Thermochemical wastewater valorization via enhanced microbial toxicity tolerance

Jayakody, Lahiru N.; Johnson, Christopher W.; Whitham, Jason M.; Giannone, Richard J.; Black, Brenna A.; Cleveland, Nicholas S.; Klingeman, Dawn Marie; Michener, William E.; Olstad, Jessica L.; Vardon, Derek R.; Brown, Robert C.; Brown, Steven D.; Hettich, Robert L.; Guss, Adam M.; Beckham, Gregg T.

doi:10.1039/c8ee00460a

Title: Thermochemical wastewater valorization via enhanced microbial toxicity tolerance

Journal Article · Tue Apr 17 00:00:00 EDT 2018 · Energy & Environmental Science

DOI:https://doi.org/10.1039/c8ee00460a· OSTI ID:1542241

^[1];

^[2];

^[2]; Black, Brenna A. ^[1]; Cleveland, Nicholas S. ^[1];

^[2]; Michener, William E. ^[1]; Olstad, Jessica L. ^[1];

^[1];

^[3];

^[4];

^[2];

^[1]

National Renewable Energy Lab. (NREL), Golden, CO (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Iowa State Univ., Ames, IA (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); LanzaTech, Inc., Skokie, IL (United States)

Thermochemical (TC) biomass conversion processes such as pyrolysis and liquefaction generate considerable amounts of wastewater, which often contains highly toxic compounds that are incredibly challenging to convert via standard wastewater treatment approaches such as anaerobic digestion. These streams represent a cost for TC biorefineries, and a potential valorization opportunity, if effective conversion methods are developed. The primary challenge hindering microbial conversion of TC wastewater is toxicity. In this study, we employ a robust bacterium, Pseudomonas putida, with TC wastewater streams to demonstrate that aldehydes are the most inhibitory compounds in these streams. Proteomics, transcriptomics, and fluorescence-based immunoassays of P. putida grown in a representative wastewater stream indicate that stress results from protein damage, which we hypothesize is a primary toxicity mechanism. Constitutive overexpression of the chaperone genes, groEL, groES, and clpB, in a genome-reduced P. putida strain improves the tolerance towards multiple TC wastewater samples up to 200-fold. Moreover, the concentration ranges of TC wastewater are industrially relevant for further bioprocess development for all wastewater streams examined here, representing different TC process configurations. Furthermore, we demonstrate proof-of-concept polyhydroxyalkanoate production from the usable carbon in an exemplary TC wastewater stream. Altogether, this study demonstrates that protein quality control machinery and repair mechanisms can enable substantial gains in microbial tolerance to highly toxic substrates, including heterogeneous waste streams. When coupled to other metabolic engineering advances such as expanded substrate utilization and enhanced product accumulation, this study generally enables new strategies for biological conversion of highly-toxic, organic-rich wastewater via engineered aerobic monocultures or designer consortia.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725; AC36-08GO28308; AC02-05CH11231

OSTI ID:: 1542241

Alternate ID(s):: OSTI ID: 1434804

Report Number(s):: NREL/JA-2A00-71485; EESNBY

Journal Information:: Energy & Environmental Science, Vol. 11, Issue 6; ISSN 1754-5692

Publisher:: Royal Society of ChemistryCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 65 works

Citation information provided by
Web of Science

References (113)

