The pentose phosphate pathway of cellulolytic clostridia relies on 6-phosphofructokinase instead of transaldolase

Koendjbiharie, Jeroen G.; Hon, Shuen; Pabst, Martin; Hooftman, Robert; Stevenson, David M.; Cui, Jingxuan; Amador-Noguez, Daniel; Lynd, Lee R.; Olson, Daniel G.; van Kranenburg, Richard

doi:10.1074/jbc.ra119.011239

Title: The pentose phosphate pathway of cellulolytic clostridia relies on 6-phosphofructokinase instead of transaldolase

Journal Article · 21 December 2019 · Journal of Biological Chemistry

DOI: https://doi.org/10.1074/jbc.ra119.011239 · OSTI ID:1625094

Koendjbiharie, Jeroen G. ^[1]; Hon, Shuen ^[2]; Pabst, Martin ^[3]; Hooftman, Robert ^[4]; Stevenson, David M. ^[5]; Cui, Jingxuan ^[6]; Amador-Noguez, Daniel ^[7]; Lynd, Lee R. ^[8]; Olson, Daniel G. ^[2];

^[9]

Corbion, Gorinchem (Netherlands); DOE/OSTI
Dartmouth College, Hanover, NH (United States). Thayer School of Engineering; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Bioenergy Innovation
Delft Univ. of Technology (Netherlands). Cell Systems Engineering
Wageningen Univ. and Research, Wageningen (Netherlands). Lab. of Microbiology
Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Bioenergy Innovation; Dartmouth College, Hanover, NH (United States). Dept. of Biological Sciences
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Bioenergy Innovation; Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology
Dartmouth College, Hanover, NH (United States). Thayer School of Engineering; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Bioenergy Innovation; Dartmouth College, Hanover, NH (United States). Dept. of Biological Sciences
Corbion, Gorinchem (Netherlands); Wageningen Univ. and Research, Wageningen (Netherlands). Lab. of Microbiology

The genomes of most cellulolytic clostridia do not contain genes annotated as transaldolase. Therefore, for assimilating pentose sugars or for generating C₅precursors (such as ribose) during growth on other (non-C₅) substrates, they must possess a pathway that connects pentose metabolism with the rest of metabolism. Here we provide evidence that for this connection cellulolytic clostridia rely on the sedoheptulose 1,7-bisphosphate (SBP) pathway, using pyrophosphate-dependent phosphofructokinase (PP_i-PFK) instead of transaldolase. In this reversible pathway, PFK converts sedoheptulose 7-phosphate (S7P) to SBP, after which fructose-bisphosphate aldolase cleaves SBP into dihydroxyacetone phosphate and erythrose 4-phosphate. We show that PP_i-PFKs of Clostridium thermosuccinogenes and Clostridium thermocellum indeed can convert S7P to SBP, and have similar affinities for S7P and the canonical substrate fructose 6-phosphate (F6P). By contrast, (ATP-dependent) PfkA of Escherichia coli, which does rely on transaldolase, had a very poor affinity for S7P. This indicates that the PP_i-PFK of cellulolytic clostridia has evolved the use of S7P. We further show thatC. thermosuccinogenescontains a significant SBP pool, an unusual metabolite that is elevated during growth on xylose, demonstrating its relevance for pentose assimilation. Last, we demonstrate that a second PFK of C. thermosuccinogenes that operates with ATP and GTP exhibits unusual kinetics toward F6P, as it appears to have an extremely high degree of cooperative binding, resulting in a virtual on/off switch for substrate concentrations near its K_½value. In summary, our results confirm the existence of an SBP pathway for pentose assimilation in cellulolytic clostridia.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1625094

Journal Information:: Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Journal Issue: 7 Vol. 295; ISSN 0021-9258

Publisher:: American Society for Biochemistry and Molecular BiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (72)

