The host plant metabolite glucose is the precursor of diffusible signal factor (DSF) family signals in Xanthomonas campestris

Applied and Environmental Microbiology

Volumn 81, Issue 8, 2015, Pages 2861-2868

  Deng, Yinyue ^a,b   Liu, Xiaoling ^c   Wu, Ji'en ^a   Lee, Jasmine ^a   Chen, Shaohua ^a,b   Cheng, Yingying ^b   Zhang, Chunyan ^a   Zhang, Lian Hui ^a,b  

^a INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^b SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

^c CHONGQING ACADEMY OF CHINESE MATERIA MEDICA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOFILMS; BIOSYNTHESIS; CELL SIGNALING; GLUCOSE; LIQUID CHROMATOGRAPHY;

BIOFILM FORMATION; CELL-CELL COMMUNICATIONS; CHROMATOGRAPHIC SEPARATIONS; DIFFUSIBLE SIGNALS; SIGNAL SYNTHESIS; SYNTHETIC MECHANISM; VIRULENCE FACTORS; XANTHOMONAS CAMPESTRIS;

METABOLITES;

BACTERIUM; BIOFILM; GLUCOSE; GROWTH RATE; HOST PLANT; METABOLITE; VIRULENCE;

BURKHOLDERIA CENOCEPACIA; XANTHOMONAS CAMPESTRIS; XANTHOMONAS CAMPESTRIS PV. CAMPESTRIS;

BACTERIAL PROTEIN; GLUCOSE; VIRULENCE FACTOR;

BIOFILM; BRASSICA RAPA; CHEMISTRY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; XANTHOMONAS CAMPESTRIS;

BACTERIAL PROTEINS; BIOFILMS; BRASSICA RAPA; GLUCOSE; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VIRULENCE FACTORS; XANTHOMONAS CAMPESTRIS;

EID: 84927794954     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03813-14     Document Type: Article

References (39)

