Outer membrane vesicles catabolize lignin-derived aromatic compounds in Pseudomonas putida KT2440

Salvachua, Davinia; Werner, Allison; Michalska, Martyna; Black, Brenna A.; Donohoe, Bryon S.; Haugen, Stefan J.; Ramirez, Kelsey J.; Amore, Antonella; Laible, Philip D.

doi:10.1073/pnas.1921073117

Outer membrane vesicles catabolize lignin-derived aromatic compounds in Pseudomonas putida KT2440

Journal Article · Tue Apr 28 04:00:00 EDT 2020 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1921073117· OSTI ID:1774636

Salvachua, Davinia; Werner, Allison; Michalska, Martyna; Black, Brenna A.; Donohoe, Bryon S.; Haugen, Stefan J.; Ramirez, Kelsey J.; Amore, Antonella; Laible, Philip D.

Lignin is an abundant and recalcitrant component of plant cell walls. While lignin degradation in nature is typically attributed to fungi, growing evidence suggests that bacteria also catabolize this complex biopolymer. However, the spatiotemporal mechanisms for lignin catabolism remain unclear. Improved understanding of this biological process would aid in our collective knowledge of both carbon cycling and microbial strategies to valorize lignin to value-added compounds. Here, we examine lignin modifications and the exoproteome of three aromatic–catabolic bacteria: Pseudomonas putida KT2440, Rhodoccocus jostii RHA1, and Amycolatopsis sp. ATCC 39116. P. putida cultivation in lignin-rich media is characterized by an abundant exoproteome that is dynamically and selectively packaged into outer membrane vesicles (OMVs). Interestingly, many enzymes known to exhibit activity toward lignin-derived aromatic compounds are enriched in OMVs from early to late stationary phase, corresponding to the shift from bioavailable carbon to oligomeric lignin as a carbon source. In vivo and in vitro experiments demonstrate that enzymes contained in the OMVs are active and catabolize aromatic compounds. Taken together, this work supports OMV-mediated catabolism of lignin-derived aromatic compounds as an extracellular strategy for nutrient acquisition by soil bacteria and suggests that OMVs could pote

Research Organization:: Argonne National Laboratory (ANL)

Sponsoring Organization:: USDOE Office of Energy Efficiency and Renewable Energy (EERE) - Bioenergy Technologies Office (BETO); USDOE Office of Science - Office of Biological and Environmental Research; Argonne National Laboratory - Laboratory Directed Research and Development (LDRD)

DOE Contract Number:: AC02-06CH11357

OSTI ID:: 1774636

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 17 Vol. 117; ISSN 0027-8424

Country of Publication:: United States

Language:: English

References (68)

