Serine 363 of a hydrophobic region of Archaeal ribulose 1,5-bisphosphate carboxylase/oxygenase from Archaeoglobus fulgidus and Thermococcus kodakaraensis affects CO2/O2 substrate specificity and oxygen sensitivity
Abstract
Archaeal ribulose 1, 5-bisphospate carboxylase/oxygenase (RubisCO) is differentiated from other RubisCO enzymes and is classified as a form III enzyme, as opposed to the form I and form II RubisCOs typical of chemoautotrophic bacteria and prokaryotic and eukaryotic phototrophs. The form III enzyme from archaea is particularly interesting as several of these proteins exhibit unusual and reversible sensitivity to molecular oxygen, including the enzyme from Archaeoglobus fulgidus. Previous studies with A. fulgidus RbcL2 had shown the importance of Met-295 in oxygen sensitivity and pointed towards the potential significance of another residue (Ser-363) found in a hydrophobic pocket that is conserved in all RubisCO proteins. In the current study, further structure/function studies have been performed focusing on Ser-363 of A. fulgidus RbcL2; various changes in this and other residues of the hydrophobic pocket point to and definitively establish the importance of Ser-363 with respect to interactions with oxygen. In addition, previous findings had indicated discrepant CO2/O2 specificity determinations of the Thermococcus kodakaraensis RubisCO, a close homolog of A. fulgidus RbcL2. As a result, it is shown here that the T. kodakaraensis enzyme exhibits a similar substrate specificity as the A. fulgidus enzyme and is also oxygen sensitive, with equivalent residues involvedmore »
- Authors:
-
- The Ohio State Univ., Columbus, OH (United States)
- Univ. of Freiburg (Germany)
- Publication Date:
- Research Org.:
- The Ohio State Univ., Columbus, OH (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1324973
- Grant/Contract Number:
- FG02-08ER15976
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS ONE
- Additional Journal Information:
- Journal Volume: 10; Journal Issue: 9; Journal ID: ISSN 1932-6203
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Ribulose-1,5-bisphosphate carboxylase oxygenase; oxygen; enzymes; complement system; enzyme structure; crystal structure; enzyme assays; recombinant proteins
Citation Formats
Kreel, Nathan E., Tabita, F. Robert, and Berg, Ivan. Serine 363 of a hydrophobic region of Archaeal ribulose 1,5-bisphosphate carboxylase/oxygenase from Archaeoglobus fulgidus and Thermococcus kodakaraensis affects CO2/O2 substrate specificity and oxygen sensitivity. United States: N. p., 2015.
Web. doi:10.1371/journal.pone.0138351.
Kreel, Nathan E., Tabita, F. Robert, & Berg, Ivan. Serine 363 of a hydrophobic region of Archaeal ribulose 1,5-bisphosphate carboxylase/oxygenase from Archaeoglobus fulgidus and Thermococcus kodakaraensis affects CO2/O2 substrate specificity and oxygen sensitivity. United States. https://doi.org/10.1371/journal.pone.0138351
Kreel, Nathan E., Tabita, F. Robert, and Berg, Ivan. Fri .
"Serine 363 of a hydrophobic region of Archaeal ribulose 1,5-bisphosphate carboxylase/oxygenase from Archaeoglobus fulgidus and Thermococcus kodakaraensis affects CO2/O2 substrate specificity and oxygen sensitivity". United States. https://doi.org/10.1371/journal.pone.0138351. https://www.osti.gov/servlets/purl/1324973.
