The cyclic-di-GMP diguanylate cyclase CdgA has a role in biofilm formation and exopolysaccharide production in Azospirillum brasilense

Research in Microbiology

Volumn 167, Issue 3, 2016, Pages 190-201

  Ramírez Mata, Alberto ^a   López Lara, Lilia I ^a   Xiqui Vázquez, Ma Luisa ^a   Jijón Moreno, Saúl ^a   Romero Osorio, Angelica ^a   Baca, Beatriz E ^a  

^a BENEMÉRITA UNIVERSIDAD AUTÓNOMA DE PUEBLA   (Mexico)

Author keywords

Azospirillum brasilense; Biofilm production; Cyclic di GMP; Diguanylate cyclase activity

Indexed keywords

CRYSTAL VIOLET; DEOXYRIBONUCLEASE I; DIGUANYLATE CYCLASE A; DNA; EXOPOLYSACCHARIDE; FLAVINE ADENINE NUCLEOTIDE; GREEN FLUORESCENT PROTEIN; GUANOSINE TRIPHOSPHATE; GUANYLATE CYCLASE; MAGNESIUM; UNCLASSIFIED DRUG; BACTERIAL POLYSACCHARIDE; BIS(3',5')-CYCLIC DIGUANYLIC ACID; COENZYME; CYCLIC GMP; DIGUANYLATE CYCLASE; ESCHERICHIA COLI PROTEIN; LYASE;

ARTICLE; AZOSPIRILLUM BRASILENSE; BACTERIAL GROWTH; BACTERIAL STRAIN; BIOFILM; CONFOCAL LASER MICROSCOPY; DELETION MUTANT; ENZYME ACTIVITY; EPIFLUORESCENCE MICROSCOPY; GENE INACTIVATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PURIFICATION; STAINING; THICKNESS; WILD TYPE; ANALOGS AND DERIVATIVES; BIOSYNTHESIS; COENZYME; CONFOCAL MICROSCOPY; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGICAL EXAMINATION; PHYSIOLOGY;

AZOSPIRILLUM BRASILENSE; BACTERIOLOGICAL TECHNIQUES; BIOFILMS; COENZYMES; CYCLIC GMP; ESCHERICHIA COLI PROTEINS; FLAVIN-ADENINE DINUCLEOTIDE; GUANOSINE TRIPHOSPHATE; MAGNESIUM; MICROSCOPY, CONFOCAL; PHOSPHORUS-OXYGEN LYASES; POLYSACCHARIDES, BACTERIAL; STAINING AND LABELING;

EID: 84955260872     PISSN: 09232508     EISSN: 17697123     Source Type: Journal    
DOI: 10.1016/j.resmic.2015.12.004     Document Type: Article

References (45)

