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Title: Simultaneous Catabolism of Plant-Derived Aromatic Compounds Results in Enhanced Growth for Members of the Roseobacter Lineage

Abstract

ABSTRACT Plant-derived aromatic compounds are important components of the dissolved organic carbon pool in coastal salt marshes, and their mineralization by resident bacteria contributes to carbon cycling in these systems. Members of the roseobacter lineage of marine bacteria are abundant in coastal salt marshes, and several characterized strains, includingSagittula stellataE-37, utilize aromatic compounds as primary growth substrates. The genome sequence ofS. stellatacontains multiple, potentially competing, aerobic ring-cleaving pathways. Preferential hierarchies in substrate utilization and complex transcriptional regulation have been demonstrated to be the norm in many soil bacteria that also contain multiple ring-cleaving pathways. The purpose of this study was to ascertain whether substrate preference exists inS. stellatawhen the organism is provided a mixture of aromatic compounds that proceed through different ring-cleaving pathways. We focused on the protocatechuate (pca) and the aerobic benzoyl coenzyme A (box) pathways and the substrates known to proceed through them,p-hydroxybenzoate (POB) and benzoate, respectively. When these two substrates were provided at nonlimiting carbon concentrations, temporal patterns of cell density, gene transcript abundance, enzyme activity, and substrate concentrations indicated thatS. stellatasimultaneously catabolized both substrates. Furthermore, enhanced growth rates were observed whenS. stellatawas provided both compounds simultaneously compared to the rates of cells grown singly with anmore » equimolar concentration of either substrate alone. This simultaneous-catabolism phenotype was also demonstrated in another lineage member,Ruegeria pomeroyiDSS-3. These findings challenge the paradigm of sequential aromatic catabolism reported for soil bacteria and contribute to the growing body of physiological evidence demonstrating the metabolic versatility of roseobacters.« less

Authors:
;
Publication Date:
Research Org.:
Energy Frontier Research Centers (EFRC) (United States). Center for Direct Catalytic Conversion of Biomass to Biofuels (C3Bio)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1385755
DOE Contract Number:  
SC000997
Resource Type:
Journal Article
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 79; Journal Issue: 12; Related Information: C3Bio partners with Purdue University (lead); Argonne National Laboratory; National Renewable Energy Laboratory; Northeastern University; University of Tennessee; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
catalysis (homogeneous), catalysis (heterogeneous), biofuels (including algae and biomass), bio-inspired, materials and chemistry by design, synthesis (self-assembly), synthesis (scalable processing)

Citation Formats

Gulvik, Christopher A., and Buchan, Alison. Simultaneous Catabolism of Plant-Derived Aromatic Compounds Results in Enhanced Growth for Members of the Roseobacter Lineage. United States: N. p., 2013. Web. doi:10.1128/AEM.00405-13.
Gulvik, Christopher A., & Buchan, Alison. Simultaneous Catabolism of Plant-Derived Aromatic Compounds Results in Enhanced Growth for Members of the Roseobacter Lineage. United States. doi:10.1128/AEM.00405-13.
Gulvik, Christopher A., and Buchan, Alison. Fri . "Simultaneous Catabolism of Plant-Derived Aromatic Compounds Results in Enhanced Growth for Members of the Roseobacter Lineage". United States. doi:10.1128/AEM.00405-13.
@article{osti_1385755,
title = {Simultaneous Catabolism of Plant-Derived Aromatic Compounds Results in Enhanced Growth for Members of the Roseobacter Lineage},
author = {Gulvik, Christopher A. and Buchan, Alison},
abstractNote = {ABSTRACT Plant-derived aromatic compounds are important components of the dissolved organic carbon pool in coastal salt marshes, and their mineralization by resident bacteria contributes to carbon cycling in these systems. Members of the roseobacter lineage of marine bacteria are abundant in coastal salt marshes, and several characterized strains, includingSagittula stellataE-37, utilize aromatic compounds as primary growth substrates. The genome sequence ofS. stellatacontains multiple, potentially competing, aerobic ring-cleaving pathways. Preferential hierarchies in substrate utilization and complex transcriptional regulation have been demonstrated to be the norm in many soil bacteria that also contain multiple ring-cleaving pathways. The purpose of this study was to ascertain whether substrate preference exists inS. stellatawhen the organism is provided a mixture of aromatic compounds that proceed through different ring-cleaving pathways. We focused on the protocatechuate (pca) and the aerobic benzoyl coenzyme A (box) pathways and the substrates known to proceed through them,p-hydroxybenzoate (POB) and benzoate, respectively. When these two substrates were provided at nonlimiting carbon concentrations, temporal patterns of cell density, gene transcript abundance, enzyme activity, and substrate concentrations indicated thatS. stellatasimultaneously catabolized both substrates. Furthermore, enhanced growth rates were observed whenS. stellatawas provided both compounds simultaneously compared to the rates of cells grown singly with an equimolar concentration of either substrate alone. This simultaneous-catabolism phenotype was also demonstrated in another lineage member,Ruegeria pomeroyiDSS-3. These findings challenge the paradigm of sequential aromatic catabolism reported for soil bacteria and contribute to the growing body of physiological evidence demonstrating the metabolic versatility of roseobacters.},
doi = {10.1128/AEM.00405-13},
journal = {Applied and Environmental Microbiology},
issn = {0099-2240},
number = 12,
volume = 79,
place = {United States},
year = {2013},
month = {4}
}