Through the wall: extracellular vesicles in Gram-positive bacteria, mycobacteria and fungi Brown, Lisa; Wolf, Julie M.; Prados-Rosales, Rafael Nature Reviews Microbiology, Vol. 13, Issue 10 https://doi.org/10.1038/nrmicro3480	journal	September 2015
Pseudomonas putida as a functional chassis for industrial biocatalysis: From native biochemistry to trans-metabolism Nikel, Pablo I.; de Lorenzo, Víctor Metabolic Engineering, Vol. 50 https://doi.org/10.1016/j.ymben.2018.05.005	journal	November 2018
Characterization of multicopper oxidase CopA from Pseudomonas putida KT2440 and Pseudomonas fluorescens Pf-5: Involvement in bacterial lignin oxidation Granja-Travez, Rommel Santiago; Bugg, Timothy D. H. Archives of Biochemistry and Biophysics, Vol. 660 https://doi.org/10.1016/j.abb.2018.10.012	journal	December 2018
Opportunities and challenges in biological lignin valorization Beckham, Gregg T.; Johnson, Christopher W.; Karp, Eric M. Current Opinion in Biotechnology, Vol. 42 https://doi.org/10.1016/j.copbio.2016.02.030	journal	December 2016
Long-Distance Delivery of Bacterial Virulence Factors by Pseudomonas aeruginosa Outer Membrane Vesicles Bomberger, Jennifer M.; MacEachran, Daniel P.; Coutermarsh, Bonita A. PLoS Pathogens, Vol. 5, Issue 4 https://doi.org/10.1371/journal.ppat.1000382	journal	April 2009
Extracellular vesicles carry cellulases in the industrial fungus Trichoderma reesei de Paula, Renato Graciano; Antoniêto, Amanda Cristina Campos; Nogueira, Karoline Maria Vieira Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1487-7	journal	June 2019
Lignin Valorization: Improving Lignin Processing in the Biorefinery Ragauskas, A. J.; Beckham, G. T.; Biddy, M. J. Science, Vol. 344, Issue 6185, p. 1246843-1246843 https://doi.org/10.1126/science.1246843	journal	May 2014
Genetic and Biochemical Investigations on Bacterial Catabolic Pathways for Lignin-Derived Aromatic Compounds Masai, Eiji; Katayama, Yoshihiro; Fukuda, Masao Bioscience, Biotechnology, and Biochemistry, Vol. 71, Issue 1 https://doi.org/10.1271/bbb.60437	journal	January 2007
The β-Ketoadipate Pathway And The Biology Of Self-Identity Harwood, Caroline S.; Parales, Rebecca E. Annual Review of Microbiology, Vol. 50, Issue 1, p. 553-590 https://doi.org/10.1146/annurev.micro.50.1.553	journal	October 1996
Post-Fermentation Recovery of Biobased Carboxylic Acids Karp, Eric M.; Cywar, Robin M.; Manker, Lorenz P. ACS Sustainable Chemistry & Engineering, Vol. 6, Issue 11 https://doi.org/10.1021/acssuschemeng.8b03703	journal	October 2018
Outer Membrane Vesicles (OMVs) of Gram-negative Bacteria: A Perspective Update Jan, Arif Tasleem Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01053	journal	June 2017
A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids Wessel, D.; Flügge, U. I. Analytical Biochemistry, Vol. 138, Issue 1 https://doi.org/10.1016/0003-2697(84)90782-6	journal	April 1984
Identification of DypB from Rhodococcus jostii RHA1 as a Lignin Peroxidase Ahmad, Mark; Roberts, Joseph N.; Hardiman, Elizabeth M. Biochemistry, Vol. 50, Issue 23 https://doi.org/10.1021/bi101892z	journal	June 2011
Lignin Biosynthesis Boerjan, Wout; Ralph, John; Baucher, Marie Annual Review of Plant Biology, Vol. 54, Issue 1, p. 519-546 https://doi.org/10.1146/annurev.arplant.54.031902.134938	journal	June 2003
Identification and Characterization of a Multifunctional Dye Peroxidase from a Lignin-Reactive Bacterium Brown, Margaret E.; Barros, Tiago; Chang, Michelle C. Y. ACS Chemical Biology, Vol. 7, Issue 12 https://doi.org/10.1021/cb300383y	journal	September 2012
Non-classical protein secretion in bacteria Bendtsen, Jannick D.; Kiemer, Lars; Fausbøll, Anders BMC Microbiology, Vol. 5, Issue 1 https://doi.org/10.1186/1471-2180-5-58	journal	October 2005
Enzymatic conversion of lignin into renewable chemicals Bugg, Timothy DH; Rahmanpour, Rahman Current Opinion in Chemical Biology, Vol. 29 https://doi.org/10.1016/j.cbpa.2015.06.009	journal	December 2015
Oxidoreductases on their way to industrial biotransformations Martínez, Angel T.; Ruiz-Dueñas, Francisco J.; Camarero, Susana Biotechnology Advances, Vol. 35, Issue 6 https://doi.org/10.1016/j.biotechadv.2017.06.003	journal	November 2017
Elucidating Tricin-Lignin Structures: Assigning Correlations in HSQC Spectra of Monocot Lignins Lan, Wu; Yue, Fengxia; Rencoret, Jorge Polymers, Vol. 10, Issue 8 https://doi.org/10.3390/polym10080916	journal	August 2018