Biosynthesis of poly(3-hydroxydecanoate) and 3-hydroxydodecanoate dominating polyhydroxyalkanoates by β-oxidation pathway inhibited Pseudomonas putida Liu, Qian; Luo, Ge; Zhou, Xin Rong Metabolic Engineering, Vol. 13, Issue 1 https://doi.org/10.1016/j.ymben.2010.10.004	journal	January 2011
In-silico-driven metabolic engineering of Pseudomonas putida for enhanced production of poly-hydroxyalkanoates Poblete-Castro, Ignacio; Binger, Danielle; Rodrigues, Andre Metabolic Engineering, Vol. 15 https://doi.org/10.1016/j.ymben.2012.10.004	journal	January 2013
Production of bioenergy and biochemicals from industrial and agricultural wastewater Angenent, Largus T.; Karim, Khursheed; Al-Dahhan, Muthanna H. Trends in Biotechnology, Vol. 22, Issue 9 https://doi.org/10.1016/j.tibtech.2004.07.001	journal	September 2004
Molecular Chaperone Functions in Protein Folding and Proteostasis Kim, Yujin E.; Hipp, Mark S.; Bracher, Andreas Annual Review of Biochemistry, Vol. 82, Issue 1 https://doi.org/10.1146/annurev-biochem-060208-092442	journal	June 2013
Pseudomonas 2.0: genetic upgrading of P. putida KT2440 as an enhanced host for heterologous gene expression Martínez-García, Esteban; Nikel, Pablo I.; Aparicio, Tomás Microbial Cell Factories, Vol. 13, Issue 1 https://doi.org/10.1186/s12934-014-0159-3	journal	November 2014
A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: Application for DNA fragment transfer between chromosomes and plasmid transformation Choi, Kyoung-Hee; Kumar, Ayush; Schweizer, Herbert P. Journal of Microbiological Methods, Vol. 64, Issue 3 https://doi.org/10.1016/j.mimet.2005.06.001	journal	March 2006
Toward a Semisynthetic Stress Response System To Engineer Microbial Solvent Tolerance Zingaro, Kyle A.; Papoutsakis, Eleftherios Terry mBio, Vol. 3, Issue 5 https://doi.org/10.1128/mBio.00308-12	journal	October 2012
The Phosphotransferase System Formed by PtsP, PtsO, and PtsN Proteins Controls Production of Polyhydroxyalkanoates in Pseudomonas putida Velazquez, F.; Pfluger, K.; Cases, I. Journal of Bacteriology, Vol. 189, Issue 12 https://doi.org/10.1128/JB.00033-07	journal	April 2007
SignalP 4.0: discriminating signal peptides from transmembrane regions Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar Nature Methods, Vol. 8, Issue 10 https://doi.org/10.1038/nmeth.1701	journal	September 2011
Engineering glutathione biosynthesis of Saccharomyces cerevisiae increases robustness to inhibitors in pretreated lignocellulosic materials Ask, Magnus; Mapelli, Valeria; Höck, Heidi Microbial Cell Factories, Vol. 12, Issue 1 https://doi.org/10.1186/1475-2859-12-87	journal	January 2013
Microalgae fermentation of acetic acid-rich pyrolytic bio-oil: Reducing bio-oil toxicity by alkali treatment Zhao, Xuefei; Chi, Zhanyou; Rover, Marjorie Environmental Progress & Sustainable Energy, Vol. 32, Issue 4 https://doi.org/10.1002/ep.11813	journal	July 2013
The Path Forward for Biofuels and Biomaterials Ragauskas, Arthur J.; Williams, Charlotte K.; Davison, Brian H. Science, Vol. 311, Issue 5760, p. 484-489 https://doi.org/10.1126/science.1114736	journal	January 2006
Molecular Analysis of a Plasmid-encoded Phenol Hydroxylase from Pseudomonas CF600 Shingler, V.; Franklin, F. C. H.; Tsuda, M. Microbiology, Vol. 135, Issue 5 https://doi.org/10.1099/00221287-135-5-1083	journal	May 1989
Biotechnological domestication of pseudomonads using synthetic biology Nikel, Pablo I.; Martínez-García, Esteban; de Lorenzo, Víctor Nature Reviews Microbiology, Vol. 12, Issue 5 https://doi.org/10.1038/nrmicro3253	journal	April 2014
Development of a high efficiency integration system and promoter library for rapid modification of Pseudomonas putida KT2440 Elmore, Joshua R.; Furches, Anna; Wolff, Gara N. Metabolic Engineering Communications, Vol. 5 https://doi.org/10.1016/j.meteno.2017.04.001	journal	December 2017
Pyrolysis of biomass to produce fuels and chemical feedstocks Yaman, Serdar Energy Conversion and Management, Vol. 45, Issue 5 https://doi.org/10.1016/S0196-8904(03)00177-8	journal	March 2004
