Identification of the YfgF MASE1 domain as a modulator of bacterial responses to aspartate

Article English OPEN
Lacey, Melissa ; Agasing, Agnieshka ; Lowry, Rebecca ; Green, Jeffrey (2013)
  • Publisher: The Royal Society
  • Journal: Open Biology, volume 3, issue 6 (eissn: 2046-2441)
  • Related identifiers: doi: 10.1098/rsob.130046, pmc: PMC3718329
  • Subject: 200 | Research Article | Salmonella | MASE1 domain | cyclic-di-GMP | 1001 | Research | oxidative stress | chemotaxis

Complex 3'-5'-cyclic diguanylic acid (c-di-GMP) responsive regulatory networks that are modulated by the action of multiple diguanylate cyclases (DGC; GGDEF domain proteins) and phosphodiesterases (PDE; EAL domain proteins) have evolved in many bacteria. YfgF proteins possess a membrane-anchoring domain (MASE1), a catalytically inactive GGDEF domain and a catalytically active EAL domain. Here, sustained expression of the Salmonella enterica spp. Enterica ser. Enteritidis YfgF protein is shown to mediate inhibition of the formation of the aspartate chemotactic ring on motility agar under aerobic conditions. This phenomenon was c-di-GMP-independent because it occurred in a Salmonella strain that lacked the ability to synthesize c-di-GMP and also when PDE activity was abolished by site-directed mutagenesis of the EAL domain. YfgF-mediated inhibition of aspartate chemotactic ring formation was impaired in the altered redox environment generated by exogenous p-benzoquinone. This ability of YfgF to inhibit the response to aspartate required a motif, (213)Lys-Lys-Glu(215), in the predicted cytoplasmic loop between trans-membrane regions 5 and 6 of the MASE1 domain. Thus, for the first time the function of a MASE1 domain as a redox-responsive regulator of bacterial responses to aspartate has been shown.
  • References (32)
    32 references, page 1 of 4

    Mills E, Pultz IS, Kulasekara HD, Miller SI. 2011 The bacterial second messenger c-di-GMP: mechanisms of signalling. Cell Microbiol. 13, 1122 - 1129.

    (doi:10.1111/j.1462-5822.2011.01619.x) Pesavento C, Hengge R. 2009 Bacterial nucleotidebased second messengers. Curr. Opin. Microbiol. 12, 170 - 176. (doi:10.1016/j.mib.2009.01.007) Lacey MM, Partridge JD, Green J. 2010 Escherichia coli K12 YfgF is an anaerobic cyclic di-GMP phosphodiesterase with roles in cell surface re-modelling and the oxidative stress response. Microbiology 156, 2873 - 2888. (doi:10.

    1099/mic.0.037887-0)

    Nikolskaya AN, Mulkidjanian AY, Beech IB, Galperin MY. 2003 MASE1 and MASE2: two novel integral membrane sensory domains. J. Mol. Microbiol.

    Biotechnol. 5, 11 - 16. (doi:10.1159/000068720) Solano C, Garc´ıa B, Latasa C, Toledo-Arana A, Zorraquino V, Valle J, Casals J, Pedroso E, Lasa I.

    2009 Genetic reductionist approach for dissecting individual roles of GGDEF proteins within the c-diGMP signalling network in Salmonella. Proc. Natl Acad. Sci. USA 101, 16 322 - 16 327. (doi:10.1073/ pnas.0812573106)

    Girgis HS, Liu Y, Ryu WS, Tavazoie S. 2007 A comprehensive genetic characterization of bacterial motility. PLoS Genet. 3, 1644 - 1660. (doi:10.1371/ journal.pgen.0030154)

    7. Lennox ES. 1955 Transduction of linked genetic characters of the host by bacteriophage P1. Virology 1, 190 - 206. (doi:10.1016/0042- 6822(55)90016-7)

    8. Sambrook JW, Russell DW. 2001 Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Press.

    9. Umemura T, Matsumoto Y, Ohnishi K, Homma M, Kawagishi I. 2002 Sensing of cytoplasmic pH by bacterial chemoreceptors involves the linker region that connects the membrane-spanning and the signal-modulating helices. J. Biol. Chem. 277, 1593 - 1598. (doi:10.1074/jbc.M109930200)

  • Related Research Results (1)
  • Metrics
    No metrics available
Share - Bookmark