Outer membrane vesicles from Fibrobacter succinogenes S85 contain an array of carbohydrate-active enzymes with versatile polysaccharide-degrading capacity Arntzen, Magnus Ø.; Várnai, Anikó; Mackie, Roderick I. Environmental Microbiology, Vol. 19, Issue 7 https://doi.org/10.1111/1462-2920.13770	journal	May 2017
Induction of Extracellular Hydroxyl Radical Production by White-Rot Fungi through Quinone Redox Cycling Gomez-Toribio, V.; Garcia-Martin, A. B.; Martinez, M. J. Applied and Environmental Microbiology, Vol. 75, Issue 12 https://doi.org/10.1128/AEM.02137-08	journal	April 2009
Compositional Analysis of Lignocellulosic Feedstocks. 1. Review and Description of Methods Sluiter, Justin B.; Ruiz, Raymond O.; Scarlata, Christopher J. Journal of Agricultural and Food Chemistry, Vol. 58, Issue 16, p. 9043-9053 https://doi.org/10.1021/jf1008023	journal	August 2010
The revisited genome of Pseudomonas putida KT2440 enlightens its value as a robust metabolic chassis : Re-annotation of the Pseudomonas putida KT2440 genome Belda, Eugeni; van Heck, Ruben G. A.; José Lopez-Sanchez, Maria Environmental Microbiology, Vol. 18, Issue 10 https://doi.org/10.1111/1462-2920.13230	journal	April 2016
Outer-membrane vesicles from Gram-negative bacteria: biogenesis and functions Schwechheimer, Carmen; Kuehn, Meta J. Nature Reviews Microbiology, Vol. 13, Issue 10 https://doi.org/10.1038/nrmicro3525	journal	September 2015
Bioprocess development for muconic acid production from aromatic compounds and lignin Salvachúa, Davinia; Johnson, Christopher W.; Singer, Christine A. Green Chemistry, Vol. 20, Issue 21 https://doi.org/10.1039/C8GC02519C	journal	January 2018
A commercial laccase-mediator system to delignify and improve saccharification of the fast-growing Paulownia fortunei (Seem.) Hemsl. Rencoret, Jorge; Pereira, Antonio; Marques, Gisela Holzforschung, Vol. 73, Issue 1 https://doi.org/10.1515/hf-2018-0095	journal	December 2018
Spatial-fluxomics provides a subcellular-compartmentalized view of reductive glutamine metabolism in cancer cells Lee, Won Dong; Mukha, Dzmitry; Aizenshtein, Elina Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-09352-1	journal	March 2019
The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes Floudas, Dimitrios; Binder, Manfred; Riley, Robert Science, Vol. 336, Issue 6089 https://doi.org/10.1126/science.1221748	journal	June 2012
The Entner-Doudoroff pathway empowers Pseudomonas putida KT2440 with a high tolerance to oxidative stress : Perturbing the upper metabolism of Chavarría, Max; Nikel, Pablo I.; Pérez-Pantoja, Danilo Environmental Microbiology, Vol. 15, Issue 6 https://doi.org/10.1111/1462-2920.12069	journal	January 2013
Xenobiotic Reductase A in the Degradation of Quinoline by Pseudomonas putida 86: Physiological Function, Structure and Mechanism of 8-Hydroxycoumarin Reduction Griese, Julia J.; P. Jakob, Roman; Schwarzinger, Stephan Journal of Molecular Biology, Vol. 361, Issue 1 https://doi.org/10.1016/j.jmb.2006.06.007	journal	August 2006
Mechanisms of outer membrane vesicle entry into host cells: MicroReview - OMV entry into host cells O'Donoghue, Eloise J.; Krachler, Anne Marie Cellular Microbiology, Vol. 18, Issue 11 https://doi.org/10.1111/cmi.12655	journal	September 2016
Types and origins of bacterial membrane vesicles Toyofuku, Masanori; Nomura, Nobuhiko; Eberl, Leo Nature Reviews Microbiology, Vol. 17, Issue 1 https://doi.org/10.1038/s41579-018-0112-2	journal	November 2018
Sub-atomic Resolution Crystal Structure of Cholesterol Oxidase: What Atomic Resolution Crystallography Reveals about Enzyme Mechanism and the Role of the FAD Cofactor in Redox Activity Lario, Paula I.; Sampson, Nicole; Vrielink, Alice Journal of Molecular Biology, Vol. 326, Issue 5 https://doi.org/10.1016/S0022-2836(03)00054-8	journal	March 2003
Azoreductase: a key player of xenobiotic metabolism Misal, Santosh A.; Gawai, Kachru R. Bioresources and Bioprocessing, Vol. 5, Issue 1 https://doi.org/10.1186/s40643-018-0206-8	journal	April 2018
Bacterial Nanobioreactors–Directing Enzyme Packaging into Bacterial Outer Membrane Vesicles Alves, Nathan J.; Turner, Kendrick B.; Daniele, Michael A. ACS Applied Materials & Interfaces, Vol. 7, Issue 44 https://doi.org/10.1021/acsami.5b08811	journal	October 2015
