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Cell polarity/motility in bacteria: closer to eukaryotes than expected?

2010; Springer Nature; Volume: 29; Issue: 14 Linguagem: Inglês

10.1038/emboj.2010.144

1460-2075

Emilia M. F. Mauriello,

Bacterial biofilms and quorum sensing

Have you seen?21 July 2010free access Cell polarity/motility in bacteria: closer to eukaryotes than expected? Emilia M F Mauriello Corresponding Author Emilia M F Mauriello Department of Molecular and Cell Biology, University of California, Berkeley, CA, USA Search for more papers by this author Emilia M F Mauriello Corresponding Author Emilia M F Mauriello Department of Molecular and Cell Biology, University of California, Berkeley, CA, USA Search for more papers by this author Author Information Emilia M F Mauriello 1 1Department of Molecular and Cell Biology, University of California, Berkeley, CA, USA *Correspondence to: [email protected] The EMBO Journal (2010)29:2258-2259https://doi.org/10.1038/emboj.2010.144 There is an Article (July 2010) associated with this Have you seen ...?. PDFDownload PDF of article text and main figures. ToolsAdd to favoritesDownload CitationsTrack CitationsPermissions ShareFacebookTwitterLinked InMendeleyWechatReddit Figures & Info The Gram-negative bacterium Myxococcus xanthus glides on solid surfaces and periodically reverses the direction of movement. Work published in this issue of The EMBO Journal (Leonardy et al, 2010) reports on the small GTPase MglA that ensures the correct polarity of the motility engines through its GTP/GDP cycle in conjunction with its cognate GAP, MglB. MglA has also been shown to interact with the actin-like protein MreB in eukaryotic-like motility complexes. Altogether, the data suggest that compelling similarities exist between the mechanisms of motility and establishment of cell polarity in M. xanthus and eukaryotes. M. xanthus moves through the synergistic activity of two genetically, functionally and structurally different motility engines (Hodgkin and Kaiser, 1979). The first motility system, Social (S) motility, functions through the extension and retraction of polar Type IV Pili (Sun et al, 2000), whereas the second motility system, Adventurous (A) motility, is powered by distributed motors that assemble at the leading cell pole. These motors behave similarly to the eukaryotic focal adhesion complexes observed in apicomplexan parasites (Mignot et al, 2007). M. xanthus cells periodically reverse the direction of their movement by switching the polarity of the A and S engines at a frequency that is modulated by the Frz chemosensory system (Zusman et al, 2007) (Figure 1). Recently, evidence indicates the fact that similar mechanisms are shared by M. xanthus and eukaryotic cells regarding the way in which motility functions and cell polarity are established. In particular, the featured paper from the Sogaard–Andersen laboratory describes the importance of a small GTPase, MglA and its GTP/GDP cycle in the regulation of cell polarity in M. xanthus (Leonardy et al, 2010). The GTPases of the Ras superfamily perform a broad range of functions in eukaryotic cells including transport, signal transduction and cell migration (Charest and Firtel, 2007). The gene encoding MglA was first reported by Hodgkin and Kaiser (1979) and annotated as mutual gliding A (mglA) mutant, because its deletion caused defects in both A and S motility (Hodgkin and Kaiser, 1979). Some years later, Hartzell (1997) showed that MglA belongs to the Ras superfamily of small eukaryotic GTPases. In fact, the expression of the yeast Ras family protein SAR1 in mglA cells that were unable to sporulate rescued sporulation (Hartzell, 1997). Mauriello et al (2010) first showed that MglA is able to slowly hydrolyse GTP in vitro and represents a polarity factor in M. xanthus as it (i) localizes mostly at the leading cell pole (also along the cell, in positions occupied by the A motility machineries); (ii) establishes the polar localization of motility proteins using mechanisms that might also involve the actin-like protein, MreB (Mauriello et al, 2010). Figure 1.The core of the Frz system, such as chemotaxis pathways in enteric bacteria, consists of a receptor, FrzCD, a histidine kinase, FrzE, a CheW-like coupling protein FrzA and a dual response regulator protein, FrzZ (Zusman et al, 2007). MglA and MglB are downstream of the Frz pathway. The Frz pathway might act as a direct or indirect GEF of MglA and mediate the accumulation of GTP-bound MglA at the leading pole. MglB, acting as a GAP, inhibits MglA localization at the lagging pole by keeping the concentration of GTP-bound MglA very low at this site. The MglA GTPase activity is essential to establish the correct polar localization of RomR and PilT, but not AlgZ. Mauriello et al (2010) showed that in the absence of MglA, AglZ and FrzS are mislocalized (AglZ also signals directly to FrzCD). In the absence of MglA, activity cells still reverse, suggesting the presence of a yet unproved regulatory activity of the Frz pathway on MglA (dashed line) and the existence of an intrinsic reversal clock. Download figure Download PowerPoint In their recent work, Leonardy et al (2010) conducted elegant biochemical analyses to assign MglB, the small protein produced by the first gene of the mglBA operon, the function of the cognate GAP of MglA. The authors, in fact, showed that MglB specifically recognizes, binds to and stabilizes the GTP-bound form of MglA, significantly