Glycolaldehyde causes DNA-protein crosslinks: a new aspect of ethylene oxide genotoxicity Hengstler, Jan Georg; Fuchs, Jürgen; Gebhard, Susanne Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, Vol. 304, Issue 2 https://doi.org/10.1016/0027-5107(94)90215-1	journal	January 1994
The effects of phenol and some alkyl phenolics on batch anaerobic methanogenesis Fedorak, Phillip M.; Hrudey, Steve E. Water Research, Vol. 18, Issue 3 https://doi.org/10.1016/0043-1354(84)90113-1	journal	January 1984
How biotech can transform biofuels Lynd, Lee R.; Laser, Mark S.; Bransby, David Nature Biotechnology, Vol. 26, Issue 2, p. 169-172 https://doi.org/10.1038/nbt0208-169	journal	February 2008
Aldehydes with high and low toxicities inactivate cells by damaging distinct cellular targets Xie, Ming-Zhang; Shoulkamy, Mahmoud I.; Salem, Amir M. H. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, Vol. 786 https://doi.org/10.1016/j.mrfmmm.2016.02.005	journal	April 2016
The Techno-Economic Basis for Coproduct Manufacturing To Enable Hydrocarbon Fuel Production from Lignocellulosic Biomass Biddy, Mary J.; Davis, Ryan; Humbird, David ACS Sustainable Chemistry & Engineering, Vol. 4, Issue 6 https://doi.org/10.1021/acssuschemeng.6b00243	journal	May 2016
Ethylene Glycol Metabolism by Pseudomonas putida Mückschel, Björn; Simon, Oliver; Klebensberger, Janosch Applied and Environmental Microbiology, Vol. 78, Issue 24 https://doi.org/10.1128/AEM.02062-12	journal	September 2012
Review: Mechanisms of Disaggregation and Refolding of Stable Protein Aggregates by Molecular Chaperones Ben-Zvi, Anat Peres; Goloubinoff, Pierre Journal of Structural Biology, Vol. 135, Issue 2 https://doi.org/10.1006/jsbi.2001.4352	journal	August 2001
The Growth of Bacterial Cultures Monod, J. Annual Review of Microbiology, Vol. 3, Issue 1 https://doi.org/10.1146/annurev.mi.03.100149.002103	journal	October 1949
Chaperone machines for protein folding, unfolding and disaggregation Saibil, Helen Nature Reviews Molecular Cell Biology, Vol. 14, Issue 10 https://doi.org/10.1038/nrm3658	journal	September 2013
A systematic survey of in vivo obligate chaperonin-dependent substrates Fujiwara, Kei; Ishihama, Yasushi; Nakahigashi, Kenji The EMBO Journal, Vol. 29, Issue 9 https://doi.org/10.1038/emboj.2010.52	journal	April 2010
Structural basis for intersubunit signaling in a protein disaggregating machine Biter, A. B.; Lee, S.; Sung, N. Proceedings of the National Academy of Sciences, Vol. 109, Issue 31 https://doi.org/10.1073/pnas.1207040109	journal	July 2012
Vergärung von Flash-Pyrolyseöl aus Holz zu Biogas Willner, T.; Scherer, P.; Meier, D. Chemie Ingenieur Technik, Vol. 76, Issue 6 https://doi.org/10.1002/cite.200403359	journal	June 2004
Genome-wide RNAi screen reveals the E3 SUMO-protein ligase gene SIZ1 as a novel determinant of furfural tolerance in Saccharomyces cerevisiae Xiao, Han; Zhao, Huimin Biotechnology for Biofuels, Vol. 7, Issue 1 https://doi.org/10.1186/1754-6834-7-78	journal	January 2014
Conversion of levoglucosan and cellobiosan by Pseudomonas putida KT2440 Linger, Jeffrey G.; Hobdey, Sarah E.; Franden, Mary Ann Metabolic Engineering Communications, Vol. 3 https://doi.org/10.1016/j.meteno.2016.01.005	journal	December 2016
Molecular mechanisms of yeast tolerance and in situ detoxification of lignocellulose hydrolysates Liu, Z. Lewis Applied Microbiology and Biotechnology, Vol. 90, Issue 3 https://doi.org/10.1007/s00253-011-3167-9	journal	March 2011
GroESL overexpression imparts Escherichia coli tolerance to i-, n-, and 2-butanol, 1,2,4-butanetriol and ethanol with complex and unpredictable patterns Zingaro, Kyle A.; Terry Papoutsakis, Eleftherios Metabolic Engineering, Vol. 15 https://doi.org/10.1016/j.ymben.2012.07.009	journal	January 2013
A microbial polyhydroxyalkanoates (PHA) based bio- and materials industry Chen, Guo-Qiang Chemical Society Reviews, Vol. 38, Issue 8 https://doi.org/10.1039/b812677c	journal	January 2009
Solvent-tolerant bacteria in biocatalysis de Bont, J. Trends in Biotechnology, Vol. 16, Issue 12 https://doi.org/10.1016/S0167-7799(98)01234-7	journal	December 1998
