Post-transcriptional regulation of the alginate biosynthetic gene algD by the Gac/Rsm system in azotobacter vinelandii

Journal of Molecular Microbiology and Biotechnology

Volumn 21, Issue 3-4, 2011, Pages 147-159

  Manzo, Joaquín ^a   Cocotl Yañez, Miguel ^a,b   Tzontecomani, Tomás ^a   Martínez, Verónica M ^a   Bustillos, Rocío ^a   Velásquez, Claudia ^a   Goiz, Yolanda ^a   Solís, Yuri ^a   López, Liliana ^a   Fuentes, Luis E ^a   Nuñez, Cinthia ^b   Segura, Daniel ^b   Espín, Guadalupe ^b   Castañeda, Miguel ^a  

^a BENEMÉRITA UNIVERSIDAD AUTÓNOMA DE PUEBLA   (Mexico)

^b INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

Author keywords

algD; Alginate; Azotobacter; GacS A; RsmA Z Y

Indexed keywords

ALGINIC ACID; MESSENGER RNA;

ARTICLE; AZOTOBACTER VINELANDII; BACTERIAL GENE; BACTERIAL GENOME; BIOSYNTHESIS; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION; GENE OVEREXPRESSION; IN VITRO STUDY; NONHUMAN; PROTEIN INTERACTION; TRANSCRIPTION REGULATION;

AZOTOBACTER; AZOTOBACTER VINELANDII; BACTERIA (MICROORGANISMS); GAMMAPROTEOBACTERIA;

EID: 84856493466     PISSN: 14641801     EISSN: 16602412     Source Type: Journal    
DOI: 10.1159/000334244     Document Type: Article

References (58)

