Alginate synthesis in Azotobacter vinelandii is increased by reducing the intracellular production of ubiquinone

Applied Microbiology and Biotechnology

Volumn 97, Issue 6, 2013, Pages 2503-2512

  Núñez, Cinthia ^a   Peña, Carlos ^a   Kloeckner, Wolf ^b   Hernández Eligio, Alberto ^a   Bogachev, Alexander V ^c   Moreno, Soledad ^a   Guzmán, Josefina ^a   Büchs, Jochen ^b   Espín, Guadalupe ^a  

^a INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

^b RWTH AACHEN UNIVERSITY   (Germany)

^c MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

algD expression; Alginate; Azotobacter vinelandii; Gene regulation; Respirometric analysis; Ubiquinone

Indexed keywords

ALGD EXPRESSION; AZOTOBACTER VINELANDII; EXPRESSION LEVELS; GENETIC COMPLEMENTATION; INTRACELLULAR PRODUCTION; RESPIROMETRIC ANALYSIS; REVERSE TRANSCRIPTION PCR; UBIQUINONE;

BIOCHEMISTRY; BIOSYNTHESIS; GENE ENCODING; GENE EXPRESSION; GENE EXPRESSION REGULATION; NITROGEN FIXATION; TRANSCRIPTION;

ALGINATE;

ALGINIC ACID; UBIQUINONE;

BACTERIUM; GENE EXPRESSION; GROWTH RATE; MUTATION; NITROGEN FIXATION; POLYMERASE CHAIN REACTION; POLYSACCHARIDE; QUANTITATIVE ANALYSIS; REAL TIME; SOIL MICROORGANISM;

ARTICLE; AZOTOBACTER VINELANDII; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM MUTANT; CHEMICAL ANALYSIS; GENE CONTROL; GENE EXPRESSION; GENE LOCUS; GENE SEQUENCE; GENETIC TRANSCRIPTION; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; REPRODUCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNTHESIS; WILD TYPE;

ALGINATES; AZOTOBACTER VINELANDII; BIOSYNTHETIC PATHWAYS; CULTURE MEDIA; DNA TRANSPOSABLE ELEMENTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC COMPLEMENTATION TEST; GLUCURONIC ACID; HEXURONIC ACIDS; MUTAGENESIS, INSERTIONAL; NITROGEN FIXATION; REAL-TIME POLYMERASE CHAIN REACTION; UBIQUINONE;

AZOTOBACTER VINELANDII; BACTERIA (MICROORGANISMS);

EID: 84878863667     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-012-4329-0     Document Type: Article

References (46)