Anaerobic digestion in global bio-energy production: Potential and research challenges Appels, Lise; Lauwers, Joost; Degrève, Jan Renewable and Sustainable Energy Reviews, Vol. 15, Issue 9 https://doi.org/10.1016/j.rser.2011.07.121	journal	December 2011
Industrial biotechnology of Pseudomonas putida and related species Poblete-Castro, Ignacio; Becker, Judith; Dohnt, Katrin Applied Microbiology and Biotechnology, Vol. 93, Issue 6 https://doi.org/10.1007/s00253-012-3928-0	journal	February 2012
SUMO expression shortens the lag phase of Saccharomyces cerevisiae yeast growth caused by complex interactive effects of major mixed fermentation inhibitors found in hot-compressed water-treated lignocellulosic hydrolysate Jayakody, Lahiru N.; Kadowaki, Masafumi; Tsuge, Keisuke Applied Microbiology and Biotechnology, Vol. 99, Issue 1 https://doi.org/10.1007/s00253-014-6174-9	journal	October 2014
Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network Goloubinoff, P.; Mogk, A.; Zvi, A. P. B. Proceedings of the National Academy of Sciences, Vol. 96, Issue 24 https://doi.org/10.1073/pnas.96.24.13732	journal	November 1999
Production of Clean Pyrolytic Sugars for Fermentation Rover, Marjorie R.; Johnston, Patrick A.; Jin, Tao ChemSusChem, Vol. 7, Issue 6, p. 1662-1668 https://doi.org/10.1002/cssc.201301259	journal	April 2014
Chemical Processing in High-Pressure Aqueous Environments. 8. Improved Catalysts for Hydrothermal Gasification Elliott, Douglas C.; Hart, Todd R.; Neuenschwander, Gary G. Industrial & Engineering Chemistry Research, Vol. 45, Issue 11 https://doi.org/10.1021/ie060031o	journal	May 2006
Allelic exchange in Escherichia coli using the Bacillus subtilis sacB gene and a temperature-sensitive pSC101 replicon Blomfield, I. C.; Vaughn, V.; Rest, R. F. Molecular Microbiology, Vol. 5, Issue 6, p. 1447-1457 https://doi.org/10.1111/j.1365-2958.1991.tb00791.x	journal	June 1991
Molecular Mechanisms of Aldehyde Toxicity: A Chemical Perspective LoPachin, Richard M.; Gavin, Terrence Chemical Research in Toxicology, Vol. 27, Issue 7 https://doi.org/10.1021/tx5001046	journal	June 2014
Engineering solventogenic clostridia Papoutsakis, Eleftherios T. Current Opinion in Biotechnology, Vol. 19, Issue 5, p. 420-429 https://doi.org/10.1016/j.copbio.2008.08.003	journal	October 2008
Engineering Escherichia coli membrane phospholipid head distribution improves tolerance and production of biorenewables Tan, Zaigao; Khakbaz, Pouyan; Chen, Yingxi Metabolic Engineering, Vol. 44 https://doi.org/10.1016/j.ymben.2017.08.006	journal	November 2017
The metabolic cost of flagellar motion in P seudomonas putida KT2440 : Cost vs. benefit of Martínez-García, Esteban; Nikel, Pablo I.; Chavarría, Max Environmental Microbiology, Vol. 16, Issue 1 https://doi.org/10.1111/1462-2920.12309	journal	November 2013
Biochar enables anaerobic digestion of aqueous phase from intermediate pyrolysis of biomass Torri, Cristian; Fabbri, Daniele Bioresource Technology, Vol. 172, p. 335-341 https://doi.org/10.1016/j.biortech.2014.09.021	journal	November 2014
Integration of pyrolysis and anaerobic digestion – Use of aqueous liquor from digestate pyrolysis for biogas production Hübner, Tobias; Mumme, Jan Bioresource Technology, Vol. 183 https://doi.org/10.1016/j.biortech.2015.02.037	journal	May 2015
Measurement of Emissions from Air Pollution Sources. 3. C ₁ −C ₂₉ Organic Compounds from Fireplace Combustion of Wood Schauer, James J.; Kleeman, Michael J.; Cass, Glen R. Environmental Science & Technology, Vol. 35, Issue 9 https://doi.org/10.1021/es001331e	journal	May 2001
A review of imperative technologies for wastewater treatment II: hybrid methods Gogate, Parag R.; Pandit, Aniruddha B. Advances in Environmental Research, Vol. 8, Issue 3-4 https://doi.org/10.1016/S1093-0191(03)00031-5	journal	March 2004
MutY catalytic core, mutant and bound adenine structures define specificity for DNA repair enzyme superfamily Guan, Yue; Manuel, Raymond C.; Arvai, Andrew S. Nature Structural Biology, Vol. 5, Issue 12 https://doi.org/10.1038/4168	journal	December 1998
Fermentation of levoglucosan with oleaginous yeasts for lipid production Lian, Jieni; Garcia-Perez, Manuel; Chen, Shulin Bioresource Technology, Vol. 133 https://doi.org/10.1016/j.biortech.2013.01.031	journal	April 2013