1. Aarons S, Abbas A, Adams C, Fenton A, O'Gara F: A regulatory RNA (PrrB RNA) modulates expression of secondary metabolite genes in Pseudomonas fluorescens F113. J Bacteriol 2000;14:3913-3919.
2. Alexeyev MF, Shokolenko IN, Croughan TP: Improved antibiotic-resistance gene cassettes and omega elements for Escherichia coli vector construction and in vitro deletion/insertion mutagenesis. Gene 1995;160:63-67.
3. Bagdasarian M, Lurz R, Ruckert B, Franklin FC, Bagdasarian MM, Frey J, Timmis KN: Specificpurpose plasmid cloning vectors. II. Broad host range, high copy number, RSF1010-derived vectors, and a host-vector system for gene cloning in Pseudomonas. Gene 1981;16:237-247.
4. Baker CS, Eöry LA, Yakhnin H, Mercante J, Romeo T, Babitzke P: CsrA inhibits translation initiation of Escherichia coli hfq by binding to a single site overlapping the Shine-Dalgarno sequence. J Bacteriol 2007;189:5472-5481.
5. Bali A, Blanco G, Hill S, Kennedy C: Excretion of ammonium by a nifL mutant of Azotobacter vinelandii fixing nitrogen. Appl Environ Microbiol 1992;58:1711-1718.
6. Blatny JM, Brautaset T, Winther-Larsen HC, Haugan K, Valla S: 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.
7. Blumenkrantz N, Asboe-Hansen G: New method for quantitative determination of uronic acids. Anal Biochem 1973;54:484-489.
8. Brencic A, Lory S: Determination of the regulon and identification of novel mRNA targets of Pseudomonas aeruginosa RsmA. Mol Microbiol 2009;72:612-632.
9. Brosius J, Ullrich A, Raker MA, Gray A, Dull TJ, Gutell RR, Noller HF: Construction and fine mapping of recombinant plasmids containing the rrnB ribosomal RNA operon of Escherichia coli. Plasmid 1981;6:112-118.
10. Burrowes E, Baysse C, Adams C, O'Gara F: Influence of the regulatory protein RsmA on cellular functions in Pseudomonas aeruginosa PAO1, as revealed by transcriptome analysis. Microbiology 2006;152:405-418.
11. Campos ME, Martínez-Salazar J, Lloret L, Núñez C, Espín G, Soberón-Chávez G: Characterization of the gene coding for GDP-mannose dehydrogenase (algD) from Azotobacter vinelandii. J Bacteriol 1996;178:1793-1799.
12. Castañeda M, Guzmán J, Moreno S, Espín G: The GacS sensor kinase regulates alginate and polyhydroxybutyrate production in Azotobacter vinelandii. J Bacteriol 2000;182:2624-2628.
13. Castañeda M, Sánchez J, Moreno S, Núñez C, Espín G: The global regulators GacA and aσ s form part of a cascade that controls alginate production in Azotobacter vinelandii. J Bacteriol 2001;183:6787-6793.
14. Clementi F: Alginate production by Azotobacter vinelandii. Crit Rev Biotech 1997;17:327-361.
15. Cui Y, Chatterjee A, Chatterjee AK: Effects of the two-component system comprising GacA and GacS of Erwinia carotovora subsp. carotovora on the production of global regulatory rsmB RNA, extracellular enzymes, and harpin Ecc. Mol Plant-Microbe Interact 2001;14:516-526.
16. Dubey AK, Baker CS, Romeo T, Babitzke P: RNA sequence and secondary structure participate in high-affinity CsrA-RNA interaction. RNA 2007;11:1579-1587.
17. Fortune DR, Suyemoto M, Altier C: Identification of CsrC and characterization of its role in epithelial cell invasion in Salmonella enterica serovar Typhimurium. Infect Immun 2006;74:331-339.
18. Galindo E, Peña C, Núñez C, Segura D, Espín G: Molecular and bioengineering strategies to improve alginate and polyhydroxyalkanoate production by Azotobacter vinelandii. Microb Cell Fact 2007;6:7-21.
19. Gaona G, Núñez C, Goldberg JB, Linford AS, Nájera R, Castañeda M, Guzmán J, Espín G, Soberón-Chávez G: Characterization of the Azotobacter vinelandii algC gene involved in alginate and lipopolysaccharide production. FEMS Microbiol Lett 2004;238:199-206.
20. Heeb S, Haas D: Regulatory roles of the GacS/GacA two component system in plant-associated and other Gram-negative bacteria. Mol Plant-Microbe Interact 2001;14:1351-1363.