@article{osti_1324973,
title = {Serine 363 of a hydrophobic region of Archaeal ribulose 1,5-bisphosphate carboxylase/oxygenase from Archaeoglobus fulgidus and Thermococcus kodakaraensis affects CO2/O2 substrate specificity and oxygen sensitivity},
author = {Kreel, Nathan E. and Tabita, F. Robert and Berg, Ivan},
abstractNote = {Archaeal ribulose 1, 5-bisphospate carboxylase/oxygenase (RubisCO) is differentiated from other RubisCO enzymes and is classified as a form III enzyme, as opposed to the form I and form II RubisCOs typical of chemoautotrophic bacteria and prokaryotic and eukaryotic phototrophs. The form III enzyme from archaea is particularly interesting as several of these proteins exhibit unusual and reversible sensitivity to molecular oxygen, including the enzyme from Archaeoglobus fulgidus. Previous studies with A. fulgidus RbcL2 had shown the importance of Met-295 in oxygen sensitivity and pointed towards the potential significance of another residue (Ser-363) found in a hydrophobic pocket that is conserved in all RubisCO proteins. In the current study, further structure/function studies have been performed focusing on Ser-363 of A. fulgidus RbcL2; various changes in this and other residues of the hydrophobic pocket point to and definitively establish the importance of Ser-363 with respect to interactions with oxygen. In addition, previous findings had indicated discrepant CO2/O2 specificity determinations of the Thermococcus kodakaraensis RubisCO, a close homolog of A. fulgidus RbcL2. As a result, it is shown here that the T. kodakaraensis enzyme exhibits a similar substrate specificity as the A. fulgidus enzyme and is also oxygen sensitive, with equivalent residues involved in oxygen interactions.},
doi = {10.1371/journal.pone.0138351},
journal = {PLoS ONE},
number = 9,
volume = 10,
place = {United States},
year = {Fri Sep 18 00:00:00 EDT 2015},
month = {Fri Sep 18 00:00:00 EDT 2015}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 13 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Distinct form I, II, III, and IV Rubisco proteins from the three kingdoms of life provide clues about Rubisco evolution and structure/function relationships
journal, June 2007
- Tabita, F. R.; Satagopan, S.; Hanson, T. E.
- Journal of Experimental Botany, Vol. 59, Issue 7
The CO2/O2 specificity of ribulose 1,5-bisphosphate carboxylase/oxygenase: Dependence on ribulosebisphosphate concentration, pH and temperature
journal, June 1984
- Jordan, Douglas B.; Ogren, William L.
- Planta, Vol. 161, Issue 4
Role of auxiliary proteins in Rubisco biogenesis and function
journal, June 2015
- Hauser, Thomas; Popilka, Leonhard; Hartl, F. Ulrich
- Nature Plants, Vol. 1, Issue 6
Distinct form I, II, III, and IV Rubisco proteins from the three kingdoms of life provide clues about Rubisco evolution and structure/function relationships
journal, June 2007
- Tabita, F. R.; Satagopan, S.; Hanson, T. E.
- Journal of Experimental Botany, Vol. 59, Issue 7
Function, Structure, and Evolution of the RubisCO-Like Proteins and Their RubisCO Homologs
journal, December 2007
- Tabita, F. R.; Hanson, T. E.; Li, H.
- Microbiology and Molecular Biology Reviews, Vol. 71, Issue 4
Unusual Ribulose 1,5-Bisphosphate Carboxylase/Oxygenase of Anoxic Archaea
journal, March 1999
- Watson, Gregory M. F.; Yu, Jae-Pil; Tabita, F. Robert
- Journal of Bacteriology, Vol. 181, Issue 5
Positive and Negative Selection of Mutant Forms of Prokaryotic (Cyanobacterial) Ribulose-1,5-bisphosphate Carboxylase/Oxygenase
journal, August 2003
- Smith, Stephanie A.; Tabita, F. Robert
- Journal of Molecular Biology, Vol. 331, Issue 3
A Rubisco Mutant That Confers Growth under a Normally “Inhibitory” Oxygen Concentration
journal, September 2009
- Satagopan, Sriram; Scott, Stephanie S.; Smith, Todd G.
- Biochemistry, Vol. 48, Issue 38
Modified Pathway To Synthesize Ribulose 1,5-Bisphosphate in Methanogenic Archaea
journal, September 2004
- Finn, M. W.; Tabita, F. R.
- Journal of Bacteriology, Vol. 186, Issue 19
Rubisco Synthesis, Assembly, Mechanism, and Regulation
journal, July 1995
- Gutteridge, Steven; Gatenby, Anthony A.