Conversion and assimilation of furfural and 5-(hydroxymethyl)furfural by Pseudomonas putida KT2440 Guarnieri, Michael T.; Ann Franden, Mary; Johnson, Christopher W. Metabolic Engineering Communications, Vol. 4 https://doi.org/10.1016/j.meteno.2017.02.001	journal	June 2017
Engineering ethanologenic Escherichia coli for levoglucosan utilization Layton, Donovan S.; Ajjarapu, Avanthi; Choi, Dong Won Bioresource Technology, Vol. 102, Issue 17 https://doi.org/10.1016/j.biortech.2011.06.011	journal	September 2011
Hybrid thermochemical processing: fermentation of pyrolysis-derived bio-oil Jarboe, Laura R.; Wen, Zhiyou; Choi, DongWon Applied Microbiology and Biotechnology, Vol. 91, Issue 6 https://doi.org/10.1007/s00253-011-3495-9	journal	July 2011
Principles of ubiquitin and SUMO modifications in DNA repair Bergink, Steven; Jentsch, Stefan Nature, Vol. 458, Issue 7237 https://doi.org/10.1038/nature07963	journal	March 2009
A comparative view of metabolite and substrate stress and tolerance in microbial bioprocessing: From biofuels and chemicals, to biocatalysis and bioremediation Nicolaou, Sergios A.; Gaida, Stefan M.; Papoutsakis, Eleftherios T. Metabolic Engineering, Vol. 12, Issue 4 https://doi.org/10.1016/j.ymben.2010.03.004	journal	July 2010
Crosstalk between SUMO and Ubiquitin on PCNA Is Mediated by Recruitment of the Helicase Srs2p Papouli, Efterpi; Chen, Shuhua; Davies, Adelina A. Molecular Cell, Vol. 19, Issue 1 https://doi.org/10.1016/j.molcel.2005.06.001	journal	July 2005
Aromatic Production from Catalytic Fast Pyrolysis of Biomass-Derived Feedstocks Carlson, Torren R.; Tompsett, Geoffrey A.; Conner, William C. Topics in Catalysis, Vol. 52, Issue 3 https://doi.org/10.1007/s11244-008-9160-6	journal	January 2009
Recent advances in heterogeneous catalysts for bio-oil upgrading via “ex situ catalytic fast pyrolysis”: catalyst development through the study of model compounds Ruddy, Daniel A.; Schaidle, Joshua A.; Ferrell III, Jack R. Green Chem., Vol. 16, Issue 2 https://doi.org/10.1039/C3GC41354C	journal	January 2014
A thermochemical–biochemical hybrid processing of lignocellulosic biomass for producing fuels and chemicals Shen, Yanwen; Jarboe, Laura; Brown, Robert Biotechnology Advances, Vol. 33, Issue 8 https://doi.org/10.1016/j.biotechadv.2015.10.006	journal	December 2015
Aromatic catabolic pathway selection for optimal production of pyruvate and lactate from lignin Johnson, Christopher W.; Beckham, Gregg T. Metabolic Engineering, Vol. 28 https://doi.org/10.1016/j.ymben.2015.01.005	journal	March 2015
Yeast fermentation of carboxylic acids obtained from pyrolytic aqueous phases for lipid production Lian, Jieni; Garcia-Perez, Manuel; Coates, Ralph Bioresource Technology, Vol. 118 https://doi.org/10.1016/j.biortech.2012.05.010	journal	August 2012
Characterization of bio-oil recovered as stage fractions with unique chemical and physical properties Pollard, A. S.; Rover, M. R.; Brown, R. C. Journal of Analytical and Applied Pyrolysis, Vol. 93 https://doi.org/10.1016/j.jaap.2011.10.007	journal	January 2012
Increased tolerance and conversion of inhibitors in lignocellulosic hydrolysates by Saccharomyces cerevisiae Almeida, Joao; Modig, Tobias; Petersson, Anneli Journal of Chemical Technology & Biotechnology, Vol. 82, Issue 4, p. 340-349 https://doi.org/10.1002/jctb.1676	journal	January 2007
Broad host range vectors for stable genomic library construction Lynch, Michael D.; Gill, Ryan T. Biotechnology and Bioengineering, Vol. 94, Issue 1 https://doi.org/10.1002/bit.20836	journal	January 2006
Towards lignin consolidated bioprocessing: simultaneous lignin depolymerization and product generation by bacteria Salvachúa, Davinia; Karp, Eric M.; Nimlos, Claire T. Green Chemistry, Vol. 17, Issue 11 https://doi.org/10.1039/C5GC01165E	journal	January 2015
Beyond editing: repurposing CRISPR–Cas9 for precision genome regulation and interrogation Dominguez, Antonia A.; Lim, Wendell A.; Qi, Lei S. Nature Reviews Molecular Cell Biology, Vol. 17, Issue 1 https://doi.org/10.1038/nrm.2015.2	journal	December 2015