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Ferredoxin:NAD ⁺ Oxidoreductase of Thermoanaerobacterium saccharolyticum and Its Role in Ethanol Formation Tian, Liang; Lo, Jonathan; Shao, Xiongjun Applied and Environmental Microbiology, Vol. 82, Issue 24 https://doi.org/10.1128/aem.02130-16	journal	September 2016
Phosphoketolase Pathway for Xylose Catabolism in Clostridium acetobutylicum Revealed by 13C Metabolic Flux Analysis Liu, L.; Zhang, L.; Tang, W. Journal of Bacteriology, Vol. 194, Issue 19 https://doi.org/10.1128/jb.00713-12	journal	August 2012
Ethanol Production by Thermophilic Bacteria: Relationship Between Fermentation Product Yields of and Catabolic Enzyme Activities in Clostridium thermocellum and Thermoanaerobium brockii Lamed, R.; Zeikus, J. G. Journal of Bacteriology, Vol. 144, Issue 2 https://doi.org/10.1128/jb.144.2.569-578.1980	journal	January 1980
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Time-resolved metabolomics reveals metabolic modulation in rice foliage Sato, Shigeru; Arita, Masanori; Soga, Tomoyoshi BMC Systems Biology, Vol. 2, Issue 1 https://doi.org/10.1186/1752-0509-2-51	journal	January 2008
Transcriptomic and proteomic analyses of core metabolism in Clostridium termitidis CT1112 during growth on α-cellulose, xylan, cellobiose and xylose Munir, Riffat I.; Spicer, Victor; Krokhin, Oleg V. BMC Microbiology, Vol. 16, Issue 1 https://doi.org/10.1186/s12866-016-0711-x	journal	May 2016
Development of a core Clostridium thermocellum kinetic metabolic model consistent with multiple genetic perturbations Dash, Satyakam; Khodayari, Ali; Zhou, Jilai Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0792-2	journal	May 2017
Targeted redox and energy cofactor metabolomics in Clostridium thermocellum and Thermoanaerobacterium saccharolyticum Sander, Kyle; Asano, Keiji G.; Bhandari, Deepak Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0960-4	journal	November 2017
Sedoheptulose-7-phosphate kinase activity of phosphofructokinase from the different tissues of rabbit Karadsheh, Naif S.; Tejwani, Gopi A.; Ramaiah, Abburi Biochimica et Biophysica Acta (BBA) - Enzymology, Vol. 327, Issue 1 https://doi.org/10.1016/0005-2744(73)90104-6	journal	November 1973
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Glycolysis without pyruvate kinase in Clostridium thermocellum Olson, Daniel G.; Hörl, Manuel; Fuhrer, Tobias Metabolic Engineering, Vol. 39 https://doi.org/10.1016/j.ymben.2016.11.011	journal	January 2017
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Quantitative Isotope-Dilution High-Resolution-Mass-Spectrometry Analysis of Multiple Intracellular Metabolites in Clostridium autoethanogenum with Uniformly ¹³ C-Labeled Standards Derived from Spirulina Schatschneider, Sarah; Abdelrazig, Salah; Safo, Laudina Analytical Chemistry, Vol. 90, Issue 7 https://doi.org/10.1021/acs.analchem.7b04758	journal	March 2018
Converting Transaldolase into Aldolase through Swapping of the Multifunctional Acid–Base Catalyst: Common and Divergent Catalytic Principles in F6P Aldolase and Transaldolase Sautner, Viktor; Friedrich, Mascha Miriam; Lehwess-Litzmann, Anja Biochemistry, Vol. 54, Issue 29 https://doi.org/10.1021/acs.biochem.5b00283	journal	July 2015
Anaerobic microbial metabolism can proceed close to thermodynamic limits Jackson, Bradley E.; McInerney, Michael J. Nature, Vol. 415, Issue 6870 https://doi.org/10.1038/415454a	journal	January 2002
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Characterization of the pyrophosphate-dependent 6-phosphofructokinase from Methylococcus capsulatus Bath Reshetnikov, Alexander S.; Rozova, Olga N.; Khmelenina, Valentina N. FEMS Microbiology Letters, Vol. 288, Issue 2 https://doi.org/10.1111/j.1574-6968.2008.01366.x	journal	November 2008
Investigating the Central Metabolism of Clostridium thermosuccinogenes Koendjbiharie, Jeroen Girwar; Wiersma, Kilian; van Kranenburg, Richard Applied and Environmental Microbiology, Vol. 84, Issue 13 https://doi.org/10.1128/AEM.00363-18	journal	April 2018
Ferredoxin:NAD ⁺ Oxidoreductase of Thermoanaerobacterium saccharolyticum and Its Role in Ethanol Formation Tian, Liang; Lo, Jonathan; Shao, Xiongjun Applied and Environmental Microbiology, Vol. 82, Issue 24 https://doi.org/10.1128/AEM.02130-16	journal	September 2016