1. Deng Y, Wu J, Tao F, Zhang LH. 2011. Listening to a new language: DSF-based quorum sensing in Gram-negative bacteria. Chem Rev 111: 160-173. http://dx.doi.org/10.1021/cr100354f.
2. Fuqua C, Greenberg EP. 2002. Listening in on bacteria: acyl-homoserine lactone signaling. Nat Rev Mol Cell Biol 3:685-695. http://dx.doi.org/10.1038/nrm907.
3. Zhang LH, Dong YH. 2004. Quorum sensing and signal interference: diverse implications. Mol Microbiol 53:1563-1571. http://dx.doi.org/10.1111/j.1365-2958.2004.04234.x.
4. Whitehead NA, Barnard AM, Slater H, Simpson NJ, Salmond GP. 2001. Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev 25: 365-404. http://dx.doi.org/10.1111/j.1574-6976.2001.tb00583.x.
5. Williams P, Winzer K, Chan WC, Cámara M. 2007. Look who's talking: communication and quorum sensing in the bacterial world. Philos Trans R Soc Lond B Biol Sci 362:1119-1134. http://dx.doi.org/10.1098/rstb.2007.2039.
6. Moré MI, Finger LD, Stryker JL, Fuqua C, Eberhard A, Winans SC. 1996. Enzymatic synthesis of a quorum-sensing autoinducer through use of defined substrates. Science 272:1655-1658. http://dx.doi.org/10.1126/science.272.5268.1655.
7. Schaefer AL, Val DL, Hanzelka BL, Cronan JE, Jr, Greenberg EP. 1996. Generation of cell-to-cell signals in quorum sensing: acyl homoserine lactone synthase activity of a purified Vibrio fischeri LuxI protein. Proc Natl Acad Sci U S A 93:9505-9509. http://dx.doi.org/10.1073/pnas.93.18.9505.
8. Zhang LH. 2003. Quorum quenching and proactive host defense. Trends Plant Sci 8:238-244. http://dx.doi.org/10.1016/S1360-1385(03)00063-3.
9. Deng Y, Boon C, Eberl L, Zhang LH. 2009. Differential modulation of Burkholderia cenocepacia virulence and energy metabolism by quorum sensing signal BDSF and its synthase. J Bacteriol 191:7270-7278. http://dx.doi.org/10.1128/JB.00681-09.
10. He YW, Zhang LH. 2008. Quorum sensing and virulence regulation in Xanthomonas campestris. FEMS Microbiol Rev 32:842-857. http://dx.doi.org/10.1111/j.1574-6976.2008.00120.x.
11. Wang LH, He Y, Gao Y, Wu JE, Dong YH, He C, Wang SX, Weng LX, Xu JL, Tay L, Fang RX, Zhang LH. 2004. A bacterial cell-cell communication signal with cross-kingdom structural analogues. Mol Microbiol 51:903-912.
12. Huang TP, Lee Wong AC. 2007. Extracellular fatty acids facilitate flagella-independent translocation by Stenotrophomonas maltophilia. Res Microbiol 158:702-711. http://dx.doi.org/10.1016/j.resmic.2007.09.002.
13. Almeida RP, Killiny N, Newman KL, Chatterjee S, Ionescu M, Lindow SE. 2012. Contribution of rpfB to cell-to-cell signal synthesis, virulence, and vector transmission of Xylella fastidiosa. Mol Plant Microbe Interact 25:453-462. http://dx.doi.org/10.1094/MPMI-03-11-0074.
14. Colnaghi Simionato AV, da Silva DS, Lambais MR, Carrilho E. 2007. Characterization of a putative Xylella fastidiosa diffusible signal factor by HRGC-EI-MS. J Mass Spectrom 42:490-496. http://dx.doi.org/10.1002/jms.1181.
15. Boon C, Deng Y, Wang LH, He Y, Xu JL, Fan Y, Pan SQ, Zhang LH. 2008. A novel DSF-like signal from Burkholderia cenocepacia interferes with Candida albicans morphological transition. ISME J 2:27-36. http://dx.doi.org/10.1038/ismej.2007.76.
16. Davies DG, Marques CN. 2009. A fatty acid messenger is responsible for inducing dispersion in microbial biofilms. J Bacteriol 191:1393-1403. http://dx.doi.org/10.1128/JB.01214-08.
17. Deng Y, Wu JE, Eberl L, Zhang LH. 2010. Structural and functional characterization of diffusible signal factor family quorum-sensing signals produced by members of the Burkholderia cepacia complex. Appl Environ Microbiol 76:4675-4683. http://dx.doi.org/10.1128/AEM.00480-10.
18. He YW, Wu J, Cha JS, Zhang LH. 2010. Rice bacterial blight pathogen Xanthomonas oryzae pv. oryzae produces multiple DSF-family signals in regulation of virulence factor production. BMC Microbiol 10:187. http://dx.doi.org/10.1186/1471-2180-10-187.
19. Vílchez R, Lemme A, Ballhausen B, Thiel V, Schulz S, Jansen R, Sztajer H, Wagner-Döbler I. 2010. Streptococcus mutans inhibits Candida albicans hyphal formation by the fatty acid signaling molecule trans-2-decenoic acid (SDSF). ChemBioChem 11:1552-1562. http://dx.doi.org/10.1002/cbic.201000086.
20. Barber CE, Tang JL, Feng JX, Pan MQ, Wilson TJ, Slater H, Dow JM, Williams P, Daniels MJ. 1997. A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. Mol Microbiol 24:555-566. http://dx.doi.org/10.1046/j.1365-2958.1997.3721736.x.
21. Bi H, Yu Y, Dong H, Wang H, Cronan JE. 2014. Xanthomonas campestris RpfB is a fatty Acyl-CoA required to counteract the thioesterase activity of the RpfF diffusible signal factor (DSF) synthase. Mol Microbiol 93:262-275. http://dx.doi.org/10.1111/mmi.12657.
