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Simultaneous catabolism of plant-derived aromatic compounds results in enhanced growth for members of the Roseobacter lineage.

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, including Sagittula stellata E-37, utilize aromatic compounds as primary growth substrates. The genome sequence of S. stellata contains 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 in S. stellata when 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 that S. stellata simultaneously catabolized both substrates. Furthermore, enhanced growth rates were observed when S. stellata was 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 pomeroyi DSS-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.

SUBMITTER: Gulvik CA

PROVIDER: S-EPMC3675927 | biostudies-literature | 2013 Jun

REPOSITORIES: biostudies-literature

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Simultaneous catabolism of plant-derived aromatic compounds results in enhanced growth for members of the Roseobacter lineage.

Gulvik Christopher A CA Buchan Alison A

Applied and environmental microbiology 20130405 12

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, including Sagittula stellata E-37, utilize aromatic compounds as primary growth substrates. The genome sequence of S. stellata contains multiple, potentially c ...[more]

PMID: 23563956

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Project description:The production of biofuels from lignocellulose yields a substantial lignin by-product stream that currently has few applications. Biological conversion of lignin-derived compounds into chemicals and fuels has the potential to improve the economics of lignocellulose-derived biofuels, but few microbes are able both to catabolize lignin-derived aromatic compounds and to generate valuable products. While Escherichia coli has been engineered to produce a variety of fuels and chemicals, it is incapable of catabolizing most aromatic compounds. Therefore, we engineered E. coli to catabolize protocatechuate, a common intermediate in lignin degradation, as the sole source of carbon and energy via heterologous expression of a nine-gene pathway from Pseudomonas putida KT2440. We next used experimental evolution to select for mutations that increased growth with protocatechuate more than 2-fold. Increasing the strength of a single ribosome binding site in the heterologous pathway was sufficient to recapitulate the increased growth. After optimization of the core pathway, we extended the pathway to enable catabolism of a second model compound, 4-hydroxybenzoate. These engineered strains will be useful platforms to discover, characterize, and optimize pathways for conversions of lignin-derived aromatics.IMPORTANCE Lignin is a challenging substrate for microbial catabolism due to its polymeric and heterogeneous chemical structure. Therefore, engineering microbes for improved catabolism of lignin-derived aromatic compounds will require the assembly of an entire network of catabolic reactions, including pathways from genetically intractable strains. Constructing defined pathways for aromatic compound degradation in a model host would allow rapid identification, characterization, and optimization of novel pathways. We constructed and optimized one such pathway in E. coli to enable catabolism of a model aromatic compound, protocatechuate, and then extended the pathway to a related compound, 4-hydroxybenzoate. This optimized strain can now be used as the basis for the characterization of novel pathways.

Dataset Information

Simultaneous catabolism of plant-derived aromatic compounds results in enhanced growth for members of the Roseobacter lineage.

Publications

Simultaneous catabolism of plant-derived aromatic compounds results in enhanced growth for members of the Roseobacter lineage.

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