Aqueous Stream Characterization from Biomass Fast Pyrolysis and Catalytic Fast Pyrolysis Black, Brenna A.; Michener, William E.; Ramirez, Kelsey J. ACS Sustainable Chemistry & Engineering, Vol. 4, Issue 12 https://doi.org/10.1021/acssuschemeng.6b01766	journal	September 2016
Microbial engineering strategies to improve cell viability for biochemical production Lo, Tat-Ming; Teo, Wei Suong; Ling, Hua Biotechnology Advances, Vol. 31, Issue 6 https://doi.org/10.1016/j.biotechadv.2013.02.001	journal	November 2013
Engineering microbes for tolerance to next-generation biofuels Dunlop, Mary J. Biotechnology for Biofuels, Vol. 4, Issue 1 https://doi.org/10.1186/1754-6834-4-32	journal	January 2011
Reaction of glycolaldehyde with proteins: latent crosslinking potential of alpha-hydroxyaldehydes. Acharya, A. S.; Manning, J. M. Proceedings of the National Academy of Sciences, Vol. 80, Issue 12 https://doi.org/10.1073/pnas.80.12.3590	journal	June 1983
Dissecting a complex chemical stress: chemogenomic profiling of plant hydrolysates Skerker, Jeffrey M.; Leon, Dacia; Price, Morgan N. Molecular Systems Biology, Vol. 9, Issue 1 https://doi.org/10.1038/msb.2013.30	journal	January 2013
Improved Stress Tolerance of GroESL-Overproducing Lactococcus lactis and Probiotic Lactobacillus paracasei NFBC 338 Desmond, C.; Fitzgerald, G. F.; Stanton, C. Applied and Environmental Microbiology, Vol. 70, Issue 10 https://doi.org/10.1128/AEM.70.10.5929-5936.2004	journal	October 2004
Cellulosic hydrolysate toxicity and tolerance mechanisms in Escherichia coli Mills, Tirzah Y.; Sandoval, Nicholas R.; Gill, Ryan T. Biotechnology for Biofuels, Vol. 2, Issue 1, Article No. 26 https://doi.org/10.1186/1754-6834-2-26	journal	January 2009
A perspective on oxygenated species in the refinery integration of pyrolysis oil Talmadge, Michael S.; Baldwin, Robert M.; Biddy, Mary J. Green Chem., Vol. 16, Issue 2 https://doi.org/10.1039/C3GC41951G	journal	January 2014
Characterization and Catalytic Upgrading of Aqueous Stream Carbon from Catalytic Fast Pyrolysis of Biomass Starace, Anne K.; Black, Brenna A.; Lee, David D. ACS Sustainable Chemistry & Engineering, Vol. 5, Issue 12 https://doi.org/10.1021/acssuschemeng.7b03344	journal	November 2017
From dirt to industrial applications: Pseudomonas putida as a Synthetic Biology chassis for hosting harsh biochemical reactions Nikel, Pablo I.; Chavarría, Max; Danchin, Antoine Current Opinion in Chemical Biology, Vol. 34 https://doi.org/10.1016/j.cbpa.2016.05.011	journal	October 2016
Lignin valorization through integrated biological funneling and chemical catalysis Linger, J. G.; Vardon, D. R.; Guarnieri, M. T. Proceedings of the National Academy of Sciences, Vol. 111, Issue 33, p. 12013-12018 https://doi.org/10.1073/pnas.1410657111	journal	August 2014
Chaperone-based procedure to increase yields of soluble recombinant proteins produced in E. coli de Marco, Ario; Deuerling, Elke; Mogk, Axel BMC Biotechnology, Vol. 7, Issue 1 https://doi.org/10.1186/1472-6750-7-32	journal	January 2007
Identification and detoxification of glycolaldehyde, an unattended bioethanol fermentation inhibitor Jayakody, Lahiru N.; Ferdouse, Jannatul; Hayashi, Nobuyuki Critical Reviews in Biotechnology, Vol. 37, Issue 2 https://doi.org/10.3109/07388551.2015.1128877	journal	December 2015
Eliminating a global regulator of carbon catabolite repression enhances the conversion of aromatic lignin monomers to muconate in Pseudomonas putida KT2440 Johnson, Christopher W.; Abraham, Paul E.; Linger, Jeffrey G. Metabolic Engineering Communications, Vol. 5 https://doi.org/10.1016/j.meteno.2017.05.002	journal	December 2017
A review of imperative technologies for wastewater treatment I: oxidation technologies at ambient conditions Gogate, Parag R.; Pandit, Aniruddha B. Advances in Environmental Research, Vol. 8, Issue 3-4 https://doi.org/10.1016/S1093-0191(03)00032-7	journal	March 2004
Overliming detoxification of pyrolytic sugar syrup for direct fermentation of levoglucosan to ethanol Chi, Zhanyou; Rover, Marjorie; Jun, Erin Bioresource Technology, Vol. 150 https://doi.org/10.1016/j.biortech.2013.09.138	journal	December 2013
