Time-resolved, deuterium-based fluxomics uncovers the hierarchy and dynamics of sugar processing by Pseudomonas putida

Metabolic Engineering - Tập 79 - Trang 159-172 - 2023
Daniel C. Volke1, Nicolas Gurdo1, Riccardo Milanesi2, Pablo I. Nikel1
1The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, 2800, Kongens Lyngby, Denmark
2Department of Biotechnology and Biosciences, University of Milano-Bicocca, 20126 Milano, Italy

Tài liệu tham khảo

Allen, 2020, Tracing metabolic flux through time and space with isotope labeling experiments, Curr. Opin. Biotechnol., 64, 92, 10.1016/j.copbio.2019.11.003 Amirmozafari, 1993, Nutritional requirements for synthesis of heat-stable enterotoxin by Yersinia enterocolitica, Appl. Environ. Microbiol., 59, 3314, 10.1128/aem.59.10.3314-3320.1993 An, 2016, Regulation of pyrroloquinoline quinone-dependent glucose dehydrogenase activity in the model rhizosphere-dwelling bacterium Pseudomonas putida KT2440, Appl. Environ. Microbiol., 82, 4955, 10.1128/AEM.00813-16 Ankenbauer, 2020, Pseudomonas putida KT2440 is naturally endowed to withstand industrial-scale stress conditions, Microb. Biotechnol., 13, 1145, 10.1111/1751-7915.13571 Bachmann, 2013, Availability of public goods shapes the evolution of competing metabolic strategies, Proc. Natl. Acad. Sci. U.S.A., 110, 14302, 10.1073/pnas.1308523110 Bagdasarian, 1981, Specific purpose plasmid cloning vectors. II. Broad host range, high copy number, RSF1010-derived vectors, and a host-vector system for gene cloning in Pseudomonas, Gene, 16, 237, 10.1016/0378-1119(81)90080-9 Bar-Even, 2012, Rethinking glycolysis: on the biochemical logic of metabolic pathways, Nat. Chem. Biol., 8, 509, 10.1038/nchembio.971 Basan, 2015, Overflow metabolism in Escherichia coli results from efficient proteome allocation, Nature, 528, 99, 10.1038/nature15765 Bednarski, 2021, In vivo 2H/13C flux analysis in metabolism research, Curr. Opin. Biotechnol., 71, 1, 10.1016/j.copbio.2021.04.005 Belda, 2016, The revisited genome of Pseudomonas putida KT2440 enlightens its value as a robust metabolic chassis, Environ. Microbiol., 18, 3403, 10.1111/1462-2920.13230 Bernal, 2016, Acetate metabolism regulation in Escherichia coli: carbon overflow, pathogenicity, and beyond, Appl. Microbiol. Biotechnol., 100, 8985, 10.1007/s00253-016-7832-x Bilbao, 2023, PeakDecoder enables machine learning-based metabolite annotation and accurate profiling in multidimensional mass spectrometry measurements, Nat. Commun., 14, 2461, 10.1038/s41467-023-37031-9 Bitzenhofer, 2021, Towards robust Pseudomonas cell factories to harbour novel biosynthetic pathways, Essays Biochem., 65, 319, 10.1042/EBC20200173 Brito, 2020, Inorganic phosphate solubilization by rhizosphere bacterium Paenibacillus sonchi: gene expression and physiological functions, Front. Microbiol., 11, 10.3389/fmicb.2020.588605 Buch, 2008, Metabolic channeling of glucose towards gluconate in phosphate-solubilizing Pseudomonas aeruginosa P4 under phosphorus deficiency, Res. Microbiol., 159, 635, 10.1016/j.resmic.2008.09.012 Bujdoš, 2023, Engineering of Pseudomonas putida for accelerated co-utilization of glucose and cellobiose yields aerobic overproduction of pyruvate explained by an upgraded metabolic model, Metab. Eng., 75, 29, 10.1016/j.ymben.2022.10.011 Butaitė, 2017, Siderophore cheating and cheating resistance shape competition for