Release of outer membrane vesicles in Pseudomonas putida as a response to stress caused by cationic surfactants Marisa Heredia, Romina; Sabrina Boeris, Paola; Sebastián Liffourrena, Andrés Microbiology, Vol. 162, Issue 5 https://doi.org/10.1099/mic.0.000265	journal	May 2016
Pathways for degradation of lignin in bacteria and fungi Bugg, Timothy D. H.; Ahmad, Mark; Hardiman, Elizabeth M. Natural Product Reports, Vol. 28, Issue 12, p. 1883-1896 https://doi.org/10.1039/c1np00042j	journal	January 2011
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
Unrivalled diversity: the many roles and reactions of bacterial cytochromes P450 in secondary metabolism Greule, Anja; Stok, Jeanette E.; De Voss, James J. Natural Product Reports, Vol. 35, Issue 8 https://doi.org/10.1039/C7NP00063D	journal	January 2018
Discovery of potential pathways for biological conversion of poplar wood into lipids by co-fermentation of Rhodococci strains Li, Xiaolu; He, Yucai; Zhang, Libing Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1395-x	journal	March 2019
Genome-wide identification of tolerance mechanisms toward p -coumaric acid in Pseudomonas putida Calero, Patricia; Jensen, Sheila I.; Bojanovič, Klara Biotechnology and Bioengineering, Vol. 115, Issue 3 https://doi.org/10.1002/bit.26495	journal	November 2017
A protocatechuate biosensor for Pseudomonas putida KT2440 via promoter and protein evolution Jha, Ramesh K.; Bingen, Jeremy M.; Johnson, Christopher W. Metabolic Engineering Communications, Vol. 6 https://doi.org/10.1016/j.meteno.2018.03.001	journal	June 2018
Proteomic Characterization of the Outer Membrane Vesicle of Pseudomonas putida KT2440 Choi, Chi-Won; Park, Edmond Changkyun; Yun, Sung Ho Journal of Proteome Research, Vol. 13, Issue 10 https://doi.org/10.1021/pr500411d	journal	September 2014
The metabolic versatility of pseudomonads Clarke, Patricia H. Antonie van Leeuwenhoek, Vol. 48, Issue 2 https://doi.org/10.1007/BF00405197	journal	January 1982
Identification of distinct nanoparticles and subsets of extracellular vesicles by asymmetric flow field-flow fractionation Zhang, Haiying; Freitas, Daniela; Kim, Han Sang Nature Cell Biology, Vol. 20, Issue 3 https://doi.org/10.1038/s41556-018-0040-4	journal	February 2018
Genomic and proteomic analysis of lignin degrading and polyhydroxyalkanoate accumulating β-proteobacterium Pandoraea sp. ISTKB Kumar, Madan; Verma, Sandhya; Gazara, Rajesh Kumar Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1148-2	journal	June 2018
A field of dreams: Lignin valorization into chemicals, materials, fuels, and health-care products Becker, Judith; Wittmann, Christoph Biotechnology Advances, Vol. 37, Issue 6 https://doi.org/10.1016/j.biotechadv.2019.02.016	journal	November 2019
Protecting enzymatic function through directed packaging into bacterial outer membrane vesicles Alves, Nathan J.; Turner, Kendrick B.; Medintz, Igor L. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep24866	journal	April 2016
Microbial degradation of aromatic compounds — from one strategy to four Fuchs, Georg; Boll, Matthias; Heider, Johann Nature Reviews Microbiology, Vol. 9, Issue 11, p. 803-816 https://doi.org/10.1038/nrmicro2652	journal	October 2011
Lignin Conversion to Low-Molecular-Weight Aromatics via an Aerobic Oxidation-Hydrolysis Sequence: Comparison of Different Lignin Sources Das, Amit; Rahimi, Alireza; Ulbrich, Arne ACS Sustainable Chemistry & Engineering, Vol. 6, Issue 3 https://doi.org/10.1021/acssuschemeng.7b03541	journal	January 2018
Cellulosomes localise on the surface of membrane vesicles from the cellulolytic bacterium Clostridium thermocellum Ichikawa, Shunsuke; Ogawa, Satoru; Nishida, Ayami FEMS Microbiology Letters, Vol. 366, Issue 12 https://doi.org/10.1093/femsle/fnz145	journal	June 2019
Exo-MFA – A 13C metabolic flux analysis framework to dissect tumor microenvironment-secreted exosome contributions towards cancer cell metabolism Achreja, Abhinav; Zhao, Hongyun; Yang, Lifeng Metabolic Engineering, Vol. 43 https://doi.org/10.1016/j.ymben.2017.01.001	journal	September 2017
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
Bacterial catabolism of lignin-derived aromatics: New findings in a recent decade: Update on bacterial lignin catabolism: Bacterial catabolism of lignin-derived aromatics Kamimura, Naofumi; Takahashi, Kenji; Mori, Kosuke Environmental Microbiology Reports, Vol. 9, Issue 6 https://doi.org/10.1111/1758-2229.12597	journal	November 2017