- The Plant Cell, Vol. 7, Issue 7
Ribulose bisphosphate carboxylase/oxygenase from the hyperthermophilic archaeon Pyrococcus kodakaraensis KOD1 is composed solely of large subunits and forms a pentagonal structure
journal, October 1999
- Maeda, Norihiro; Kitano, Ken; Fukui, Toshiaki
- Journal of Molecular Biology, Vol. 293, Issue 1
Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4
journal, August 1970
- Laemmli, U. K.
- Nature, Vol. 227, Issue 5259, p. 680-685
Presence of a Structurally Novel Type Ribulose-bisphosphate Carboxylase/Oxygenase in the Hyperthermophilic Archaeon, Pyrococcus kodakaraensis KOD1
journal, February 1999
- Ezaki, Satoshi; Maeda, Norihiro; Kishimoto, Tsukuru
- Journal of Biological Chemistry, Vol. 274, Issue 8
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice
journal, January 1994
- Thompson, Julie D.; Higgins, Desmond G.; Gibson, Toby J.
- Nucleic Acids Research, Vol. 22, Issue 22, p. 4673-4680
Ribulose bisphosphate carboxylase/oxygenase from the hyperthermophilic archaeon Pyrococcus kodakaraensis KOD1 is composed solely of large subunits and forms a pentagonal structure
journal, October 1999
- Maeda, Norihiro; Kitano, Ken; Fukui, Toshiaki
- Journal of Molecular Biology, Vol. 293, Issue 1
Substrate-induced Assembly of Methanococcoides burtonii d-Ribulose-1,5-bisphosphate Carboxylase/Oxygenase Dimers into Decamers
journal, October 2009
- Alonso, Hernán; Blayney, Michelle J.; Beck, Jennifer L.
- Journal of Biological Chemistry, Vol. 284, Issue 49
Archaeal Type III RuBisCOs Function in a Pathway for AMP Metabolism
journal, February 2007
- Sato, T.; Atomi, H.; Imanaka, T.
- Science, Vol. 315, Issue 5814
Serine-376 contributes to the binding of substrate by ribulose-bisphosphate carboxylase/oxygenase from Anacystis nidulans
journal, March 1992
- Lee, Garrett J.; McFadden, Bruce A.
- Biochemistry, Vol. 31, Issue 8
A faster Rubisco with potential to increase photosynthesis in crops
journal, September 2014
- Lin, Myat T.; Occhialini, Alessandro; Andralojc, P. John
- Nature, Vol. 513, Issue 7519
A Rubisco Mutant That Confers Growth under a Normally “Inhibitory” Oxygen Concentration
journal, September 2009
- Satagopan, Sriram; Scott, Stephanie S.; Smith, Todd G.
- Biochemistry, Vol. 48, Issue 38
The Genome of M. acetivorans Reveals Extensive Metabolic and Physiological Diversity
journal, April 2002
- Galagan, J. E.
- Genome Research, Vol. 12, Issue 4
Carbon dioxide fixation in ‘Archaeoglobus lithotrophicus’: are there multiple autotrophic pathways?: Autotrophic CO2 fixation in Archaeoglobus
journal, April 2011
- Estelmann, Sebastian; Ramos-Vera, Walter Hugo; Gad'on, Nasser
- FEMS Microbiology Letters, Vol. 319, Issue 1
Structural mechanism of RuBisCO activation by carbamylation of the active site lysine
journal, October 2012
- Stec, B.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 46
SWISS-MODEL and the Swiss-Pdb Viewer: An environment for comparative protein modeling
journal, January 1997
- Guex, Nicolas; Peitsch, Manuel C.