iron in soil and freshwater Pseudomonas communities, Nat. Commun., 8, 414, 10.1038/s41467-017-00509-4 Calero, 2019, Chasing bacterial chassis for metabolic engineering: a perspective review from classical to non-traditional microorganisms, Microb. Biotechnol., 12, 98, 10.1111/1751-7915.13292 Caspi, 2018, The MetaCyc database of metabolic pathways and enzymes, Nucleic Acids Res., 46, D633, 10.1093/nar/gkx935 Chavarría, 2013, The Entner-Doudoroff pathway empowers Pseudomonas putida KT2440 with a high tolerance to oxidative stress, Environ. Microbiol., 15, 1772, 10.1111/1462-2920.12069 Chen, 2016, The Entner-Doudoroff pathway is an overlooked glycolytic route in cyanobacteria and plants, Proc. Natl. Acad. Sci. U.S.A., 113, 5441, 10.1073/pnas.1521916113 Christodoulou, 2018, Reserve flux capacity in the pentose phosphate pathway enables Escherichia coli's rapid response to oxidative stress, Cell Syst, 6, 569, 10.1016/j.cels.2018.04.009 Coffee, 1972, The kinetic characterization of gluconokinase from a pseudomonad, Arch. Biochem. Biophys., 149, 549, 10.1016/0003-9861(72)90354-2 Davis, 2015, High cell density cultivation of Pseudomonas putida KT2440 using glucose without the need for oxygen enriched air supply, Biotechnol. Bioeng., 112, 725, 10.1002/bit.25474 de Kok, 2012, Energy coupling in Saccharomyces cerevisiae: selected opportunities for metabolic engineering, FEMS Yeast Res., 12, 387, 10.1111/j.1567-1364.2012.00799.x de Oliveira, 2021, Glucose metabolism in Pseudomonas aeruginosa is cyclic when producing polyhydroxyalkanoates and rhamnolipids, J. Biotechnol., 342, 54, 10.1016/j.jbiotec.2021.10.007 del Castillo, 2007, Convergent peripheral pathways catalyze initial glucose catabolism in Pseudomonas putida: genomic and flux analysis, J. Bacteriol., 189, 5142, 10.1128/JB.00203-07 Dolan, 2020, Contextual flexibility in Pseudomonas aeruginosa central carbon metabolism during growth in single carbon sources, mBio, 11, 10.1128/mBio.02684-19 Dolan, 2022, Systems-wide dissection of organic acid assimilation in Pseudomonas aeruginosa reveals a novel path to underground metabolism, mBio, 13, 10.1128/mbio.02541-22 Eisenberg, 1967, Gluconate metabolism in Escherichia coli, J. Bacteriol., 93, 941, 10.1128/jb.93.3.941-949.1967 Escobar-Turriza, 2019, Identification of functional signatures in the metabolism of the three cellular domains of life, PLoS One, 14, 10.1371/journal.pone.0217083 Fan, 2014, Quantitative flux analysis reveals folate-dependent NADPH production, Nature, 510, 298, 10.1038/nature13236 Fernández-Cabezón, 2021, Spatiotemporal manipulation of the mismatch repair system of Pseudomonas putida accelerates phenotype emergence, ACS Synth. Biol., 10, 1214, 10.1021/acssynbio.1c00031 Fernández-Cabezón, 2022, Dynamic flux regulation for high-titer anthranilate production by plasmid-free, conditionally-auxotrophic strains of Pseudomonas putida, Metab. Eng., 73, 11, 10.1016/j.ymben.2022.05.008 Fernández, 2012, Mechanisms of resistance to chloramphenicol in Pseudomonas putida KT2440, Antimicrob. Agents Chemother., 56, 1001, 10.1128/AAC.05398-11 Flamholz, 2013, Glycolytic strategy as a tradeoff between energy yield and protein cost, Proc. Natl. Acad. Sci. U.S.A., 110, 10039, 10.1073/pnas.1215283110 Fuhrer, 2005, Experimental identification and quantification of glucose metabolism in seven bacterial species, J. Bacteriol., 187, 1581, 