Identification and characterization of multiple rubisco activases in chemoautotrophic bacteria

Nature Communications

Volumn 6, Issue , 2015, Pages

  Tsai, Yi Chin Candace ^a   Lapina, Maria Claribel ^a   Bhushan, Shashi ^a   Mueller Cajar, Oliver ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CBBO PROTEIN; CBBQ PROTEIN; MOLECULAR MOTOR; RIBULOSEBISPHOSPHATE CARBOXYLASE; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR; BACTERIAL PROTEIN; CARRIER PROTEIN; CBBQ PROTEIN, BACTERIA;

BACTERIUM; CARBON DIOXIDE; ENZYME ACTIVITY; INHIBITION; INHIBITOR; MUTATION; PHOSPHATE; PHOTOSYNTHESIS; PROTEIN; SUGAR;

ACIDITHIOBACILLUS FERROOXIDANS; ARTICLE; CHEMOLITHOAUTOTROPH; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME MECHANISM; MUTATIONAL ANALYSIS; NONHUMAN; ACIDITHIOBACILLUS; CHEMOAUTOTROPHY; ELECTRON MICROSCOPY; ENZYME ASSAY; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; METABOLISM; PHOTOSYNTHESIS; RHODOBACTER SPHAEROIDES; RHODOPSEUDOMONAS; RHODOSPIRILLUM RUBRUM;

ACIDITHIOBACILLUS FERROOXIDANS; ALPHAPROTEOBACTERIA;

ACIDITHIOBACILLUS; BACTERIAL PROTEINS; CARRIER PROTEINS; CHEMOAUTOTROPHIC GROWTH; ENZYME ASSAYS; ESCHERICHIA COLI; MICROSCOPY, ELECTRON; PHOTOSYNTHESIS; RHODOBACTER SPHAEROIDES; RHODOPSEUDOMONAS; RHODOSPIRILLUM RUBRUM; RIBULOSE-BISPHOSPHATE CARBOXYLASE;

EID: 84947206879     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9883     Document Type: Article

References (70)