enhancing the hydrolysis of GTP. The GTPase activity, but not the ability to bind GTP, is lost when MglA carries a G to V substitution that locks the protein in the GTP-bound state. Subsequent in vivo analyses revealed the biological significance of the MglA-MglB combined activity and the function of the GTP/GDP cycle in the establishment of cell polarity in M. xanthus. Although mglA mutant cells appear to be completely non-motile, mglAG21V and mglB mutant cells show a hyper-reversing phenotype. This suggests that while the complete absence of MglA causes a lack of cell movement, the lack of only the GTPase activity leads to an unregulated reversal frequency and switch of polarity. Double mutants and phenotypic analyses show that the Frz chemosensory system signals, directly or indirectly, to MglA to control the reversal frequency (Figure 1). The result represents an additional point of similarity with eukaryotic organisms, such as Dictyostelium discoideum in which small GTPases work in concert with chemoreceptors to polarize the cell and determine directional movement during chemotaxis. On the basis of localization studies, the authors hypothesize how MglB exerts its function as a GAP of MglA and propose that the establishment of cell polarity depends on the equilibrium between GTP and GDP-bound MglA. First of all, the authors show that GTP-bound MglA (YFP-MglA and YFP-MglAG21V) predominantly localizes at the leading cell pole and switches its polar localization upon cell reversals. Conversely, GDP-bound MglA (YFP-MglAT26/27N) is diffused in the cytoplasm. MglB-YFP localizes at the opposite pole with respect to MglA. YFP-MglA localization is affected in mglB mutant cells in which the protein localizes at both cell poles. The authors propose that the Frz pathway acts as a direct or indirect GEF as it favours the accumulation of GTP-bound MglA at the leading pole. At the opposite pole, MglB keeps the concentration of GTP-bound MglA very low by promoting GTP hydrolysis. A reversal occurs when GTP-bound MglA reaches a concentration high enough to form a cluster at the lagging pole. By an as of yet unknown mechanism, MglB then relocates the old leading pole and a new reversal cycle begins. Patryn et al (2010) proposed, based on immunofluorescence microscopy studies, that the relocation of MglA from pole to pole occurs in a helical manner further reinforcing the hypothesis that MglA and MreB work in concert (Mauriello et al, 2010; Patryn et al, 2010). Interestingly, in the absence of MglA GTPase activity, cells are still able to reverse suggesting the existence in M. xanthus cells of a yet uncharacterized intrinsic reversal clock. Acknowledgements I thank Eva Campodonico and Juan-Jesus Vicente for helpful criticisms and discussions. EMFM's salary is supported by grants from the National Institute of Health to DRZ (GM020509). Conflict of Interest The author declares that she has no conflict of interest. References Charest PG, Firtel RA (2007) Big roles for small GTPases in the control of directed cell movement. Biochem J 401: 377–390CrossrefCASPubMedWeb of Science®Google Scholar Hartzell PL (1997) Complementation of sporulation and motility defects in a prokaryote by a eukaryotic GTPase. Proc Natl Acad Sci USA 94: 9881–9886CrossrefCASPubMedGoogle Scholar Hodgkin J, Kaiser D (1979) Genetics of gliding motility in Myxococcus xanthus (Myxobacterales): two gene systems control movement. Mol Gen Genet 171: 177–191CrossrefWeb of Science®Google Scholar Leonardy S, Miertzschke M, Bulyha I, Sperling EAW, Søgaard-Andersen L (2010) Regulation of dynamic polarity switching in bacteria by a Ras-like G-protein and its cognate GAP. EMBO J 29: 2276–2289Wiley Online LibraryCASPubMedWeb of Science®Google Scholar Mauriello EM, Mouhamar F, Nan B, Ducret A, Dai D, Zusman DR, Mignot T (2010) Bacterial motility complexes require the actin-like protein, MreB and the Ras homologue, MglA. EMBO J 29: 315–326Wiley Online LibraryCASPubMedWeb of Science®Google Scholar Mignot T, Shaevitz JW, Hartzell PL, Zusman DR (2007) Evidence that focal adhesion complexes power bacterial gliding motility. Science 315: 853–856CrossrefCASPubMedWeb of Science®Google Scholar Patryn J, Allen K, Dziewanowska K, Otto R, Hartzell PL (2010) Localization of MglA, an essential gliding motility protein in Myxococcus xanthus. Cytoskeleton (Hoboken) 67: 322–337Wiley Online LibraryCASPubMedWeb of Science®Google Scholar Sun H, Zusman DR, Shi W (2000) Type IV pilus of Myxococcus xanthus is a motility apparatus controlled by the frz chemosensory system. Curr Biol 10: 1143–1146CrossrefCASPubMedWeb of Science®Google Scholar Zusman DR, Scott AE, Yang Z, Kirby JR (2007) Chemosensory pathways, motility and development in Myxococcus xanthus. Nat Rev Microbiol 5: 862–872CrossrefCASPubMedWeb of Science®Google Scholar Previous ArticleNext Article Read MoreAbout the coverClose modalView large imageVolume 29,Issue 14,July 21, 2010This giant scarab beetle is a male Chalcosoma caucasus, commonly known as the 'Atlas beetle', one of the largest insects on Earth. Males often measure up to 120 mm in length and live in Malaysia and Indonesia. This photograph was selected as one of the top ten images in the EMBO Journal Cover Contest 2010. The photographer, Marcus Resch from the University of Erlangen-Nürnberg, Germany, is a structural biologist with an interest in "all kinds of insects and insectivorous plants." Volume 29Issue 1421 July 2010In this issue FiguresReferencesRelatedDetailsLoading ...