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

Davinia Salvachua, Allison Werner, Isabel Pardo, Martyna Michalska, Brenna Black, Bryon Donohoe, Stefan Haugen, Rui Katahira, Sandra Notonier, Kelsey Ramirez, Antonella Amore, Samuel Purvine, Erika Zink, Paul Abraham, Richard Giannone, Suresh Poudel, Philip Laible, Robert Hettich, Gregg Beckham

Research output: Contribution to journalArticlepeer-review

86 Scopus Citations

Abstract

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 potentially be useful tools for synthetic biology and biotechnological applications.

Original languageAmerican English
Pages (from-to)9302-9310
Number of pages9
JournalProceedings of the National Academy of Sciences of the United States of America
Volume117
Issue number17
DOIs
StatePublished - 28 Apr 2020

Bibliographical note

Publisher Copyright:
© 2020 National Academy of Sciences. All rights reserved.

NREL Publication Number

  • NREL/JA-5100-76402

Keywords

  • Biological funneling
  • Extracellular vesicle
  • Lignin valorization
  • Outer membrane vesicle
  • Pseudomonas putida

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