1. Römling U., Gomelsky M., Galperin M.Y. C-di-GMP: the dawning of a novel bacterial signaling system. Mol Microbiol 2005, 57:629-639.
2. Newell P., Yoshioka S., Hvorecny K.L., Monds R.D., O'Toole G.A. Systematic analysis of diguanylate cyclases that promote biofilm formation by Pseudomonas fluorencens Pf0-1. J Bacteriol 2011, 193:4685-4698.
3. Ryan R.P., McCarthy Y., Andrade M., Farah C.S., Armitage J.P., Dow J.M. Cell-cell signal dependent dynamic interactions between HD-GYP and GGDEF domain proteins mediate virulence in Xanthomonas campestris. Proc Natl Acad Sci U S A 2010, 107:5989-5994.
4. Pedraza R.O., Mentel M.I., Ragout A.L., Xiqui M.L., Segundo D.M., Baca B.E. The role of chemotaxis in the association Azospirillum brasilense-plant. Chemotaxis: types, clinical significance, and mathematical models 2011, 53-83. Nova Science Publishers. T.C. Williams (Ed.).
5. Römling U., Galperin M.Y., Gomelsky M. C-di- GMP: the first 25 years of a universal bacterial second messenger. Microb Mol Biol Rev 2013, 77:1-52.
6. Karatan E., Watnick P. Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev 2009, 73:310-347.
7. Galperin M.A. Census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiol 2005, 5:35-54.
8. Bordeleau E., Fortier L.E., Malouin, Burrus V. c-di-GMP turn over in Clostridium difficile is controlled by a plethora of diguanylate cyclases and phosphodiesterases. PLos Genet 2011, 7:e1002039. 10.1371/journal.pgen.100203.
9. Wang Y., JiXu A., Chen Y., Wang J., Zhu G.Y., Ling X., et al. GGDEF and EAL proteins play different roles in the control of Sinorhizobium meliloti growth, motility, exopolysaccharide production, and competitive nodulation on host alfalfa. Acta Bichem Biophys Sin 2010, 42:410-417.
10. Jonas C., Melefors Ö., Römling U. Regulation of c-di-GMP metabolism in biofilms. Future Microbiol 2009, 4:341-358. 10.2217/fmb.09.7.
11. Lee E.R., Baker J.L., Weinberg Z., Sudarsan N., Breaker R.R. An allosteric self-splicing ribozyme triggered by a bacterial second messenger. Science 2010, 329:845-848.
12. Ma L., Conover M., Lu H., Parsek M.R., Bayles K., Wozniak D.J. Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Path 2009, 5. 10.1371/journal.ppat.1000354.
13. Steenhoudt O., Vanderleyden J. Azospirillum, a free living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemistry and ecological aspects. FEMS Microbiol Rev 2000, 24:487-506.
14. Alexandre G., Greer-Phillips S., Zhulin I.B. Ecological role of energy taxis in microorganisms. FEMS Microbiol Rev 2004, 28:113-126.
15. Alexandre G. Coupling metabolism and chemotaxis dependent behaviours by energy taxis receptors. Microbiology 2010, 156:2283-2293.
16. Fibach-Paldi S., Burdman S., Okon Y. Key physiological properties contributing to rhizosphere adaptation and plant growth promotion abilities of Azospirillum brasilense. FEMS Microbiol Lett 2012, 326:99-108.
17. Greer-Phillips S.E., Stephens B.B., Alexandre G. An energy taxis transducer promotes root colonization by Azospirillum brasilense. J Bacteriol 2004, 186:6595-6604.
18. Wisniewski-Dyé F., Borziak K., Khalsa-Moyers G., Alexandre G., Sukharnikov L.O., Wuichet K., et al. Azospirillum genomes reveal transition of bacteria from aquatic to terrestrial environments. PLoS Genet 2011, 7:e102430. 10.1371/journal.pgen.1002430.
19. Carreño-López R., Sánchez A., Camargo N., Elmerich C., Baca B.E. Characterization of chsA, a new gene controlling the chemotactic response, in Azospirillum brasilense Sp7. Arch Microbiol 2009, 191:501-507.
20. Katupitiya S., Millet J., Vesk M., Viccars L., Zeman A., Lidong Z., et al. A mutant of Azospirillum brasilense Sp7 impaired in flocculation with a modified colonization pattern and superior nitrogen fixation in association with wheat. Appl Environ Microbiol 1995, 61:1987-1995.
21. Pereg-Gerk L., Paquelin A., Gounon P., Kennedy I.R., Elmerich C. A transcriptional regulator of the LuxR-UhpA family, FlcA, controls flocculation and wheat root surface colonization by Azospirillum brasilense Sp7. Mol Plant-Microbe Interact 1998, 11:177-187.
22. Bible A., Stephens B., Ortega D., Zhihong X., Alexandre G. Function of a chemotaxis-like signal transduction pathway in modulating motility, cell clumping and cell length in the alpha-proteobacterium Azospirillum brasilense. J Bacteriol 2008, 1-11.
