Calvin cycle mutants of photoheterotrophic purple nonsulfur bacteria fail to grow due to an electron imbalance rather than toxic metabolite accumulation

Journal of Bacteriology

Volumn 196, Issue 6, 2014, Pages 1231-1237

  Gordon, Gina C ^a,b   McKinlay, James B ^a  

^a INDIANA UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTRON TRANSPORT; HYDROGEN; MALATES; MUTATION; OXIDATION-REDUCTION; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PHOTOSYNTHESIS; RHODOPSEUDOMONAS; RHODOSPIRILLUM RUBRUM; RIBULOSEPHOSPHATES; SUCCINIC ACID;

EID: 84894317624     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01299-13     Document Type: Article

References (33)

1. Muller FM. 1933. On the metabolism of purple sulphur bacteria in organic media. Arch. Microbiol. 4:131-166.
2. Calvin M. 1962. The path of carbon in photosynthesis: the carbon cycle is a tool for exploring chemical biodynamics and the mechanism of quantum conversion. Science 135:879-889. http://dx.doi.org/10.1126/science.135.3507.879.
3. Richardson DJ, King GF, Kelly DJ, McEwan AG, Ferguson SJ, Jackson JB. 1988. The role of auxiliary oxidants in maintaining redox balance during phototrophic growth of Rhodobacter capsulatus on propionate or butyrate. Arch. Microbiol. 150:131-137. http://dx.doi.org/10.1007/BF00425152.
4. Hillmer P, Gest H. 1977. H2 metabolism in the photosynthetic bacterium Rhodopseudomonas capsulata: H2 production by growing cultures. J. Bacteriol. 129:724-731.
5. Hallenbeck PL, Lerchen R, Hessler P, Kaplan S. 1990. Roles of CfxA, CfxB, and external electron acceptors in regulation of ribulose 1,5-bisphosphate carboxylase/oxygenase expression in Rhodobacter sphaeroides. J. Bacteriol. 172:1736-1748.
6. Falcone DL, Tabita FR. 1991. Expression of endogenous and foreign ribulose 1,5-bisphosphate carboxylase-oxygenase (RubisCO) genes in a RubisCO deletion mutant of Rhodobacter sphaeroides. J. Bacteriol. 173: 2099-2108.
7. Paoli GC, Vichivanives P, Tabita FR. 1998. Physiological control and regulation of the Rhodobacter capsulatus cbb operons. J. Bacteriol. 180: 4258-4269.
8. McKinlay JB, Harwood CS. 2010. Carbon dioxide fixation as a central redox cofactor recycling mechanism in bacteria. Proc. Natl. Acad. Sci. U. S. A. 107:11669-11675. http://dx.doi.org/10.1073/pnas.1006175107.
9. Laguna R, Tabita FR, Alber BE. 2011. Acetate-dependent photoheterotrophic growth and the differential requirement for the Calvin-Benson-Bassham reductive pentose phosphate cycle in Rhodobacter sphaeroides and Rhodopseudomonas palustris. Arch. Microbiol. 193:151-154. http://dx.doi.org/10.1007/s00203-010-0652-y.
10. McKinlay JB, Harwood CS. 2011. Calvin cycle flux, pathway constraints, and substrate oxidation state together determine the H2 biofuel yield in photoheterotrophic bacteria. mBio 2(2):e00323-10. http://dx.doi.org/10.1128/mBio.00323-10.
11. Wang D, Zhang Y, Pohlmann EL, Li J, Roberts GP. 2011. The poor growth of Rhodospirillum rubrum mutants lacking RubisCO is due to the accumulation of ribulose-1,5-bisphosphate. J. Bacteriol. 193:3293-3303. http://dx.doi.org/10.1128/JB.00265-11.
12. Hallenbeck PL, Lerchen R, Hessler P, Kaplan S. 1990. Phosphoribulokinase activity and regulation of CO2 fixation critical for photosynthetic growth of Rhodobacter sphaeroides. J. Bacteriol. 172:1749-1761.
13. Hädicke O, Grammel H, Klamt S. 2011. Metabolic network modeling of redox balancing and biohydrogen production in purple nonsulfur bacteria. BMC Syst. Biol. 5:150. http://dx.doi.org/10.1186/1752-0509-5-150.
14. Klamt S, Schuster S, Gilles ED. 2002. Calculability analysis in underdetermined metabolic networks illustrated by a model of the central metabolism in purple nonsulfur bacteria. Biotechnol. Bioeng. 77:734-751. http://dx.doi.org/10.1002/bit.10153.
15. Gharibi H, Atikol U, Öztürk Y, Gökçe A, Peksel B, Gürgan M, Özgür E, Gündüz U, Eroǧlu İ, Yücel M. 2012. Hydrogen production properties of Rhodobacter capsulatus with genetically modified redox balancing pathways. Int. J. Hydrogen Energy 37:2014-2020. http://dx.doi.org/10.1016/j.ijhydene.2011.06.078.