1. Lin, M. T., Occhialini, A., Andralojc, P. J., Parry, M. A. & Hanson, M. R. A faster Rubisco with potential to increase photosynthesis in crops. Nature 513, 547-550 (2014).
2. Parry, M. A. et al. Rubisco activity and regulation as targets for crop improvement. J. Exp. Bot. 64, 717-730 (2013).
3. Zhu, X. G., Long, S. P. & Ort, D. R. Improving photosynthetic efficiency for greater yield. Annu. Rev. Plant Biol. 61, 235-261 (2010).
4. Whitney, S. M., Baldet, P., Hudson, G. S. & Andrews, T. J. Form I Rubiscos from non-green algae are expressed abundantly but not assembled in tobacco chloroplasts. Plant J. 26, 535-547 (2001).
5. Whitney, S. M., Houtz, R. L. & Alonso, H. Advancing our understanding and capacity to engineer nature's CO(2)-sequestering enzyme, rubisco. Plant Physiol. 155, 27-35 (2011).
6. Whitney, S. M., Birch, R., Kelso, C., Beck, J. L. & Kapralov, M. V. Improving recombinant Rubisco biogenesis, plant photosynthesis and growth by coexpressing its ancillary RAF1 chaperone. Proc. Natl Acad. Sci. USA 112, 3564-3569 (2015).
7. Mueller-Cajar, O., Stotz, M. & Bracher, A. Maintaining photosynthetic CO2 fixation via protein remodelling: the Rubisco activases. Photosynth. Res. 119, 191-201 (2014).
8. Hauser, T., Popilka, L., Hartl, F. U. & Hayer-Hartl, M. Role of auxiliary proteins in Rubisco biogenesis and function. Nat. Plants 1, 15065 (2015).
9. Andersson, I. & Backlund, A. Structure and function of Rubisco. Plant Physiol. Biochem. 46, 275-291 (2008).
10. Satagopan, S., Chan, S., Perry, L. J. & Tabita, F. R. Structure-function studies with the unique hexameric form II ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) from Rhodopseudomonas palustris. J. Biol. Chem. 289, 21433-21450 (2014).
11. Badger, M. R. & Bek, E. J. Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle. J. Exp. Bot. 59, 1525-1541 (2008).
12. Bauwe, H., Hagemann, M. & Fernie, A. R. Photorespiration: players, partners and origin. Trends Plant Sci. 15, 330-336 (2010).
13. Tcherkez, G. G. B., Farquhar, G. D. & Andrews, T. J. Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proc. Natl Acad. Sci. USA 103, 7246-7251 (2006).
14. Pearce, F. G. & Andrews, T. J. The relationship between side reactions and slow inhibition of ribulose-bisphosphate carboxylase revealed by a loop 6 mutant of the tobacco enzyme. J. Biol. Chem. 278, 32526-32536 (2003).
15. Pearce, F. G. Catalytic by-product formation and ligand binding by ribulose bisphosphate carboxylases from different phylogenies. Biochem. J. 399, 525-534 (2006).
16. Parry, M. A. J., Keys, A. J., Madgwick, P. J., Carmo-Silva, A. E. & Andralojc, P. J. Rubisco regulation: a role for inhibitors. J. Exp. Bot. 59, 1569-1580 (2008).
17. Cleland, W. W., Andrews, T. J., Gutteridge, S., Hartman, F. C. & Lorimer, G. H. Mechanism of Rubisco - the carbamate as general base. Chem. Rev. 98, 549-561 (1998).
18. Portis, A. R. Rubisco activase - Rubisco's catalytic chaperone. Photosynth. Res. 75, 11-27 (2003).
19. Mueller-Cajar, O. et al. Structure and function of the AAA + protein CbbX, a red-type Rubisco activase. Nature 479, 194-199 (2011).
20. Stotz, M. et al. Structure of green-type Rubisco activase from tobacco. Nat. Struct. Mol. Biol. 18, 1366-1370 (2011).
21. Salvucci, M. E., Portis, A. R. & Ogren, W. L. A soluble chloroplast protein catalyzes ribulosebisphosphate carboxylase oxygenase activation in vivo. Photosynth. Res. 7, 193-201 (1985).
22. Sauer, R. T. & Baker, T. A. AAA + Proteases: ATP-fueled machines of protein destruction. Annu. Rev. Biochem. 80, 587-612 (2011).
23. Weibezahn, J. et al. Thermotolerance requires refolding of aggregated proteins by substrate translocation through the central pore of ClpB. Cell 119, 653-665 (2004).
24. Scales, J. C., Parry, M. A. & Salvucci, M. E. A non-radioactive method for measuring Rubisco activase activity in the presence of variable ATP: ADP ratios, including modifications for measuring the activity and activation state of Rubisco. Photosynth. Res. 119, 355-365 (2014).
25. Henderson, J. N., Kuriata, A. M., Fromme, R., Salvucci, M. E. & Wachter, R. M. Atomic resolution X-ray structure of the substrate recognition domain of higher plant ribulose-bisphosphate carboxylase/oxygenase (rubisco) activase. J. Biol. Chem. 286, 35683-35688 (2011).