21. Heeb S, Blumer C, Haas D: Regulatory RNA as mediator in GacA/RsmA-dependent global control of exoproduct formation in Pseudomonas fluorescens CHA0. J Bacteriol 2002;184:1046-1056.
22. Heurlier K, Williams F, Heeb S, Dormond C, Pessi G, Singer D, Cámara M, Williams P, Haas D: Positive control of swarming, rhamnolipid synthesis, and lipase production by the posttranscriptional RsmA/RsmZ system in Pseudomonas aeruginosa PAO1. J Bacteriol 2004;186:2936-2945.
23. Humair B, Wackwitz B, Haas D: GacA-controlled activation of promoters for small RNA genes in Pseudomonas fluorescens. Appl Environ Microbiol 2010;76:1497-1506.
24. Kay E, Dubuis C, Haas D: Three small RNAs jointly ensure secondary metabolism and biocontrol in Pseudomonas fluorescens CHA0. Proc Natl Acad Sci USA 2005;102:17136-17141.
25. Kay E, Humair B, Denervaud V, Riedel K, Spahr S, Eberl L, Valverde CV, Haas D: Two GacAdependent small RNAs modulate the quorumsensing response in Pseudomonas aeruginosa. J Bacteriol 2006;188:6026-6033.
26. Kennedy C, Gamal R, Humphrey R, Ramos J, Brigle K, Dean D: The nifH, nifM, and nifN genes of Azotobacter vinelandii: characterization by Tn5 mutagenesis and isolation from pLARF1 gene banks. Mol Gen Genet 1986;205:318-325.
27. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, Roop II RM, Peterson KM: Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 1995;166:175-176.
28. Lapouge K, Schubert M, Allain FH, Haas D: Gac/Rsm signal transduction pathway of gammaproteobacteria: from RNA recognition to regulation of social behaviour. Mol Microbiol 2008;67:241-253.
29. Lapouge K, Sineva E, Lindell M, Starke K, Baker CS, Babitzke P, Haas D: Mechanism of hcnA mRNA recognition in the Gac/Rsm signal transduction pathway of Pseudomonas fluorescens. Mol Microbiol 2007;66:341-356.
30. Larsen B, Haug A: Biosynthesis of alginate. 1. Composition and structure of alginate produced by Azotobacter vinelandii. Carbohydr Res 1971;17:287-296.
31. Lenz DH, Miller MB, Zhu J, Kulkarni RV, Bassler BL: CsrA and three redundant small RNAs regulate quorum sensing in Vibrio cholerae. Mol Microbiol 2005;58:1186-1202.
32. Lin LP, Sadoff HA: Chemical composition of Azotobacter vinelandii cysts. J Bacteriol 1969;100:480-486.
33. Liu MY, Gui G, Wei B, Preston III JF, Oakford L, Yuksel U, Giedroc DP, Romeo T: The RNA molecule CsrB binds to the global regulatory protein CsrA and antagonizes its activity in Escherichia coli. J Biol Chem 1997;272:17502-17510.
34. Liu MY, Yang H, Romeo T: The product of the pleiotropic Escherichia coli gene csrA modulates glycogen biosynthesis via effects on mRNA stability. J Bacteriol 1995;177:2663-2672.
35. Lloret L, Barreto R, León R, Moreno S, Martínez-Salazar J, Espín G, Soberón-Chávez G: Genetic analysis of the transcriptional arrangement of Azotobacter vinelandii alginate biosynthetic genes: identification of two independent promoters. Mol Microbiol 1996;21:449-457.
36. Martínez-Salazar J, Moreno S, Nájera R, Boucher JC, Espín G, Soberón-Chávez G, Deretic V: Characterization of the genes coding for the putative sigma factor AlgU and its negative regulators MucA, MucB, MucC, and MucD in Azotobacter vinelandii and evaluation of their role in alginate biosynthesis. J Bacteriol 1996;178:1800-1808.
37. Mejía-Ruíz H, Guzmán J, Moreno S, Soberón-Chávez, G Espín: The Azotobacter vinelandii alg8 and alg44 genes are essential for alginate synthesis and can be transcribed from an algD-independent promoter. Gene 1997a; 199:271-277.
38. Mejía-Ruíz H, Moreno S, Guzmán J, Nájera R, León R, Soberón-Chávez G, Espín G: Isolation and characterization of an Azotobacter vinelandii algK mutant. FEMS Microbiol Lett 1997b; 156:101-106.
39. Mercante J, Edwards AN, Dubey AK, Babitzke P, Romeo T: Molecular geometry of CsrA (RsmA) binding to RNA and its implications for regulated expression. J Mol Biol 2009;392:511-528.
40. Moll S, Schneider DJ, Stodghill P, Myers CR, Cartinhour SW, Filiatrault MJ: Construction of an rsmX co-variance model and identification of five rsmX non-coding RNAs in Pseudomonas syringae pv. tomato DC3000. RNA Biol 2010;7:508-516.