Of sizzling steaks and DNA repair Dingler, Felix A.; Patel, Ketan J. Science, Vol. 357, Issue 6347 https://doi.org/10.1126/science.aan8293	journal	July 2017
Improved adaptation to heat, cold, and solvent tolerance in Lactobacillus plantarum Fiocco, D.; Capozzi, V.; Goffin, P. Applied Microbiology and Biotechnology, Vol. 77, Issue 4 https://doi.org/10.1007/s00253-007-1228-x	journal	October 2007
Overexpression of groESL in Clostridium acetobutylicum Results in Increased Solvent Production and Tolerance, Prolonged Metabolism, and Changes in the Cell's Transcriptional Program Tomas, C. A.; Welker, N. E.; Papoutsakis, E. T. Applied and Environmental Microbiology, Vol. 69, Issue 8 https://doi.org/10.1128/AEM.69.8.4951-4965.2003	journal	August 2003
Chemical Processing in High-Pressure Aqueous Environments. 6. Demonstration of Catalytic Gasification for Chemical Manufacturing Wastewater Cleanup in Industrial Plants Elliott, Douglas C.; Neuenschwander, Gary G.; Phelps, Max R. Industrial & Engineering Chemistry Research, Vol. 38, Issue 3 https://doi.org/10.1021/ie980525o	journal	March 1999
Recent advances in systems metabolic engineering tools and strategies Chae, Tong Un; Choi, So Young; Kim, Je Woong Current Opinion in Biotechnology, Vol. 47 https://doi.org/10.1016/j.copbio.2017.06.007	journal	October 2017
Regulation of oxidative DNA damage repair by DNA polymerase and MutYH by cross-talk of phosphorylation and ubiquitination Markkanen, E.; van Loon, B.; Ferrari, E. Proceedings of the National Academy of Sciences, Vol. 109, Issue 2 https://doi.org/10.1073/pnas.1110449109	journal	December 2011
Anaerobic digestion of wastes containing pyrolignitic acids Andreoni, V.; Bonfanti, P.; Daffonchio, D. Biological Wastes, Vol. 34, Issue 3 https://doi.org/10.1016/0269-7483(90)90022-K	journal	January 1990
13C nuclear magnetic resonance studies of Pseudomonas putida fatty acid metabolic routes involved in poly(3-hydroxyalkanoate) synthesis. Huijberts, G. N.; de Rijk, T. C.; de Waard, P. Journal of Bacteriology, Vol. 176, Issue 6 https://doi.org/10.1128/jb.176.6.1661-1666.1994	journal	March 1994
A functional metagenomic approach for expanding the synthetic biology toolbox for biomass conversion Sommer, Morten OA; Church, George M.; Dantas, Gautam Molecular Systems Biology, Vol. 6, Issue 1 https://doi.org/10.1038/msb.2010.16	journal	January 2010
Green Fluorescent Protein (GFP): Applications, Structure, and Related Photophysical Behavior Zimmer, Marc Chemical Reviews, Vol. 102, Issue 3 https://doi.org/10.1021/cr010142r	journal	March 2002
Activity of the hybrid trp-lac (tac) promoter of Escherichia coli in Pseudomonas putida. Construction of broad-host-range, controlled-expression vectors Bagdasarian, Miroslawa M.; Amann, Egon; Lurz, Rudolf Gene, Vol. 26, Issue 2-3 https://doi.org/10.1016/0378-1119(83)90197-X	journal	December 1983
Adipic acid production from lignin Vardon, Derek R.; Franden, Mary Ann; Johnson, Christopher W. Energy & Environmental Science, Vol. 8, Issue 2 https://doi.org/10.1039/C4EE03230F	journal	January 2015
Aggresomes, inclusion bodies and protein aggregation Kopito, Ron R. Trends in Cell Biology, Vol. 10, Issue 12 https://doi.org/10.1016/S0962-8924(00)01852-3	journal	December 2000
Advanced Oxidation Processes in Water/Wastewater Treatment: Principles and Applications. A Review Oturan, Mehmet A.; Aaron, Jean-Jacques Critical Reviews in Environmental Science and Technology, Vol. 44, Issue 23 https://doi.org/10.1080/10643389.2013.829765	journal	September 2014
Separation, hydrolysis and fermentation of pyrolytic sugars to produce ethanol and lipids Lian, Jieni; Chen, Shulin; Zhou, Shuai Bioresource Technology, Vol. 101, Issue 24 https://doi.org/10.1016/j.biortech.2010.07.071	journal	December 2010
Tolerance engineering in bacteria for the production of advanced biofuels and chemicals Mukhopadhyay, Aindrila Trends in Microbiology, Vol. 23, Issue 8 https://doi.org/10.1016/j.tim.2015.04.008	journal	August 2015