26. Larson, E. M., O'Brien, C. M., Zhu, G., Spreitzer, R. J. & Portis, Jr. A. R. Specificity for activase is changed by a Pro-89 to Arg substitution in the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. J. Biol. Chem. 272, 17033-17037 (1997).
27. Ott, C. M., Smith, B. D., Portis, Jr. A. R. & Spreitzer, R. J. Activase region on chloroplast ribulose-1,5-bisphosphate carboxylase/oxygenase. J. Biol. Chem. 275, 26241-26244 (2000).
28. Andralojc, P. J. et al. 2-Carboxy-D-arabinitol 1-phosphate (CA1P) phosphatase: evidence for a wider role in plant Rubisco regulation. Biochem. J. 442, 733-742 (2012).
29. Bracher, A., Sharma, A., Starling-Windhof, A., Hartl, F. U. & Hayer-Hartl, M. Degradation of potent Rubisco inhibitor by selective sugar phosphatase. Nat. Plants 1, 14002 (2015).
30. Swan, B. K. et al. Potential for chemolithoautotrophy among ubiquitous bacteria lineages in the dark ocean. Science 333, 1296-1300 (2011).
31. Hayashi, N. R., Arai, H., Kodama, T. & Igarashi, Y. The cbbQ genes, located downstream of the form I and form II RubisCO genes, affect the activity of both RubisCOs. Biochem. Biophys. Res. Commun. 265, 177-183 (1999).
32. Hayashi, N. R., Arai, H., Kodama, T. & Igarashi, Y. The novel genes, cbbQ and cbbO, located downstream from the RubisCO genes of Pseudomonas hydrogenothermophila, affect the conformational states and activity of RubisCO. Biochem. Biophys. Res. Commun. 241, 565-569 (1997).
33. Schwedock, J. et al. Characterization and expression of genes from the RubisCO gene cluster of the chemoautotrophic symbiont of Solemya velum: cbbLSQO. Arch. Microbiol. 182, 18-29 (2004).
34. Guadalupe-Medina, V. et al. Carbon dioxide fixation by Calvin-Cycle enzymes improves ethanol yield in yeast. Biotechnol. Biofuels 6, 125 (2013).
35. Bohnke, S. & Perner, M. A function-based screen for seeking RubisCO active clones from metagenomes: novel enzymes influencing RubisCO activity. ISME J. 9, 735-745 (2015).
36. Wong, K. S. & Houry, W. A. Novel structural and functional insights into the MoxR family of AAA + ATPases. J. Struct. Biol. 179, 211-221 (2012).
37. El Bakkouri, M. et al. Structure of RavA MoxR AAA plus protein reveals the design principles of a molecular cage modulating the inducible lysine decarboxylase activity. Proc. Natl Acad. Sci. USA 107, 22499-22504 (2010).
38. Snider, J. & Houry, W. A. MoxR AAA + ATPases: A novel family of molecular chaperones? J. Struct. Biol. 156, 200-209 (2006).
39. Whittaker, C. A. & Hynes, R. O. Distribution and evolution of von Willebrand/integrin a domains: Widely dispersed adhesion and elsewhere. Mol. Biol. Cell 13, 3369-3387 (2002).
40. Xiong, J. P. et al. Crystal structure of the extracellular segment of integrin alpha V beta 3 in complex with an Arg-Gly-Asp ligand. Science 296, 151-155 (2002).
41. Santelli, E., Bankston, L. A., Leppla, S. H. & Liddington, R. C. Crystal structure of a complex between anthrax toxin and its host cell receptor. Nature 430, 905-908 (2004).
42. Siegel, L. M. & Monty, K. J. Determination of molecular weights and frictional ratios of proteins in impure systems by use of gel filtration and density gradient centrifugation. Biochim. Biophys. Acta 112, 346-362 (1966).
43. Erickson, H. P. Size and shape of protein molecules at the nanometer level determined by sedimentation, gel filtration, and electron microscopy. Biol. Proced. Online 11, 32-51 (2009).
44. Pierce, J., Tolbert, N. E. & Barker, R. Interaction of ribulosebisphosphate carboxylase-oxygenase with transition-state analogs. Biochemistry 19, 934-942 (1980).
45. Alonso, H., Blayney, M. J., Beck, J. L. & Whitney, S. M. Substrate-induced assembly of Methanococcoides burtonii D-ribulose-1,5-bisphosphate carboxylase/oxygenase dimers into decamers. J. Biol. Chem. 284, 33876-33882 (2009).
46. Catanzariti, A.-M., Soboleva, T. A., Jans, D. A., Board, P. G. & Baker, R. T. An efficient system for high-level expression and easy purification of authentic recombinant proteins. Protein Sci. 13, 1331-1339 (2004).