10.1128/JB.187.5.1581-1590.2005 Hartmans, 1989, Metabolism of styrene oxide and 2-phenylethanol in the styrene-degrading Xanthobacter strain 124X, Appl. Environ. Microbiol., 55, 2850, 10.1128/aem.55.11.2850-2855.1989 Kanehisa, 2022, KEGG for taxonomy-based analysis of pathways and genomes, Nucleic Acids Res., 51, D587, 10.1093/nar/gkac963 Kelleher, 2001, Flux estimation using isotopic tracers: common ground for metabolic physiology and metabolic engineering, Metab. Eng., 3, 100, 10.1006/mben.2001.0185 Klingner, 2015, Large-scale 13C flux profiling reveals conservation of the Entner-Doudoroff pathway as a glycolytic strategy among marine bacteria that use glucose, Appl. Environ. Microbiol., 81, 2408, 10.1128/AEM.03157-14 Koebmann, 2002, The glycolytic flux in Escherichia coli is controlled by the demand for ATP, J. Bacteriol., 184, 3909, 10.1128/JB.184.14.3909-3916.2002 Kohlstedt, 2010, Metabolic fluxes and beyond—systems biology understanding and engineering of microbial metabolism, Appl. Microbiol. Biotechnol., 88, 1065, 10.1007/s00253-010-2854-2 Kohlstedt, 2019, GC-MS-based 13C metabolic flux analysis resolves the parallel and cyclic glucose metabolism of Pseudomonas putida KT2440 and Pseudomonas aeruginosa PAO1, Metab. Eng., 54, 35, 10.1016/j.ymben.2019.01.008 Latrach-Tlemçani, 2008, Physiological states and energetic adaptation during growth of Pseudomonas putida mt-2 on glucose, Arch. Microbiol., 190, 141, 10.1007/s00203-008-0380-8 Lawson, 2021, Autotrophic and mixotrophic metabolism of an anammox bacterium revealed by in vivo 13C and 2H metabolic network mapping, ISME J., 15, 673, 10.1038/s41396-020-00805-w Lehmann, 2017, A timeline of stable isotopes and mass spectrometry in the life sciences, Mass Spectrom. Rev., 36, 58, 10.1002/mas.21497 Letunic, 2021, Interactive Tree of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation, Nucleic Acids Res., 49, W293, 10.1093/nar/gkab301 Li, 2016, Probing the metabolic water contribution to intracellular water using oxygen isotope ratios of PO4, Proc. Natl. Acad. Sci. U.S.A., 113, 5862, 10.1073/pnas.1521038113 Low, 2023, Metabolic imaging with deuterium labeled substrates, Prog. Nucl. Magn. Reson. Spectrosc., 134–135, 39 Lugtenberg, 1999, What makes Pseudomonas bacteria rhizosphere competent?, Environ. Microbiol., 1, 9, 10.1046/j.1462-2920.1999.00005.x Matsushita, 2003, 5-Keto-D-gluconate production is catalyzed by a quinoprotein glycerol dehydrogenase, major polyol dehydrogenase, in Gluconobacter species, Appl. Environ. Microbiol., 69, 1959, 10.1128/AEM.69.4.1959-1966.2003 Mendler, 2019, AnnoTree: visualization and exploration of a functionally annotated microbial tree of life, Nucleic Acids Res., 47, 4442, 10.1093/nar/gkz246 Meyrat, 2019, ATP synthesis at physiological nucleotide concentrations, Sci. Rep., 9, 3070, 10.1038/s41598-019-38564-0 Niedenführ, 2015, How to measure metabolic fluxes: a taxonomic guide for 13C fluxomics, Curr. Opin. Biotechnol., 34, 82, 10.1016/j.copbio.2014.12.003 Nikaido, 2003, Molecular basis of bacterial outer membrane permeability revisited, Microbiol. Mol. Biol. Rev., 67, 593, 10.1128/MMBR.67.4.593-656.2003 Nikel, 2009, Metabolic flux analysis of Escherichia coli creB and arcA mutants reveals shared control of carbon catabolism under microaerobic growth conditions, J. Bacteriol., 191, 5538, 10.1128/JB.00174-09 Nikel, 2014, Biotechnological