41. Moreno S, Guzmán J, Nájera R, Soberón-Chávez G, Espín G: Role of the alternative σ factor AlgU in encystment of Azotobacter vinelandii. J Bacteriol 1998;180:2766-2769.
42. Nawrocki EP, Kolbe DL, Eddy SR: Infernal 1.0: inference of RNA alignments. Bioinformatics 2009;25:1335-1337.
43. Núñez C, León R, Guzmán J, Espín G, Soberón-Chávez G: Role of Azotobacter vinelandii mucA and mucC gene products in alginate production. J Bacteriol 2000;182:6550-6556.
44. Pessi G, Williams F, Hindle Z, Heurlier K, Holden MTG, Cámara M, Haas D, Williams P: The global posttranscriptional regulator RsmA modulates production of virulence determinants and N-acylhomoserine lactones in Pseudomonas aeruginosa. J Bacteriol 2001;183:6676-6683.
45. Rediers H, Vanderleyden J, De Mot R: Azotobacter vinelandii: a Pseudomonas in disguise? Microbiology 2004;150:1117-1119.
46. Reimmann C, Valverde C, Kay E, Haas D: Posttranscriptional repression of GacS/GacAcontrolled genes by the RNA-binding protein RsmE acting together with RsmA in the biocontrol strain Pseudomonas fluorescens CHA0. J Bacteriol 2005;187:276-285.
47. Sahr T, Brüggemann H, Jules M, Lomma M, Albert-Weissenberger C, Cazalet C, Buchrieser C: Two small ncRNAs jointly govern virulence and transmission in Legionella pneumophila. Mol Microbiol 2009;72:741-762.
48. Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual, ed 2. Cold Spring Harbor, Cold Spring Harbor Laboratory, 1989.
49. Setubal JC, dos Santos P, Goldman BS, Ertesvåg H, Espin G, Rubio LM, Valla S, Almeida NF, Balasubramanian D, Cromes L, Curatti L, Du Z, Godsy E, Goodner B, Hellner-Burris K, Hernandez JA, Houmiel K, Imperial J, Kennedy C, Larson TJ, Latreille P, Ligon LS, Lu J, Maerk M, Miller NM, Norton S, O'Carroll IP, Paulsen I, Raulfs EC, Roemer R, Rosser J, Segura D, Slater S, Stricklin SL, Studholme DJ, Sun J, Viana CJ, Wallin E, Wang B, Wheeler C, Zhu H, Dean DR, Dixon R, Wood D: Genome sequence of Azotobacter vinelandii, an obligate aerobe specialized to support diverse anaerobic metabolic processes. J Bacteriol 2009;191:4534-4545.
50. Suh MH, Pulakat L, Gavini N: Isolation and characterization of nif::kanamycin and nitrogen fixation proficient Azotobacter vinelandii strain, and its implication on the status of multiple chromosomes in Azotobacter. Genetica 2000;110:101-107.
51. Suzuki K, Wang X, Weilbacher T, Pernestig AK, Melefors O, Georgellis D, Babitzke P, Romeo T: Regulatory circuitry of the CsrA/CsrB and BarA/UvrY systems of Escherichia coli. J Bacteriol 2002;184:5130-5140.
52. Teplitski M, Goodier RI, Ahmer BMM: Pathways leading from BarA/SirA to motility and virulence gene expression in Salmonella. J Bacteriol 2003;185:7257-7265.
53. Timmermans J, van Melderen L: Post-transcriptional global regulation by CsrA in bacteria. Cell Mol Life Sci 2010;67:2897-2908.
54. Valverde C, Heeb S, Keel C, and Haas D: RsmY, a small regulatory RNA, is required in concert with RsmZ for GacA-dependent expression of biocontrol traits in Pseudomonas fluorescens CHA0. Mol Microbiol 2003;50:1361-1379.
55. Vázquez A, Moreno S, Guzmán J, Alvarado A, Espín G: Transcriptional organization of the Azotobacter vinelandii algGXLIVFA genes: characterization of algF mutants. Gene 1999;232:217-222.
56. Weilbacher T, Suzuki K, Dubey AK, Wang X, Gudapaty S, Morozov I, Baker CS, Georgellis D, Babitzke P, Romeo T: A novel sRNA component of the carbon storage regulatory system of Escherichia coli. Mol Microbiol 2003;48:657-670.
57. Zuker M, Jacobson AB: Using reliability information to annotate RNA secondary structures. RNA 1998;4:669-679
58. Zuker M, Jaeger JA, Turner DH: A comparison of optimal and suboptimal RNA secondary structure predicted by free energy minimalisation with structures determined by phylogenetic comparison. Nucleic Acids Res 1991;19:2707-2714.