47. Salvucci, M. E. Subunit interactions of rubisco activase - polyethylene-glycol promotes self-association, stimulates atpase and activation activities, and enhances interactions with rubisco. Arch. Biochem. Biophys. 298, 688-696 (1992).
48. Jordan, D. B. & Chollet, R. Inhibition of ribulose bisphosphate carboxylase by substrate ribulose 1,5-bisphosphate. J.Biol.Chem. 258, 13752-13758 (1983).
49. Hernandez, J. M., Baker, S. H., Lorbach, S. C., Shively, J. M. & Tabita, F. R. Deduced amino acid sequence, functional expression, and unique enzymatic properties of the form I and form II ribulose bisphosphate carboxylase oxygenase from the chemoautotrophic bacterium Thiobacillus denitrificans. J. Bacteriol. 178, 347-356 (1996).
50. Robinson, S. P. & Portis, A. R. Release of the nocturnal inhibitor, carboxyarabinitol-1-phosphate, from ribulose bisphosphate carboxylase oxygenase by rubisco activase. FEBS Lett. 233, 413-416 (1988).
51. Robinson, S. P. & Portis, A. R. Adenosine-triphosphate hydrolysis by purified rubisco activase. Arch. Biochem. Biophys. 268, 93-99 (1989).
52. Zhang, X. & Wigley, D. B.The 'glutamate switch' provides a link between ATPase activity and ligand binding in AAA + proteins. Nat. Struct. Mol. Biol. 15, 1223-1227 (2008).
53. Li, C. H., Salvucci, M. E. & Portis, A. R. Two residues of rubisco activase involved in recognition of the rubisco substrate. J. Biol. Chem. 280, 24864-24869 (2005).
54. Heinhorst, S. et al. Two Copies of form I RuBisCO genes in Acidithiobacillus ferrooxidans ATCC 23270. Curr. Microbiol. 45, 115-117 (2002).
55. Yoshizawa, Y., Toyoda, K., Arai, H., Ishii, M. & Igarashi, Y. CO2-responsive expression and gene organization of three ribulose-1,5-bisphosphate carboxylase/oxygenase enzymes and carboxysomes in Hydrogenovibrio marinus strain MH-110. J. Bacteriol. 186, 5685-5691 (2004).
56. Esparza, M., Bowien, B., Jedlicki, E. & Holmes, D. S. Gene organization and CO(2)-responsive expression of four cbb operons in the biomining bacterium Acidithiobacillus ferrooxidans. Adv. Mater. Res 71-73, 207-210 (2009).
57. Ulbrich, C. et al. Mechanochemical removal of ribosome biogenesis factors from nascent 60S ribosomal subunits. Cell 138, 911-922 (2009).
58. Enright, A. J., Iliopoulos, I., Kyrpides, N. C. & Ouzounis, C. A. Protein interaction maps for complete genomes based on gene fusion events. Nature 402, 86-90 (1999).
59. Ammelburg, M., Frickey, T. & Lupas, A. N. Classification of AAA + proteins. J. Struct. Biol. 156, 2-11 (2006).
60. Iyer, L. M., Leipe, D. D., Koonin, E. V. & Aravind, L. Evolutionary history and higher order classification of AAA + ATPases. J. Struct. Biol. 146, 11-31 (2004).
61. Snider, J. et al. Formation of a distinctive complex between the inducible bacterial lysine decarboxylase and a novel AAA + ATPase. J. Biol. Chem. 281, 1532-1546 (2006).
62. Scheele, U. et al. Chaperone role for proteins p618 and p892 in the extracellular tail development of Acidianus two-tailed virus. J. Virol. 85, 4812-4821 (2011).
63. Valdes, J. et al. Acidithiobacillus ferrooxidans metabolism: from genome sequence to industrial applications. BMC Genomics 9, 597 (2008).
64. Mueller-Cajar, O., Morell, M. & Whitney, S. M. Directed evolution of rubisco in Escherichia coli reveals a specificity-determining hydrogen bond in the form II enzyme. Biochemistry 46, 14067-14074 (2007).
65. Guzman, L. M., Belin, D., Carson, M. J. & Beckwith, J. Tight regulation, modulation, and high-level expression by vectors containing the arabinose P-Bad promoter. J. Bacteriol. 177, 4121-4130 (1995).
66. Kreuzer, K. N. & Jongeneel, C. V. Escherichia coli phage-T4 topoisomerase. Methods Enzymol. 100, 144-160 (1983).
67. Kubien, D. S., Brown, C. M. & Kane, H. J. Quantifying the amount and activity of Rubisco in leaves. Methods Mol. Biol. 684, 349-362 (2011).
68. Horecker, B. L., Hurwitz, J. & Weissbach, A. Ribulose diphosphate. Biochem. Prep. 6, 83-90 (1958).
69. Kane, H. J., Wilkin, J. M., Portis, A. R. & Andrews, T. J. Potent inhibition of ribulose-bisphosphate carboxylase by an oxidized impurity in ribulose-1,5-bisphosphate. Plant Physiol. 117, 1059-1069 (1998).
70. Tang, G. et al. EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46 (2007).