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

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 pote

Authors:
; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
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)
OSTI Identifier:
1774636
DOE Contract Number:  
AC02-06CH11357
Resource Type:
Journal Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 117; Journal Issue: 17
Country of Publication:
United States
Language:
English
Subject:
Pseudomonas putida; biological funneling; extracellular vesicle; lignin valorization; outer membrane vesicle

Citation Formats

Salvachua, Davinia, Werner, Allison, Michalska, Martyna, Black, Brenna A., Donohoe, Bryon S., Haugen, Stefan J., Ramirez, Kelsey J., Amore, Antonella, and Laible, Philip D. Outer membrane vesicles catabolize lignin-derived aromatic compounds in Pseudomonas putida KT2440. United States: N. p., 2020. Web. doi:10.1073/pnas.1921073117.
Salvachua, Davinia, Werner, Allison, Michalska, Martyna, Black, Brenna A., Donohoe, Bryon S., Haugen, Stefan J., Ramirez, Kelsey J., Amore, Antonella, & Laible, Philip D. Outer membrane vesicles catabolize lignin-derived aromatic compounds in Pseudomonas putida KT2440. United States. https://doi.org/10.1073/pnas.1921073117
Salvachua, Davinia, Werner, Allison, Michalska, Martyna, Black, Brenna A., Donohoe, Bryon S., Haugen, Stefan J., Ramirez, Kelsey J., Amore, Antonella, and Laible, Philip D. 2020. "Outer membrane vesicles catabolize lignin-derived aromatic compounds in Pseudomonas putida KT2440". United States. https://doi.org/10.1073/pnas.1921073117.
@article{osti_1774636,
title = {Outer membrane vesicles catabolize lignin-derived aromatic compounds in Pseudomonas putida KT2440},
author = {Salvachua, Davinia and Werner, Allison and Michalska, Martyna and Black, Brenna A. and Donohoe, Bryon S. and Haugen, Stefan J. and Ramirez, Kelsey J. and Amore, Antonella and Laible, Philip D.},
abstractNote = {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},
doi = {10.1073/pnas.1921073117},
url = {https://www.osti.gov/biblio/1774636}, journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 17,
volume = 117,
place = {United States},
year = {Tue Apr 28 00:00:00 EDT 2020},
month = {Tue Apr 28 00:00:00 EDT 2020}
}

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