Biogenesis of Outer Membrane Vesicles in Serratia marcescens Is Thermoregulated and Can Be Induced by Activation of the Rcs Phosphorelay System McMahon, K. J.; Castelli, M. E.; Vescovi, E. G. Journal of Bacteriology, Vol. 194, Issue 12 https://doi.org/10.1128/JB.00016-12	journal	April 2012
Lignin depolymerization by fungal secretomes and a microbial sink Salvachúa, Davinia; Katahira, Rui; Cleveland, Nicholas S. Green Chemistry, Vol. 18, Issue 22 https://doi.org/10.1039/C6GC01531J	journal	January 2016
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
Roles of Small Laccases from Streptomyces in Lignin Degradation Majumdar, Sudipta; Lukk, Tiit; Solbiati, Jose O. Biochemistry, Vol. 53, Issue 24 https://doi.org/10.1021/bi500285t	journal	June 2014
Protein selection and export via outer membrane vesicles Bonnington, K. E.; Kuehn, M. J. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1843, Issue 8 https://doi.org/10.1016/j.bbamcr.2013.12.011	journal	August 2014
The crystal structure of Pseudomonas putida azoreductase - the active site revisited Gonçalves, Ana Maria D.; Mendes, Sónia; de Sanctis, Daniele FEBS Journal, Vol. 280, Issue 24 https://doi.org/10.1111/febs.12568	journal	November 2013
Membrane Vesicle Formation as a Multiple-Stress Response Mechanism Enhances Pseudomonas putida DOT-T1E Cell Surface Hydrophobicity and Biofilm Formation Baumgarten, Thomas; Sperling, Stefanie; Seifert, Jana Applied and Environmental Microbiology, Vol. 78, Issue 17 https://doi.org/10.1128/AEM.01525-12	journal	June 2012
New dye-decolorizing peroxidases from Bacillus subtilis and Pseudomonas putida MET94: towards biotechnological applications Santos, Ana; Mendes, Sónia; Brissos, Vânia Applied Microbiology and Biotechnology, Vol. 98, Issue 5 https://doi.org/10.1007/s00253-013-5041-4	journal	July 2013
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
Whole plant cell wall characterization using solution-state 2D NMR Mansfield, Shawn D.; Kim, Hoon; Lu, Fachuang Nature Protocols, Vol. 7, Issue 9 https://doi.org/10.1038/nprot.2012.064	journal	August 2012
Bioremediation 3 . 0 : Engineering pollutant-removing bacteria in the times of systemic biology Dvořák, Pavel; Nikel, Pablo I.; Damborský, Jiří Biotechnology Advances, Vol. 35, Issue 7 https://doi.org/10.1016/j.biotechadv.2017.08.001	journal	November 2017
PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes Yu, Nancy Y.; Wagner, James R.; Laird, Matthew R. Bioinformatics, Vol. 26, Issue 13 https://doi.org/10.1093/bioinformatics/btq249	journal	May 2010
Interaction of Bacterial Membrane Vesicles with Specific Species and Their Potential for Delivery to Target Cells Tashiro, Yosuke; Hasegawa, Yusuke; Shintani, Masaki Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00571	journal	April 2017
Systems biology-guided biodesign of consolidated lignin conversion Lin, Lu; Cheng, Yanbing; Pu, Yunqiao Green Chemistry, Vol. 18, Issue 20 https://doi.org/10.1039/C6GC01131D	journal	January 2016

Cited By (1)

Additional file 2 of Understanding of bacterial lignin extracellular degradation mechanisms by Pseudomonas putida KT2440 via secretomic analysis Xu, Zhangyang; Peng, Bo; Kitata, Reta Birhanu figshare https://doi.org/10.6084/m9.figshare.21443760.v1	dataset	January 2022

Similar Records

Outer membrane vesicles catabolize lignin-derived aromatic compounds in Pseudomonas putida KT2440

Journal Article · Tue Apr 28 00:00:00 EDT 2020 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1633770

Outer Membrane Vesicles Catabolize Lignin-Derived Aromatic Compounds in Pseudomonas putida KT2440

Journal Article · Fri Apr 03 00:00:00 EDT 2020 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1659932

Outer membrane vesicles catabolize lignin-derived aromatic compounds in Pseudomonas putida KT2440

Journal Article · Thu Apr 02 20:00:00 EDT 2020 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1609045

Related Subjects

Pseudomonas putida
biological funneling
extracellular vesicle
lignin valorization
outer membrane vesicle

Outer membrane vesicles catabolize lignin-derived aromatic compounds in Pseudomonas putida KT2440

Citation Formats

References (68)

Cited By (1)

Similar Records

Related Subjects