Journal
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Volume 117, Issue 17, Pages 9302-9310Publisher
NATL ACAD SCIENCES
DOI: 10.1073/pnas.1921073117
Keywords
extracellular vesicle; lignin valorization; outer membrane vesicle; Pseudomonas putida; biological funneling
Categories
Funding
- US Department of Energy (DOE) [DE-AC36-08GO28308]
- US DOE, Office of Energy Efficiency and Renewable Energy, Bioenergy Technologies Office
- Center for Bioenergy Innovation, a US DOE Bioenergy Research Center - Office of Biological and Environmental Research in the DOE Office of Science
- Office of Biological and Environmental Research
- Laboratory Directed Research and Development from Argonne National Laboratory by the Office of Science, of the US DOE
- Laboratory Directed Research and Development from Argonne National Laboratory by the Office of Science, of the US DOE [DE-AC02-06CH11357]
- US DOE, Office of Science, Basic Energy Sciences [DE-AC02-06CH11357]
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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.
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