16. Gest H. 1999. Memoir of a 1949 railway journey with photosynthetic bacteria. Photosynth. Res. 61:91-96. http://dx.doi.org/10.1023/A:1006257628672.
17. Wang D, Zhang Y, Welch E, Li J, Roberts GP. 2010. Elimination of RubisCO alters the regulation of nitrogenase activity and increases hydrogen production in Rhodospirillum rubrum. Int. J. Hydrogen Energy 35: 7377-7385. http://dx.doi.org/10.1016/j.ijhydene.2010.04.183.
18. Joshi HM, Tabita FR. 1996. A global two-component signal transduction system that integrates the control of photosynthesis, carbon dioxide assimilation, and nitrogen fixation. Proc. Natl. Acad. Sci. U. S. A. 93:14515-14520. http://dx.doi.org/10.1073/pnas.93.25.14515.
19. Fitzmaurice WP, Saari LL, Lowery RG, Ludden PW, Roberts GP. 1989. Genes coding for the reversible ADP-ribosylation system of dinitrogenase reductase from Rhodospirillum rubrum. Mol. Gen. Genet. 218:340-347. http://dx.doi.org/10.1007/BF00331287.
20. Ormerod JG, Ormerod KS, Gest H. 1961. Light-dependent utilization of organic compounds and photoproduction of molecular hydrogen by photosynthetic bacteria; relationships with nitrogen metabolism. Arch. Biochem. Biophys. 94:449-463. http://dx.doi.org/10.1016/0003-9861(61)90073-X.
21. Larimer FW, Chain P, Hauser L, Lamerdin J, Malfatti S, Do L, Land ML, Pelletier DA, Beatty JT, Lang AS, Tabita FR, Gibson JL, Hanson TE, Bobst C, Torres JL, Peres C, Harrison FH, Gibson J, Harwood CS. 2004. Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris. Nat. Biotechnol. 22:55-61. http://dx.doi.org/10.1038/nbt923.
22. Rey FE, Oda Y, Harwood CS. 2006. Regulation of uptake hydrogenase and effects of hydrogen utilization on gene expression in Rhodopseudomonas palustris. J. Bacteriol. 188:6143-6152. http://dx.doi.org/10.1128/JB.00381-06.
23. Kim M, Harwood CS. 1991. Regulation of benzoate-CoA ligase in Rhodopseudomonas palustris. FEMS Microbiol. Lett. 83:199-203. http://dx.doi.org/10.1111/j.1574-6968.1991.tb04440.x-i1.
24. Horton RM, Ho SN, Pullen JK, Hunt HD, Cai Z, Pease LR. 1993. Gene splicing by overlap extension. Methods Enzymol. 217:270-279.
25. Yanisch-Perron C, Vieira J, Messing J. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119. http://dx.doi.org/10.1016/0378-1119(85)90120-9.
26. Quandt J, Hyndes MF. 1993. Versatile suicide vectors which allow direct selection for gene replacement in gram-negative bacteria. Gene 127:15-21. http://dx.doi.org/10.1016/0378-1119(93)90611-6.
27. Simon R, Priefer U, Pühler A. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Nat. Biotechnol. 1:784-791. http://dx.doi.org/10.1038/nbt1183-784.
28. Huang JJ, Heiniger EK, McKinlay JB, Harwood CS. 2010. Production of hydrogen gas from light and the inorganic electron donor thiosulfate by Rhodopseudomonas palustris. Appl. Environ. Microbiol. 76:7717-7722. http://dx.doi.org/10.1128/AEM.01143-10.
29. Karr DB, Waters JK, Emerich DW. 1983. Analysis of poly-3-hydroxybutyrate in Rhizobium japonicum bacteroids by ion-exclusion high-pressure liquid chromatography and UV detection. Appl. Environ. Microbiol. 46:1339-1344.
30. Rey FE, Heiniger EK, Harwood CS. 2007. Redirection of metabolism for biological hydrogen production. Appl. Environ. Microbiol. 73:1665-1671. http://dx.doi.org/10.1128/AEM.02565-06.
31. Zou X, Zhu Y, Pohlmann EL, Li J, Zhang Y, Roberts GP. 2008. Identification and functional characterization of NifA variants that are independent of GlnB activation in the photosynthetic bacterium Rhodospirillum rubrum. Microbiology 154:2689-2699. http://dx.doi.org/10.1099/mic.0.2008/019406-0.
32. Wang X, Modak HV, Tabita FR. 1993. Photolithoautotrophic growth and control of CO2 fixation in Rhodobacter sphaeroides and Rhodospirillum rubrum in the absence of ribulose bisphosphate carboxylaseoxygenase. J. Bacteriol. 175:7109-7114.
33. Grammel H, Gilles E-D, Ghosh R. 2003. Microaerophilic cooperation of reductive and oxidative pathways allows maximal photosynthetic membrane biosynthesis in Rhodospirillum rubrum. Appl. Environ. Microbiol. 69:6577-6586. http://dx.doi.org/10.1128/AEM.69.11.6577-6586.2003.