22. He YW, Wang C, Zhou L, Song H, Dow JM, Zhang LH. 2006. Dual signaling functions of the hybrid sensor kinase RpfC of Xanthomonas campestris involve either phosphorelay or receiver domain-protein interaction. J Biol Chem 281:33414-33421. http://dx.doi.org/10.1074/jbc.M606571200.
23. Ryan RP, Fouhy Y, Lucey JF, Crossman LC, Spiro S, He YW, Zhang LH, Heeb S, Cámara M, Williams P, Dow JM. 2006. Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc Natl Acad Sci USA 103:6712-6717. http://dx.doi.org/10.1073/pnas.0600345103.
24. Slater H, Alvarez-Morales A, Barber CE, Daniels MJ, Dow JM. 2000. A two-component system involving an HD-GYP domain protein links cellcell signalling to pathogenicity gene expression in Xanthomonas campestris. Mol Microbiol 38:986-1003.
25. Cheng Z, He YW, Lim SC, Qamra R, Walsh MA, Zhang LH, Song H. 2010. Structural basis of the sensor-synthase interaction in autoinduction of the quorum sensing signal DSF biosynthesis. Structure 18:1199-1209. http://dx.doi.org/10.1016/j.str.2010.06.011.
26. Andrade MO, Alegria MC, Guzzo CR, Docena C, Rosa MC, Ramos CH, Farah CS. 2006. The HD-GYP domain of RpfG mediates a direct linkage between the Rpf quorum-sensing pathway and a subset of diguanylate cyclase proteins in the phytopathogen Xanthomonas axonopodis pv. citri. Mol Microbiol 62:537-551. http://dx.doi.org/10.1111/j.1365-2958.2006.05386.x.
27. Chatterjee S, Wistrom C, Lindow SE. 2008. A cell-cell signaling sensor is required for virulence and insect transmission of Xylella fastidiosa. Proc Natl Acad Sci U S A 105:2670-2675. http://dx.doi.org/10.1073/pnas.0712236105.
28. Fouhy Y, Scanlon K, Schouest K, Spillane C, Crossman L, Avison MB, Ryan RP, Dow JM. 2007. Diffusible signal factor-dependent cell-cell signaling and virulence in the nosocomial pathogen Stenotrophomonas maltophilia. J Bacteriol 189:4964-4968. http://dx.doi.org/10.1128/JB.00310-07.
29. Newman KL, Almeida RP, Purcell AH, Lindow SE. 2004. Cell-cell signaling controls Xylella fastidiosa interactions with both insects and plants. Proc Natl Acad Sci U S A 101:1737-1742. http://dx.doi.org/10.1073/pnas.0308399100.
30. Scarpari LM, Lambais MR, Silva DS, Carraro DM, Carrer H. 2003. Expression of putative pathogenicity-related genes in Xylella fastidiosa grown at low and high cell density conditions in vitro. FEMS Microbiol Lett 222:83-92. http://dx.doi.org/10.1016/S0378-1097(03)00251-9.
31. Bi H, Christensen QH, Feng Y, Wang H, Cronan JE. 2012. The Burkholderia cenocepacia BDSF quorum sensing fatty acid is synthesized by a bifunctional crotonase homologue having both dehydratase and thioesterase activities. Mol Microbiol 83:840-855. http://dx.doi.org/10.1111/j.1365-2958.2012.07968.x.
32. Alavi P, Muller H, Cardinale M, Zachow C, Sanchez MB, Martinez JL, Berg G. 2013. The DSF quorum sensing system controls the positive influence of Stenotrophomonas maltophilia on plants. PLoS One 8:e67103. http://dx.doi.org/10.1371/journal.pone.0067103.
33. He YW, Ng AY, Xu M, Lin K, Wang LH, Dong YH, Zhang LH. 2007. Xanthomonas campestris cell-cell communication involves a putative nucleotide receptor protein Clp and a hierarchical signalling network. Mol Microbiol 64:281-292. http://dx.doi.org/10.1111/j.1365-2958.2007.05670.x.
34. Daniels MJ, Barber CE, Turner PC, Cleary WG, Sawczyc MK. 1984. Isolation of mutants of Xanthomonas campestris pathovar campestris showing altered pathogenicity. J Gen Microbiol 130:2447-2455.
35. Jefferson RA, Kavanagh TA, Bevan MW. 1987. GUS fusions: betaglucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901-3907.
36. Dow JM, Crossman L, Findlay K, He YQ, Feng JX, Tang JL. 2003. Biofilm dispersal in Xanthomonas campestris is controlled by cell-cell signaling and is required for full virulence to plants. Proc Natl Acad Sci U S A 100:10995-11000. http://dx.doi.org/10.1073/pnas.1833360100.
37. Blom K, Dybowski C, Munson B. 1987. Mass spectral analysis of isotopically labeled compounds: average mass approach. Anal Chem 59:1372-1374. http://dx.doi.org/10.1021/ac00136a025.
38. Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML, Qu XQ, Guo WJ, Kim JG, Underwood W, Chaudhuri B, Chermak D, Antony G, White FF, Somerville SC, Mudgett MB, Frommer WB. 2010. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468:527-534. http://dx.doi.org/10.1038/nature09606.
39. Chen LQ, Qu XQ, Hou BH, Sosso D, Osorio S, Fernie AR, Frommer WB. 2012. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335:207-211. http://dx.doi.org/10.1126/science.1213351.