- Electrophoresis, Vol. 18, Issue 15, p. 2714-2723
A faster Rubisco with potential to increase photosynthesis in crops
journal, September 2014
- Lin, Myat T.; Occhialini, Alessandro; Andralojc, P. John
- Nature, Vol. 513, Issue 7519
A pentose bisphosphate pathway for nucleoside degradation in Archaea
journal, March 2015
- Aono, Riku; Sato, Takaaki; Imanaka, Tadayuki
- Nature Chemical Biology, Vol. 11, Issue 5
Anion-Exchange Analysis of Ribulose-Bisphosphate Carboxylase/Oxygenase Reactions: CO2/O2 Specificity Determination and Identification of Side Products
journal, March 1993
- Harpel, M. R.; Lee, E. H.; Hartman, F. C.
- Analytical Biochemistry, Vol. 209, Issue 2
Microbial ribulose 1,5-bisphosphate carboxylase/oxygenase: a molecule for phylogenetic and enzymological investigation
journal, January 1997
- Watson, Gregory M. F.; Tabita, F. Robert
- FEMS Microbiology Letters, Vol. 146, Issue 1
Carbon dioxide fixation in ‘Archaeoglobus lithotrophicus’: are there multiple autotrophic pathways?: Autotrophic CO2 fixation in Archaeoglobus
journal, April 2011
- Estelmann, Sebastian; Ramos-Vera, Walter Hugo; Gad'on, Nasser
- FEMS Microbiology Letters, Vol. 319, Issue 1
Structure-based Catalytic Optimization of a Type III Rubisco from a Hyperthermophile
journal, October 2010
- Nishitani, Yuichi; Yoshida, Shosuke; Fujihashi, Masahiro
- Journal of Biological Chemistry, Vol. 285, Issue 50
Rubisco Synthesis, Assembly, Mechanism, and Regulation.
journal, July 1995
- Gutteridge, S.; Gatenby, A. A.
- The Plant Cell
Corrected nucleotide sequence of M13mp18 gene III
journal, May 1992
- Ebright, Richard; Dong, Qianping; Messing, Joachim
- Gene, Vol. 114, Issue 1
The Unique Pentagonal Structure of an Archaeal Rubisco Is Essential for Its High Thermostability
journal, June 2002
- Maeda, Norihiro; Kanai, Tamotsu; Atomi, Haruyuki
- Journal of Biological Chemistry, Vol. 277, Issue 35
Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mpl8 and pUC19 vectors
journal, January 1985
- Yanisch-Perron, Celeste; Vieira, Jeffrey; Messing, Joachim
- Gene, Vol. 33, Issue 1
Tobacco fraction 1 protein: a unique genetic marker
journal, March 2003
- Kung, S.
- Science, Vol. 191, Issue 4226
Anion-Exchange Analysis of Ribulose-Bisphosphate Carboxylase/Oxygenase Reactions: CO2/O2 Specificity Determination and Identification of Side Products
journal, March 1993
- Harpel, M. R.; Lee, E. H.; Hartman, F. C.
- Analytical Biochemistry, Vol. 209, Issue 2
Species variation in the specificity of ribulose biphosphate carboxylase/oxygenase
journal, June 1981
- Jordan, Douglas B.; Ogren, William L.
- Nature, Vol. 291, Issue 5815
Structure-Function Studies with the Unique Hexameric Form II Ribulose-1,5-bisphosphate Carboxylase/Oxygenase (Rubisco) from Rhodopseudomonas palustris
journal, June 2014
- Satagopan, Sriram; Chan, Sum; Perry, L. Jeanne
- Journal of Biological Chemistry, Vol. 289, Issue 31
Crystal structure of the unactivated ribulose 1, 5-bisphosphate carboxylase/oxygenase complexed with a transition state analog, 2-carboxy-D-arabinitol 1, 5-bisphosphate: Crystal structure of rubisco complexed with CABP
journal, January 1994
- Zhang, Kam Y. J.; Cascio, Duilio; Eisenberg, David
- Protein Science, Vol. 3, Issue 1
SWISS-MODEL and the Swiss-Pdb Viewer: An environment for comparative protein modeling
journal, January 1997
- Guex, Nicolas; Peitsch, Manuel C.
