Struct Mol Biol 19: 506–510, S501.

40. MalinverniJC, WernerJ, KimS, SklarJG, KahneD, et al. (2006) YfiO stabilizes the YaeT complex and is essential for outer membrane protein assembly in Escherichia coli. Mol Microbiol 61: 151–164.

41. FanE, FiedlerS, Jacob-DubuissonF, MullerM (2012) Two-partner secretion of gram-negative bacteria: a single beta-barrel protein enables transport across the outer membrane. J Biol Chem 287: 2591–2599.

42. YouderianP, HartzellPL (2006) Transposon insertions of magellan-4 that impair social gliding motility in Myxococcus xanthus. Genetics 172: 1397–1410.

43. MacaraIG, LounsburyKM, RichardsSA, McKiernanC, Bar-SagiD (1996) The Ras superfamily of GTPases. FASEB Journal 10: 625–630.

44. RosenbergE, KellerKH, DworkinM (1977) Cell density-dependent growth of Myxococcus xanthus on casein. J Bacteriol 129: 770–777.

45. EvansAG, DaveyHM, CooksonA, CurrinnH, Cooke-FoxG, et al. (2012) Predatory activity of Myxococcus xanthus outer-membrane vesicles and properties of their hydrolase cargo. Microbiology 158: 2742–2752.

46. CowlesKN, MoserTS, SiryapornA, NyakudarikaN, DixonW, et al. (2013) The putative Poc complex controls two distinct Pseudomonas aeruginosa polar motility mechanisms. Mol Microbiol 90: 923–938.

47. WolfgangM, van PuttenJP, HayesSF, DorwardD, KoomeyM (2000) Components and dynamics of fiber formation define a ubiquitous biogenesis pathway for bacterial pili. Embo J 19: 6408–6418.

48. 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.

49. SteyertSR, PineiroSA (2007) Development of a novel genetic system to create markerless deletion mutants of Bdellovibrio bacteriovorus. Appl Environ Microbiol 73: 4717–4724.

50. DereeperA, GuignonV, BlancG, AudicS, BuffetS, et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research 36: W465–W469.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2014 Číslo 4
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

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#