Atypical Glycolysis in Clostridium thermocellum Zhou, Jilai; Olson, Daniel G.; Argyros, D. Aaron Applied and Environmental Microbiology, Vol. 79, Issue 9, p. 3000-3008 https://doi.org/10.1128/AEM.04037-12	journal	February 2013
Phosphoketolase Pathway for Xylose Catabolism in Clostridium acetobutylicum Revealed by 13C Metabolic Flux Analysis Liu, L.; Zhang, L.; Tang, W. Journal of Bacteriology, Vol. 194, Issue 19 https://doi.org/10.1128/JB.00713-12	journal	August 2012
Ethanol Production by Thermophilic Bacteria: Relationship Between Fermentation Product Yields of and Catabolic Enzyme Activities in Clostridium thermocellum and Thermoanaerobium brockii Lamed, R.; Zeikus, J. G. Journal of Bacteriology, Vol. 144, Issue 2 https://doi.org/10.1128/JB.144.2.569-578.1980	journal	January 1980
Different Physiological Roles of ATP- and PPi-Dependent Phosphofructokinase Isoenzymes in the Methylotrophic Actinomycete Amycolatopsis methanolica Alves, A. M. C. R.; Euverink, G. J. W.; Santos, H. Journal of Bacteriology, Vol. 183, Issue 24 https://doi.org/10.1128/JB.183.24.7231-7240.2001	journal	December 2001
Microbial Cellulose Utilization: Fundamentals and Biotechnology Lynd, L. R.; Weimer, P. J.; van Zyl, W. H. Microbiology and Molecular Biology Reviews, Vol. 66, Issue 3, p. 506-577 https://doi.org/10.1128/MMBR.66.3.506-577.2002	journal	September 2002
Ethanol Production by Thermophilic Bacteria: Relationship Between Fermentation Product Yields of and Catabolic Enzyme Activities in Clostridium thermocellum and Thermoanaerobium brockii Lamed, R.; Zeikus, J. G. Journal of Bacteriology, Vol. 144, Issue 2 https://doi.org/10.1128/jb.144.2.569-578.1980	journal	January 1980
Enhanced whole genome sequence and annotation of Clostridium stercorarium DSM8532T using RNA-seq transcriptomics and high-throughput proteomics Schellenberg, John J.; Verbeke, Tobin J.; McQueen, Peter BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-567	journal	January 2014
Proteomic analysis of Clostridium thermocellum core metabolism: relative protein expression profiles and growth phase-dependent changes in protein expression Rydzak, Thomas; McQueen, Peter D.; Krokhin, Oleg V. BMC Microbiology, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2180-12-214	journal	January 2012
Time-resolved metabolomics reveals metabolic modulation in rice foliage Sato, Shigeru; Arita, Masanori; Soga, Tomoyoshi BMC Systems Biology, Vol. 2, Issue 1 https://doi.org/10.1186/1752-0509-2-51	journal	January 2008
Transcriptomic and proteomic analyses of core metabolism in Clostridium termitidis CT1112 during growth on α-cellulose, xylan, cellobiose and xylose Munir, Riffat I.; Spicer, Victor; Krokhin, Oleg V. BMC Microbiology, Vol. 16, Issue 1 https://doi.org/10.1186/s12866-016-0711-x	journal	May 2016
Development of a core Clostridium thermocellum kinetic metabolic model consistent with multiple genetic perturbations Dash, Satyakam; Khodayari, Ali; Zhou, Jilai Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0792-2	journal	May 2017
Targeted redox and energy cofactor metabolomics in Clostridium thermocellum and Thermoanaerobacterium saccharolyticum Sander, Kyle; Asano, Keiji G.; Bhandari, Deepak Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0960-4	journal	November 2017
Assessing Cofactor Usage in Pseudoclostridium thermosuccinogenes via Heterologous Expression of Central Metabolic Enzymes Koendjbiharie, Jeroen Girwar; Wevers, Kimberly; van Kranenburg, Richard Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01162	journal	May 2019
Transcriptomic and proteomic analyses of core metabolism in Clostridium termitidis CT1112 during growth on α-cellulose, xylan, cellobiose and xylose Munir, Riffat; Spicer, Victor; Krokhin, Oleg Figshare https://doi.org/10.6084/m9.figshare.c.3601997.v1	collection	January 2016
Development of a core Clostridium thermocellum kinetic metabolic model consistent with multiple genetic perturbations [Supplemental Data] Khodayari, Ali; Holwerda, Evert; Olson, Daniel figshare-Supplementary information for journal article at DOI: 10.1186/s13068-017-0792-2, 3 files https://doi.org/10.6084/m9.figshare.c.3769784	collection	May 2017

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Title: The pentose phosphate pathway of cellulolytic clostridia relies on 6-phosphofructokinase instead of transaldolase

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