- Electrophoresis, Vol. 18, Issue 15, p. 2714-2723
Mechanism of Rubisco: The Carbamate as General Base ✗
journal, April 1998
- Cleland, W. Wallace; Andrews, T. John; Gutteridge, Steven
- Chemical Reviews, Vol. 98, Issue 2
Engineering of a Type III Rubisco from a Hyperthermophilic Archaeon in Order To Enhance Catalytic Performance in Mesophilic Host Cells
journal, August 2007
- Yoshida, S.; Atomi, H.; Imanaka, T.
- Applied and Environmental Microbiology, Vol. 73, Issue 19
Archaeal Type III RuBisCOs Function in a Pathway for AMP Metabolism
journal, February 2007
- Sato, T.; Atomi, H.; Imanaka, T.
- Science, Vol. 315, Issue 5814
Serine-376 contributes to the binding of substrate by ribulose-bisphosphate carboxylase/oxygenase from Anacystis nidulans
journal, March 1992
- Lee, Garrett J.; McFadden, Bruce A.
- Biochemistry, Vol. 31, Issue 8
Effect of temperature on the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light: Estimates from gas-exchange measurements on spinach
journal, January 1985
- Brooks, A.; Farquhar, G. D.
- Planta, Vol. 165, Issue 3
Presence of a Structurally Novel Type Ribulose-bisphosphate Carboxylase/Oxygenase in the Hyperthermophilic Archaeon, Pyrococcus kodakaraensis KOD1
journal, February 1999
- Ezaki, Satoshi; Maeda, Norihiro; Kishimoto, Tsukuru
- Journal of Biological Chemistry, Vol. 274, Issue 8
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice
journal, January 1994
- Thompson, Julie D.; Higgins, Desmond G.; Gibson, Toby J.
- Nucleic Acids Research, Vol. 22, Issue 22, p. 4673-4680
A pentose bisphosphate pathway for nucleoside degradation in Archaea
journal, March 2015
- Aono, Riku; Sato, Takaaki; Imanaka, Tadayuki
- Nature Chemical Biology, Vol. 11, Issue 5
Crystal Structure of a Novel-Type Archaeal Rubisco with Pentagonal Symmetry
journal, June 2001
- Kitano, Ken; Maeda, Norihiro; Fukui, Toshiaki
- Structure, Vol. 9, Issue 6
Enhanced CO2/O2 specificity of a site-directed mutant of ribulose-bisphosphate carboxylase/oxygenase.
journal, April 1992
- Harpel, M. R.; Hartman, F. C.
- Journal of Biological Chemistry, Vol. 267, Issue 10
Directed mutagenesis of chloroplast ribulosebisphosphate carboxylase/oxygenase. Substitutions at large subunit asparagine 123 and serine 379 decrease CO2/O2 specificity.
journal, February 1994
- Zhu, G.; Spreitzer, R. J.
- Journal of Biological Chemistry, Vol. 269, Issue 6
Works referencing / citing this record:
Evolutionary trends in RuBisCO kinetics and their co‐evolution with CO 2 concentrating mechanisms
journal, January 2020
- Iñiguez, Concepción; Capó‐Bauçà, Sebastià; Niinemets, Ülo
- The Plant Journal, Vol. 101, Issue 4
A synthetic pathway for the fixation of carbon dioxide in vitro
journal, November 2016
- Schwander, Thomas; Schada von Borzyskowski, Lennart; Burgener, Simon
- Science, Vol. 354, Issue 6314
Synthetic CO2-fixation enzyme cascades immobilized on self-assembled nanostructures that enhance CO2/O2 selectivity of RubisCO
journal, July 2017
- Satagopan, Sriram; Sun, Yuan; Parquette, Jon R.
- Biotechnology for Biofuels, Vol. 10, Issue 1
Photoreduction of CO 2 with a Formate Dehydrogenase Driven by Photosystem II Using a Semi-artificial Z-Scheme Architecture
journal, November 2018
- Sokol, Katarzyna P.; Robinson, William E.; Oliveira, Ana R.
- Journal of the American Chemical Society, Vol. 140, Issue 48