domestication of pseudomonads using synthetic biology, Nat. Rev. Microbiol., 12, 368, 10.1038/nrmicro3253 Nikel, 2015, Pseudomonas putida KT2440 strain metabolizes glucose through a cycle formed by enzymes of the Entner-Doudoroff, Embden-Meyerhof-Parnas, and pentose phosphate pathways, J. Biol. Chem., 290, 25920, 10.1074/jbc.M115.687749 Nikel, 2016, Pyridine nucleotide transhydrogenases enable redox balance of Pseudomonas putida during biodegradation of aromatic compounds, Environ. Microbiol., 18, 3565, 10.1111/1462-2920.13434 Nikel, 2021, Reconfiguration of metabolic fluxes in Pseudomonas putida as a response to sub-lethal oxidative stress, ISME J., 15, 1751, 10.1038/s41396-020-00884-9 Nogales, 2020, High-quality genome-scale metabolic modelling of Pseudomonas putida highlights its broad metabolic capabilities, Environ. Microbiol., 22, 255, 10.1111/1462-2920.14843 Orth, 2010, What is flux balance analysis?, Nat. Biotechnol., 28, 245, 10.1038/nbt.1614 Pedersen, 2021, High-throughput dilution-based growth method enables time-resolved exo-metabolomics of Pseudomonas putida and Pseudomonas aeruginosa, Microb. Biotechnol., 14, 2214, 10.1111/1751-7915.13905 Pfeiffer, 2001, Cooperation and competition in the evolution of ATP-producing pathways, Science, 292, 504, 10.1126/science.1058079 Phadungath, 2011, Effect of sodium gluconate on the solubility of calcium lactate, J. Dairy Sci., 94, 4843, 10.3168/jds.2011-4549 Rabinowitz, 2007, Acidic acetonitrile for cellular metabolome extraction from Escherichia coli, Anal. Chem., 79, 6167, 10.1021/ac070470c Romano, 1996, Evolution of carbohydrate metabolic pathways, Res. Microbiol., 147, 448, 10.1016/0923-2508(96)83998-2 Russell, 1995, Energetics of bacterial growth: balance of anabolic and catabolic reactions, Microbiol. Rev., 59, 48, 10.1128/mr.59.1.48-62.1995 Sambrook, 2001, Molecular cloning: a laboratory manual Sánchez-Pascuala, 2019, Functional implementation of a linear glycolysis for sugar catabolism in Pseudomonas putida, Metab. Eng., 54, 200, 10.1016/j.ymben.2019.04.005 Sandberg, 2016, Evolution of E. coli on [U-13C]-glucose reveals a negligible isotopic influence on metabolism and physiology, PLoS One, 11, 10.1371/journal.pone.0151130 Sashidhar, 2010, Mineral phosphate solubilization by rhizosphere bacteria and scope for manipulation of the direct oxidation pathway involving glucose dehydrogenase, J. Appl. Microbiol., 109, 1, 10.1111/j.1365-2672.2009.04654.x Sasnow, 2016, Bypasses in intracellular glucose metabolism in iron-limited Pseudomonas putida, Microbiol., 5, 3 Schwechheimer, 2018, Towards better understanding of industrial cell factories: novel approaches for 13C metabolic flux analysis in complex nutrient environments, Curr. Opin. Biotechnol., 54, 128, 10.1016/j.copbio.2018.07.001 Shimizu, 2019, Regulation of glycolytic flux and overflow metabolism depending on the source of energy generation for energy demand, Biotechnol. Adv., 37, 284, 10.1016/j.biotechadv.2018.12.007 Simon, 2008, The organisation of proton motive and non-proton motive redox loops in prokaryotic respiratory systems, Biochim. Biophys. Acta, 1777, 1480, 10.1016/j.bbabio.2008.09.008 Sone, 2010, Aerobic respiration in the Gram-positive bacteria, vol. 1, 35 Spaans, 2015, NADPH-generating systems in bacteria and archaea, Front. Microbiol., 6, 742, 10.3389/fmicb.2015.00742 Sweeney, 1996, Escherichia