1. Alexeyev MF, Shokolenko IN, Croughan TP (1995) Improved antibiotic-resistance gene cassettes and omega elements for Escherichia coli vector construction and in vitro deletion/insertion mutagenesis. Gene 160:63-67
2. Anderlei T, Büchs J (2001) Device for sterile online measurement of the oxygen transfer rate in shaking flasks. Biochem Eng J 7:157-162
3. Anderlei T, Zang W, Büchs J (2004) Online respiration activity measurements (OTR, CTR, RQ) in shake flasks. Biochem Eng J 17:187-194
4. Bali A, Blanco G, Hill S, Kennedy C (1992) Excretion of ammonium by a nifL mutant of Azotobacter vinelandii fixing nitrogen. Appl Environ Microbiol 58:1711-1718
5. Barry T, Geary S, Hannify S, MacGearailt C, Shalloo M, Heery D, Gannon F, Powell R (1992) Rapid mini-preparations of total RNA from bacteria. Nucleic Acids Res 20:4940
6. Bekker M, Alexeeva S, Laan W, Sawers G, Teixeira de Mattos J, Hellingwerf K (2009) The ArcBA two-component system of Escherichia coli is regulated by the redox state of both the ubiquinone and the menaquinone pool. J Bacteriol 192:746-754
7. Bertsova YV, Bogachev AV, Skulachev VP (1998) Two NADH:ubiquinone oxidoreductases of Azotobacter vinelandii and their role in the respiratory protection. Biochim Biophys Acta 1363:125-133
8. Bertsova YV, Bogachev AV, Skulachev VP (2001) Noncoupled NADH:ubiquinone oxidoreductase of Azotobacter vinelandii is required for diazotrophic growth at high oxygen concentrations. J Bacteriol 183:6869-6874
9. Campos M, Martinez-Salazar JM, Lloret L, Moreno S, Núñez C, Espín G, Soberón-Chávez G (1996) Characterization of the gene coding for GDP-mannose dehydrogenase (algD) from Azotobacter vinelandii. J Bacteriol 178:1793-1799
10. Castañeda M, Guzmán J, Moreno S, Espín G (2000) The GacS sensor kinase regulates alginate and poly-b-hydroxybutyrate production in Azotobacter vinelandii. J Bacteriol 182:2624-2628
11. s form part of a cascade that controls alginate production in Azotobacter vinelandii. J Bacteriol 183:6787-6793
12. Dalton H, Postgate JR (1968) Effect of oxygen on growth of Azotobacter chroococcum in batch and continuous cultures. J Gen Microbiol 54:463-473
13. Díaz-Barrera A, Peña C, Galindo E (2007) The oxygen transfer rate influences the molecular mass of the alginate produced by Azotobacter vinelandii. Appl Microbiol Biotechnol 76:903-910
14. Galindo E, Peña C, Núñez C, Segura D, Espín G (2007) Molecular and bioengineering strategies to improve alginate and polydydroxyalkanoate production by Azotobacter vinelandii. Microb Cell Fact 6:7
15. Georgellis D, Kwon O, Lin EC (2001) Quinones as the redox signal for the arc two-component system of bacteria. Science 292:2314-2316
16. Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557-580
17. Hay ID, Rehman ZU, Ghaffor A, Rehm BH (2010) Bacterial biosynthesis of alginates. J Chem Technol Biotechnol 85:752-759
18. Hernández RM, Orive G, Murua A, Pedraz JL (2010) Microcapsules and microcarriers for in situ cell delivery. Adv Drug Deliv Rev 62:711-730
19. Kennedy C, Gamal R, Hummprey R, Ramos J, Brigle K, Dean D (1986) The nifH, nifM, and NifN genes of Azotobacter vinelandii: characterization by Tn5 mutagenesis and isolation from pLARF1 gene bank. Mol Gen Genet 205:318-325
20. Klimek J, Ollis D (1980) Extracellular microbial polysaccharides: kinetics of Pseudomonas sp. Azotobacter vinelandii, and Aureobasidium pullulans batch fermentations. Biotechnol Bioeng 22:2321-2342
21. Knutson CA, Jeanes A (1968) A new modification of the carbazole analysis: application to heteropolysaccharides. Anal Biochem 24:470-481
22. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, Roop RM 2nd, Peterson KM (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176
23. Larsen B, Haug A (1971) Biosynthesis of alginate. 1. Composition and structure of alginate produced by Azotobacter vinelandii (Lipman). Carbohydr Res 17:287-296
24. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275
25. Malpica R, Sandoval GR, Rodriguez C, Franco B, Georgellis D (2006) Signaling by the arc two-component system provides a link between the redox state of the quinone pool and gene expression. Antioxid Redox Signal 8:781-795
