Metabolic engineering of ammonium release for nitrogen-fixing multispecies microbial cell-factories

Metabolic Engineering

Volumn 23, Issue , 2014, Pages 154-164

  Ortiz Marquez, Juan Cesar Federico ^a,b   Do Nascimento, Mauro ^a,b   Curatti, Leonardo ^a,b  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b Fundacion para Investigaciones Biologicas Aplicadas   (Argentina)

Author keywords

Ammonium excretion; Fertilizer; Microalgae biomass; Nitrogen assimilation; Nitrogen fixation; Synthetic consortia

Indexed keywords

ALGAE; AMINO ACIDS; BACTERIA; CELLS; CYTOLOGY; FERTILIZERS; GENE EXPRESSION; NITROGEN; NITROGEN FERTILIZERS;

AMMONIUM EXCRETION; BIOLOGICAL NITROGEN FIXATIONS; HOMEOSTATIC CONTROL; LIMITING CONDITION; METABOLIC PATHWAYS; MICRO-ALGAE; NITROGEN ASSIMILATION; SYNTHETIC CONSORTIUM;

NITROGEN FIXATION;

AMMONIA; GLUTAMATE AMMONIA LIGASE; NITROGEN;

ARTICLE; AZOTOBACTER VINELANDII; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM ISOLATION; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE EXPRESSION; GENE MUTATION; METABOLIC ENGINEERING; MICROALGA; NITROGEN FIXATION; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; ENZYME ACTIVE SITE; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIAL CONSORTIUM; PROCEDURES;

AMMONIA; AZOTOBACTER VINELANDII; CATALYTIC DOMAIN; GLUTAMATE-AMMONIA LIGASE; METABOLIC ENGINEERING; MICROALGAE; MICROBIAL CONSORTIA; NITROGEN FIXATION; POINT MUTATION;

EID: 84898925668     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2014.03.002     Document Type: Article

References (44)