Multiple gated cardiac blood pool imaging for left ventricular ejection fraction: Validation of the technique and assessment of variability Wackers, Frans J. Th.; Berger, Harvey J.; Johnstone, David E. The American Journal of Cardiology, Vol. 43, Issue 6 https://doi.org/10.1016/0002-9149(79)90148-6	journal	June 1979
Microbial biotechnology and circular economy in wastewater treatment Nielsen, Per Halkjaer Microbial Biotechnology, Vol. 10, Issue 5 https://doi.org/10.1111/1751-7915.12821	journal	August 2017
Enhancing muconic acid production from glucose and lignin-derived aromatic compounds via increased protocatechuate decarboxylase activity Johnson, Christopher W.; Salvachúa, Davinia; Khanna, Payal Metabolic Engineering Communications, Vol. 3 https://doi.org/10.1016/j.meteno.2016.04.002	journal	December 2016
Catalytic pyrolysis of biomass for biofuels production French, Richard; Czernik, Stefan Fuel Processing Technology, Vol. 91, Issue 1 https://doi.org/10.1016/j.fuproc.2009.08.011	journal	January 2010
Fermentation of lignocellulosic hydrolysates. II: inhibitors and mechanisms of inhibition Palmqvist, Eva; Hahn-Hägerdal, Bärbel Bioresource Technology, Vol. 74, Issue 1, p. 25-33 https://doi.org/10.1016/S0960-8524(99)00161-3	journal	August 2000
Linking pyrolysis and anaerobic digestion (Py-AD) for the conversion of lignocellulosic biomass Fabbri, Daniele; Torri, Cristian Current Opinion in Biotechnology, Vol. 38 https://doi.org/10.1016/j.copbio.2016.02.004	journal	April 2016
Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum Schäfer, Andreas; Tauch, Andreas; Jäger, Wolfgang Gene, Vol. 145, Issue 1, p. 69-73 https://doi.org/10.1016/0378-1119(94)90324-7	journal	July 1994
The Heat Shock Response: Life on the Verge of Death Richter, Klaus; Haslbeck, Martin; Buchner, Johannes Molecular Cell, Vol. 40, Issue 2 https://doi.org/10.1016/j.molcel.2010.10.006	journal	October 2010
Instability and decay of the primary structure of DNA Lindahl, Tomas Nature, Vol. 362, Issue 6422 https://doi.org/10.1038/362709a0	journal	April 1993
The HSP70 chaperone machinery: J proteins as drivers of functional specificity Kampinga, Harm H.; Craig, Elizabeth A. Nature Reviews Molecular Cell Biology, Vol. 11, Issue 8 https://doi.org/10.1038/nrm2941	journal	August 2010
Mechanisms of membrane toxicity of hydrocarbons. Sikkema, J.; de Bont, J. A.; Poolman, B. Microbiological reviews, Vol. 59, Issue 2 https://doi.org/10.1128/MMBR.59.2.201-222.1995	journal	January 1995
Pseudomonas putida KT2442 cultivated on glucose accumulates poly(3-hydroxyalkanoates) consisting of saturated and unsaturated monomers. Huijberts, G. N.; Eggink, G.; de Waard, P. Applied and Environmental Microbiology, Vol. 58, Issue 2 https://doi.org/10.1128/AEM.58.2.536-544.1992	journal	January 1992
Pyrolysis of Biomass to Produce Fuels and Chemical Feedstocks Yaman, Serdar ChemInform, Vol. 35, Issue 31 https://doi.org/10.1002/chin.200431298	journal	August 2004
Regulation of oxidative DNA damage repair by DNA polymerase λ and MutYH by cross-talk of phosphorylation and ubiquitination Markkanen, E.; Van Loon, B.; Ferrari, E. National Academy of Sciences https://doi.org/10.5167/uzh-56816	text	January 2012

Cited By (4)

Promoting microbial utilization of phenolic substrates from bio-oil Davis, Kirsten; Rover, Marjorie R.; Salvachúa, Davinia Journal of Industrial Microbiology & Biotechnology, Vol. 46, Issue 11 https://doi.org/10.1007/s10295-019-02208-z	journal	July 2019
Pseudomonas putida KT 2440 is HV 1 certified, not GRAS Kampers, Linde F. C.; Volkers, Rita J. M.; Martins dos Santos, Vitor A. P. Microbial Biotechnology, Vol. 12, Issue 5 https://doi.org/10.1111/1751-7915.13443	journal	June 2019
Recent advances in lignin valorization with bacterial cultures: microorganisms, metabolic pathways, and bio-products Xu, Zhaoxian; Lei, Peng; Zhai, Rui Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1376-0	journal	February 2019
Passive membrane transport of lignin-related compounds Vermaas, Josh V.; Dixon, Richard A.; Chen, Fang Proceedings of the National Academy of Sciences, Vol. 116, Issue 46 https://doi.org/10.1073/pnas.1904643116	journal	October 2019