26. Manzo J, Cocotl-Yañez M, Tzontecomani T, Martínez VM, Bustillos R, Velasquez C, Goiz Y, Solis LY, López L, Fuentes LE, Núñez C, Segura D, Espín G, Castañeda M (2012) Post-transcriptional regulation of the alginate biosynthetic gene algD by the Gac/Rsm system in Azotobacter vinelandii. J Mol Microb Biotechnol 21:147-159
27. Martínez-Salazar JM, Moreno S, Nájera R, Boucher JC, Espín G, Soberón-Chávez G, Deretic V (1996) Characterization of the genes coding for the putative sigma factor AlgU and its regulators MucA, MucB, MucC, and MucD in Azotobacter vinelandii and evaluation of their roles in alginate biosynthesis. J Bacteriol 178:1800-1808
28. Mejía-Ruiz H, Guzmán J, Moreno S, Soberón- Chávez G, Espín G (1997) The Azotobacter vinelandii alg8 and alg44 genes are essential for alginate synthesis and can be transcribed from an algD-independent promoter. Gene 199:271-277
29. Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Sping Harbor
30. Núñez C, León R, Guzmán J, Espín G, Soberón-Chávez G (2000a) Role of Azotobacter vinelandii mucA and mucC gene products in alginate production. J Bacteriol 182:6550-6556
31. Núñez C, Moreno S, Cárdenas L, Soberón- Chávez G, Espín G (2000b) Inactivation of the ampDE operon increases transcription of algD and affects morphology and encystment of Azotobacter vinelandii. J Bacteriol 182:4829-4835
32. +-translocating NADH:ubiquinone oxidoreductase of Azotobacter vinelandii negatively regulates alginate synthesis. Microbiology 155:249-256
33. Oelze J (2000) Respiratory protection of nitrogenase in Azotobacter species: is a widely held hypothesis unequivocally supported by experimental evidence? FEMS Microbiol Rev 24:321-333
34. Page WJ, Knosp O (1989) Hyperproduction of poly-beta-hydroxybutyrate during exponential growth of Azotobacter vinelandii UWD. Appl Environ Microbiol 55:1334-1339
35. Peña C, Galindo E, Büchs J (2011) The viscosifying power, degree acetylation and molecular mass of the alginate produced by Azotobacter vinelandii in shake flasks are determined by the oxygen transfer rate. Proc Biochem 46:290-297
36. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor
37. Segura D, Guzmán J, Espín G (2003) Azotobacter vinelandii mutants that overproduce poly-beta-hydroxybutyrate or alginate. Appl Microbiol Biotechnol 63:159-163
38. Senior PJ, Beech GA, Ritchie GA, Dawes EA (1972) The role of oxygen limitation in the formation of poly-ß-hydroxybutyrate during batch and continuous culture of Azotobacter beijerinckii. Biochem J 128:1193-1201
39. Setubal JC, dos Santos P, Goldman BS, Ertesvåg H, Espín 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, Mærk 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 CV, Wallin E, Wang B, Wheeler C, Zhu H, Dean DR, Dixon R, Wood D (2009) Genome sequence of Azotobacter vinelandii, an obligate aerobe specialized to support diverse anaerobic metabolic processes. J Bacteriol 191:4534-4545
40. Shestopalov AI, Bogachev AV, Murtazina RA, Viryasov MB, Skulachev VP (1997) Aeration-dependent changes in composition of the quinone pool in Escherichia coli. Evidence of post-transcriptional regulation of the quinone biosynthesis. FEBS Lett 404:272-274
41. Skjak-Braek G, Grasdalen H, Larsen B (1986) Monomer sequence and acetylation pattern in some bacterial alginates. Carbohydr Res 154:239-250
42. Soballe B, Poole RK (1999) Microbial ubiquinones: multiple roles in respiration, gene regulation and oxidative stress management. Microbiology 145:1817-1830
43. Vázquez A, Moreno S, Guzmán J, Alvarado A, Espín G (1999) Transcriptional organization of the Azotobacter vinelandii algGXLVIFA genes: characterization of algF mutants. Gene 232:217-222
44. Wallace BJ, Young IG (1977) Role of quinones in electron transport to oxygen and nitrate in Escherichia coli. Studies with a ubiA-menA- double quinone mutant. Biochim Biophys Acta 461:84-100
45. Wilson KJ, Sessitsch A, Corbo JC, Giller KE, Akkermans AD, Jefferson RA (1995) ß-Glucuronidase (GUS) transposons for ecological and genetic studies of rhizobia and other gram-negative bacteria. Microbiology 141:1691-1705
46. Wu G, Williams HD, Gibson F, Poole RK (1993) Mutants of Escherichia coli affected in respiration: the cloning and nucleotide sequence of ubiA, encoding the membrane-bound p-hydroxybenzoate:octaprenyl transferase. J Gen Microbiol 139:1795-1805