1. 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(5):1711-1718.
2. Barnes E.M., Zimniak P., Jayakumar A. Role of glutamine synthetase in the uptake and metabolism of methylammonium by Azotobacter vinelandii. J. Bacteriol. 1983, 156(2):752-757.
3. Beatty P.H., Good A.G. Future prospects for cereals that fix nitrogen. Science 2011, 333(6041):416-417.
4. Brennan L., Owende P. Biofuels from microalgae: a review of technologies for production, processing, and extractions of biofuels and co-products. Renew. Sustain. Energy Rev. 2010, 14(2):557-577.
5. Brewin B., Woodley P., Drummond M. The basis of ammonium release in nifl mutants of Azotobacter vinelandii. J. Bacteriol. 1999, 181(23):7356-7362.
6. Charpentier M., Oldroyd G. How close are we to nitrogen-fixing cereals?. Curr. Opin. Plant Biol. 2010, 13(5):556-564.
7. Chisti Y. Constraints to commercialization of algal fuels. J. Biotechnol. 2013, 167(3):201-214.
8. Colnaghi R., Green A., He L., Rudnick P., Kennedy C. Strategies for increased ammonium production in free-living or plant associated nitrogen fixing bacteria. Plant Soil 1997, 194(1-2):145-154.
9. Colnaghi R., Rudnick P., He L., Green A., Yan D., Larson E., Kennedy C. Lethality of glnD null mutations in Azotobacter vinelandii is suppressible by prevention of glutamine synthetase adenylylation. Microbiology 2001, 147(5):1267-1276.
10. Crespo J.L., Guerrero M.G., Florencio F.J. Mutational analysis of Asp51 of Anabaena azollae glutamine synthetase. D51E mutation confers resistance to the active site inhibitors l-methionine-DL-sulfoximine and phosphinothricin. Eur. J. Biochem. 1999, 266(3):1202-1209.
11. 2O release from agro-biofuel production negates global warming reduction by replacing fossil fuels. Atmos. Chem. Phys. 2007, 7(4):11191-11205.
12. Curatti L., Brown C.S., Ludden P.W., Rubio L.M. Genes required for rapid expression of nitrogenase activity in Azotobacter vinelandii. Proc. Natl. Acad. Sci. 2005, 102(18):6291-6296.
13. Do Nascimento M., Ortiz-Marquez J.C.F., Sanchez-Rizza L., Echarte M.M., Curatti L. Bioprospecting for fast growing and biomass characterization of oleaginous microalgae from South-Eastern Buenos Aires, Argentina. Bioresour. Technol. 2012, 125:283-290.
14. Dixon R., Kahn D. Genetic regulation of biological nitrogen fixation. Nat. Rev. Microbiol. 2004, 2(8):621-631.
15. Gong Y., Hu H., Gao Y., Xu X., Gao H. Microalgae as platforms for production of recombinant proteins and valuable compounds: progress and prospects. J. Ind. Microbiol. Biotechnol. 2011, 38(12):1879-1890.
16. Hulatt C., Thomas D. Dissolved organic matter in microalgal photobioreactors: a potential loss in solar energy conversion?. Bioresour. Technol. 2010, 101(22):8690-8697.
17. Kleinschmidt J.A., Kleiner D. The glutamine synthetase from Azotobacter vinelandii: purification, characterization, regulation and localization. Eur. J. Biochem. 1978, 89(1):51-60.
18. Liaw S.H., Eisenberg D. Structural model for the reaction mechanism of glutamine synthetase, based on five crystal structures of enzyme-substrate complexes. Biochemistry 1994, 33(3):675-681.
19. Liaw S.H., Jun G., Eisenberg D. Interactions of nucleotides with fully unadenylylated glutamine synthetase from Salmonella typhimurium. Biochemistry 1994, 33(37):11184-11188.
20. Liaw S.-H., Kuo I., Eisenberg D. Discovery of the ammonium substrate site on glutamine synthetase, a third cation binding site. Protein Sci. 1995, 4(11):2358-2365.
21. Martínez-Noël G., Curatti L., Hernandez J.A., Rubio L.M. NifB and NifEN protein levels are regulated by ClpX2 under nitrogen fixation conditions in Azotobacter vinelandii. Mol. Microbiol. 2011, 79(5):1182-1193.
22. Miller S.A. Minimizing land use and nitrogen intensity of bioenergy. Environ. Sci. Technol. 2010, 44(10):3932-3939.
23. Nelson N. A photometric adaptation of the Somogyi method for the determination of glucose. J. Biol. Chem. 1944, 153(2):375-379.
24. Oldroyd G.E., Dixon R. Biotechnological solutions to the nitrogen problem. Curr. Opin. Biotechnol. 2014, 26:19-24.
25. Olguín E.J. Dual purpose microalgae-bacteria-based systems that treat wastewater and produce biodiesel and chemical products within a Biorefinery. Biotechnol. Adv. 2012, 30(5):1031-1046.
26. Ortiz-Marquez J.C.F., Do Nascimento M., Dublan M.D., Curatti L. Association with an ammonium-excreting bacterium allows diazotrophic culture of oil-rich eukaryotic microalgae. Appl. Environ. Microbiol. 2012, 78(7):2345.
27. Ortiz-Marquez J.C.F., Do Nascimento M., Zehr J.P., Curatti L. Genetic engineering of multi-species microbial cell-factories as an alternative for bioenergy production. Trends Biotechnol. 2013, 31(9):521-529.
28. Peccia J., Haznedaroglu B., Gutierrez J., Zimmerman J.B. Nitrogen supply is an important driver of sustainable microalgae biofuel production. Trends Biotechnol. 2013, 31(3):621-639.
29. Raymond J., Siefert J.L., Staples C.R., Blankenship R.E. The natural history of nitrogen fixation. Mol. Biol. Evol. 2004, 21(3):541-554.
30. Rippka R., Deruelles J., Waterbury J.B., Herdman M., Stainer R.Y. Genetic assignments, strain histories and properties of pure culture of cyanobacteria. J. Gen. Microbiol. 1979, 111(1):1-61.
31. Rubio L.M., Ludden P.W. Biosynthesis of the iron-molybdenum cofactor of nitrogenase. Annu. Rev. Microbiol. 2008, 62:93-111.
32. Sambrook R. Molecular Cloning: A Laboratoty Manual 2001, Cold spring Harbor Laboratory Press, Cold Spring Harbor, NY. 3rd ed.
33. Sayer J., Cassman K.G. Agricultural innovation to protect the environment. Proc. Natl. Acad. Sci. 2013, 110(21):8345-8348.
34. Setubal J.C., Dos Santos P., Goldman B.S., Ertesvâg H., Espin G., Rubio L.M., Valla S., Almeida N.F., Balasubramanian D., Cromes L., Curatti L., Du Z., Godsy E., Goodner B., Hellner-Burris K., Hernandez J.A., Houmiel K., Imperial J., Kennedy C., Larson T.J., Latreille P., Ligon L.S., Lu J., Mærk M., Miller N.M., Norton S., O'Carroll I.P., Paulsen I., Raulfs E.C., Roemer R., Rosser J., Segura D., Slater S., Stricklin S.L., Studholme D.J., Sun J., Viana C.J., Wallin E., Wang B., Wheeler C., Zhu H., Dean D.R., 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.
35. Shapiro B.M., Stadtman E.R. Glutamine synthetase (Escherichia coli). Methods Enzymol. 1970, 17:910-922.
36. Stadtman E.R., Smyrniotis P.Z., Davis J.N., Wittenberger M.E. Enzymic procedures for determining the average state of adenylylation of Escherichia coli glutamine synthetase. Anal. Biochem. 1979, 95(1):275-285.
37. Strandberg G.W., Wilson P.W. Formation of the nitrogen-fixing enzyme system in Azotobacter vinelandii. Can J. Microbiol. 1968, 14(1):25-31.
38. Temme K., Zhao D., Voigt C.A. Refactoring the nitrogen fixation gene cluster from Klebsiella oxytoca. Proc. Natl. Acad. Sci. 2012, 109(18):7085-7090.
39. Wang X., Yang J.G., Chen L., Wang J.L., Cheng Q., Dixon R., Wang Y.P. Using synthetic biology to distinguish and overcome regulatory and functional barriers related to nitrogen fixation. PloS One 2013, 8(7):e68677.
40. Watanabe K., Imase M., Aoyagi H., Ohmura N., Saiki H., Tanaka H. Development of a novel artificial medium based on utilization of algal photosynthetic metabolites by symbiotic heterotrophs. J. Appl. Microbiol. 2008, 105(3):741-751.
41. Wernick D.G., Liao J.C. Protein-based biorefining: metabolic engineering for production of chemicals and fuel with regeneration of nitrogen fertilizers. Appl. Microbiol. Biotechnol. 2013, 97(4):1397-1406.
42. Wijffels R.H., Kruse O., Hellingwerf K.J. Potential of industrial biotechnology with cyanobacteria and eukaryotic microalgae. Curr. Opin. Biotechnol. 2013, 24(3):405-413.
43. 2-fixing Azotobacter vinelandii. App. Environ. Microbiol. 1988, 54(2):473-475.
44. Zehr J.P. Interactions with partners are key for oceanic nitrogen-fixing cyanobacteria: ocean-dwelling cyanobacteria associate with a variety of other microorganisms, including those that are photosynthetic. Microbe 2013, 8:117-122.