coli F-18 and E. coli K-12 eda mutants do not colonize the streptomycin-treated mouse large intestine, Infect. Immun., 64, 3504, 10.1128/iai.64.9.3504-3511.1996 Torrontegui, 1976, The uptake of 2-ketogluconate by Pseudomonas putida, Arch. Microbiol., 110, 43, 10.1007/BF00416967 Unden, 1997, Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors, Biochim. Biophys. Acta, 1320, 217, 10.1016/S0005-2728(97)00034-0 Uroz, 2020, Dual transcriptomics and proteomics analyses of the early stage of interaction between Caballeronia mineralivorans PML1(12) and mineral, Environ. Microbiol., 22, 3838, 10.1111/1462-2920.15159 Vicente, 1973, Regulation of the glucolytic enzymes in Pseudomonas putida, Arch. Microbiol., 93, 53 Vicente, 1973, Glucolysis in Pseudomonas putida: physiological role of alternative routes from the analysis of defective mutants, J. Bacteriol., 116, 908, 10.1128/jb.116.2.908-914.1973 Vicente, 1975, The uptake of glucose and gluconate by Pseudomonas putida, Mol. Cell. Biochem., 7, 59, 10.1007/BF01732164 Volke, 2020, Synthetic control of plasmid replication enables target- and self-curing of vectors and expedites genome engineering of Pseudomonas putida, Metab. Eng. Commun., 10, 10.1016/j.mec.2020.e00126 Volke, 2021, Cofactor specificity of glucose-6-phosphate dehydrogenase isozymes in Pseudomonas putida reveals a general principle underlying glycolytic strategies in bacteria, mSystems, 6, 10.1128/mSystems.00014-21 Volke, 2022, Modular (de)construction of complex bacterial phenotypes by CRISPR/nCas9-assisted, multiplex cytidine base-editing, Nat. Commun., 13, 3026, 10.1038/s41467-022-30780-z Wang, 2018, Glycolysis and its metabolic engineering applications, 1 Weimer, 2020, Industrial biotechnology of Pseudomonas putida: advances and prospects, Appl. Microbiol. Biotechnol., 104, 7745, 10.1007/s00253-020-10811-9 Wijker, 2019, 2H/1H variation in microbial lipids is controlled by NADPH metabolism, Proc. Natl. Acad. Sci. U.S.A., 116, 12173, 10.1073/pnas.1818372116 Wilkes, 2019, A cyclic metabolic network in Pseudomonas protegens Pf-5 prioritizes the Entner-Doudoroff pathway and exhibits substrate hierarchy during carbohydrate co-utilization, Appl. Environ. Microbiol., 85, 10.1128/AEM.02084-18 Winsor, 2016, Enhanced annotations and features for comparing thousands of Pseudomonas genomes in the Pseudomonas genome database, Nucleic Acids Res., 44, D646, 10.1093/nar/gkv1227 Wirth, 2020, Accelerated genome engineering of Pseudomonas putida by I-SceI―mediated recombination and CRISPR-Cas9 counterselection, Microb. Biotechnol., 13, 233, 10.1111/1751-7915.13396 Wirth, 2022, A synthetic C2 auxotroph of Pseudomonas putida for evolutionary engineering of alternative sugar catabolic routes, Metab. Eng., 74, 83, 10.1016/j.ymben.2022.09.004 Wirth, 2023, QurvE: user-friendly software for the analysis of biological growth and fluorescence data, Nat. Protoc., 10.1038/s41596-023-00850-7 Wishart, 2008, Quantitative metabolomics using NMR, Trends Anal. Chem., 27, 228, 10.1016/j.trac.2007.12.001 Zamboni, 2009, 13C-based metabolic flux analysis, Nat. Protoc., 4, 878, 10.1038/nprot.2009.58 Zhu, 2020, Biogenesis of the peptide-derived redox cofactor pyrroloquinoline quinone, Curr. Opin. Chem. Biol., 59, 93, 10.1016/j.cbpa.2020.05.001 Zotter, 2017, Quantifying enzyme activity in living cells, J. Biol. Chem., 292, 15838, 10.1074/jbc.M117.792119