23. Russell M.H., Bible A.N., Fang X., Gooding J.R., Campagna S.R., Gomelsky M., et al. Integration of the second messenger c-di-GMP into the chemotactic signaling pathway. mBio 2013, 4(2):e00001-e000013. 10.1128/mBio.00001-13.
24. Arruebarrena Di Palma A., Pereyra C., Moreno Ramírez L., Xiqui Vázquez M.L., Baca B.E., Pereyra M.A., et al. Denitrification derived nitric oxide modulates biofilm formation in Azospirillum brasilense. FEMS Microbiol Lett 2013, 338:77-85.
25. Sambrook J., Fritsch E.F., Maniatis T. Molecular cloning. A laboratory manual 1989, Cold Spring Harbour Laboratory Press, Cold Spring Harbor, NY, USA.
26. Zimmer W., Aparicio C., Elmerich C. Relation between tryptophan synthesis and indole-3-acetic acid production in Azospirillum: identification and sequencing of a trpGDC cluster. Mol Gen Genet 1991, 229:41-51.
27. Simon R., Priefer U., Pühler A. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Nat/Biotechnol 1983, 1:784-791.
28. Spiers A.J., Bohannon J., Gehrig S., Rainey P.B. Colonisation of the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose. Mol Microbiol 2003, 50:15-27.
29. Bloemberg G.V., Wijfjes A.H.M., Lamers G.E.M., Stuurman N., Lugtenberg B.J.J. Simultaneous imaging of Pseudomonas fluorescens WCS365 populations expressing three different autofluorescent proteins in the rhizosphere new perspectives for studying microbial communities. Mol Plant Microb Interact 2000, 13:1170-1176.
30. Okshevsky M., Meyer R.L. Evaluation of fluorescents stains for visualizing extracellular DNA biofilms. J Microbiol Methods 2014, 105:102-104.
31. Riccardi C., Nicoletti I. Analysis of apoptosis by propidium iodine staining and flow cytometry. Nat Protoc 2006, 1458-1461.
32. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
33. Henry J.T., Crosson S. Ligand-binding PAS domains in a genomic, cellular, and structural context. Ann Rev Microbiol 2011, 65:261-286.
34. Wassmann P., Chan C., Paul R., Beck A., Heerklotz H., Jenal U., et al. Structure of BeF3-modified response regulator PleD: implications for diguanylate cyclase activation, catalysis, and feedback inhibition. Structure 2007, 15:915-927.
35. Möglich A., Ayers R.A., Moffat K. Structure and signaling mechanism of Per-ARNT-Sim domains. Structure 2009, 10.1016/j.str.2009.08.011.
36. Chan C., Paul R., Samoray D., Amiot N.C., Giese B., Jenal U., et al. Structural basis of activity and allosteric control of diguanylate cyclase. Proc Natl Acad Sci U S A 2004, 101:17084-17089.
37. Paul R., Abel S., Wassmann P., Beck A., Heerklotz H., Jenal U. Activation of diguanylate cyclase by phosphorylation-mediate dimerization. J Biol Chem 2007, 282:29170-29177.
38. Malone J.G., Williams R., Christen M., Jenal U., Spiers A.J., Rainer P.B. The structure-function relationship of WspR, a Pseudomonas fluorescens response regulator with a GGDEF output domain. Microbiology 2007, 153:980-994.
39. Qi Y., Rao F., Luo Z., Liang Z.X. A flavin cofactor-binding PAS domain regulates c-di-GMP synthesis in AxDGC2 from Acetobacter xylinum. Biochemistry 2009, 48:10275-10285. 10.1021/bi901121w.
40. Gao S., Romdhane S.B., Beullens S., Kaever V., Lambrichts I., Fauvart M., et al. Genomic analysis of cyclic-di-GMP-related genes in rhizobial type strains and functional analysis in Rhizobium etli. Appl Microbiol Biotechnol 2014, 98:4589-4602. 10.1007/s00253-014-5722-7.
41. Friedman L., Kolter R. Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J Bacteriol 2004, 186:4457-4465.
42. Burdman S., Jurkevitch E., Soria-Díaz M.E., Gil-Serrano A.M., Okon Y. Extracellular polysaccharide composition of Azospirillum brasilense and its relation with cell aggregation. FEMS Microbiol Lett 2000, 189:259-264.
43. Okshevsky M., Meyer R.L. The role of extracellular DNA in the establishment, maintenance, and perpetuation of bacterial biofilms. Crit Rev Microbiol 2013, 10.3109/1040841X.2013.841639.
44. Blatny J.M., Brautaset T., Winther-Larsen H., et al. Construction and use of a versatile set of broad-host-range cloning and expression vectors based on the RK2 replicon. Appl Environ Microbiol 1997, 63:370-379.
45. Ditta G., Schmidhauser T., Yakobson E., Lu P., Liang X.W., Finlay D.R., et al. Plasmids related the broad host range vector pRK290, useful for gene cloning and for monitoring gene expression. Plasmid 1985, 13:149-153.