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Title: Functional Redundancy in the Hydroxycinnamate Catabolism Pathways of the Salt Marsh Bacterium Sagittula stellata E-37

Abstract

ABSTRACT The hydroxycinnamates (HCAs) ferulate andp-coumarate are among the most abundant constituents of lignin, and their degradation by bacteria is an essential step in the remineralization of vascular plant material. Here, we investigate the catabolism of these two HCAs by the marine bacteriumSagittula stellataE-37, a member of the roseobacter lineage with lignolytic potential. Bacterial degradation of HCAs is often initiated by the activity of a hydroxycinnamoyl-coenzyme A (hydroxycinnamoyl-CoA) synthase. Genome analysis ofS. stellatarevealed the presence of two feruloyl-CoA (fcs) synthase homologs, an unusual occurrence among characterized HCA degraders. In order to elucidate the role of these homologs in HCA catabolism,fcs-1andfcs-2were disrupted using insertional mutagenesis, yielding both single and doublefcsmutants. Growth onp-coumarate was abolished in thefcsdouble mutant, whereas maximum cell yield on ferulate was only 2% of that of the wild type. Interestingly, the single mutants demonstrated opposing phenotypes, where thefcs-1mutant showed impaired growth (extended lag and ∼60% of wild-type rate) onp-coumarate, and thefcs-2mutant showed impaired growth (extended lag and ∼20% of wild-type rate) on ferulate, pointing to distinct but overlapping roles of the encodedfcshomologs, withfcs-1primarily dedicated top-coumarate utilization andfcs-2playing a dominant role in ferulate utilization. Finally, a tripartite ATP-independent periplasmic (TRAP) family transporter was found to be required for growthmore » on both HCAs. These findings provide evidence for functional redundancy in the degradation of HCAs inS. stellataE-37 and offer important insight into the genetic complexity of aromatic compound degradation in bacteria. IMPORTANCEHydroxycinnamates (HCAs) are essential components of lignin and are involved in various plant functions, including defense. In nature, microbial degradation of HCAs is influential to global carbon cycling. HCA degradation pathways are also of industrial relevance, as microbial transformation of the HCA, ferulate, can generate vanillin, a valuable flavoring compound. Yet, surprisingly little is known of the genetics underlying bacterial HCA degradation. Here, we make comparisons to previously characterized bacterial HCA degraders and use a genetic approach to characterize genes involved in catabolism and uptake of HCAs in the environmentally relevant marine bacteriumSagittula stellata. We provide evidence of overlapping substrate specificity between HCA degradation pathways and uptake proteins. We conclude thatS. stellatais uniquely poised to utilize HCAs found in the complex mixtures of plant-derived compounds in nature. This strategy may be common among marine bacteria residing in lignin-rich coastal waters and has potential relevance to biotechnology sectors.« less

Authors:
; ; ; ORCiD logo;
Publication Date:
Research Org.:
Energy Frontier Research Centers (EFRC) (United States). Center for Direct Catalytic Conversion of Biomass to Biofuels (C3Bio); Purdue Univ., West Lafayette, IN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1566724
DOE Contract Number:  
SC0000997
Resource Type:
Journal Article
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 84; Journal Issue: 23; 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

Frank, Ashley M., Chua, Michelle J., Gulvik, Christopher A., Buchan, Alison, and Pettinari, M. Julia. Functional Redundancy in the Hydroxycinnamate Catabolism Pathways of the Salt Marsh Bacterium Sagittula stellata E-37. United States: N. p., 2018. Web. doi:10.1128/aem.02027-18.
Frank, Ashley M., Chua, Michelle J., Gulvik, Christopher A., Buchan, Alison, & Pettinari, M. Julia. Functional Redundancy in the Hydroxycinnamate Catabolism Pathways of the Salt Marsh Bacterium Sagittula stellata E-37. United States. doi:10.1128/aem.02027-18.
Frank, Ashley M., Chua, Michelle J., Gulvik, Christopher A., Buchan, Alison, and Pettinari, M. Julia. Fri . "Functional Redundancy in the Hydroxycinnamate Catabolism Pathways of the Salt Marsh Bacterium Sagittula stellata E-37". United States. doi:10.1128/aem.02027-18.
@article{osti_1566724,
title = {Functional Redundancy in the Hydroxycinnamate Catabolism Pathways of the Salt Marsh Bacterium Sagittula stellata E-37},
author = {Frank, Ashley M. and Chua, Michelle J. and Gulvik, Christopher A. and Buchan, Alison and Pettinari, M. Julia},
abstractNote = {ABSTRACT The hydroxycinnamates (HCAs) ferulate andp-coumarate are among the most abundant constituents of lignin, and their degradation by bacteria is an essential step in the remineralization of vascular plant material. Here, we investigate the catabolism of these two HCAs by the marine bacteriumSagittula stellataE-37, a member of the roseobacter lineage with lignolytic potential. Bacterial degradation of HCAs is often initiated by the activity of a hydroxycinnamoyl-coenzyme A (hydroxycinnamoyl-CoA) synthase. Genome analysis ofS. stellatarevealed the presence of two feruloyl-CoA (fcs) synthase homologs, an unusual occurrence among characterized HCA degraders. In order to elucidate the role of these homologs in HCA catabolism,fcs-1andfcs-2were disrupted using insertional mutagenesis, yielding both single and doublefcsmutants. Growth onp-coumarate was abolished in thefcsdouble mutant, whereas maximum cell yield on ferulate was only 2% of that of the wild type. Interestingly, the single mutants demonstrated opposing phenotypes, where thefcs-1mutant showed impaired growth (extended lag and ∼60% of wild-type rate) onp-coumarate, and thefcs-2mutant showed impaired growth (extended lag and ∼20% of wild-type rate) on ferulate, pointing to distinct but overlapping roles of the encodedfcshomologs, withfcs-1primarily dedicated top-coumarate utilization andfcs-2playing a dominant role in ferulate utilization. Finally, a tripartite ATP-independent periplasmic (TRAP) family transporter was found to be required for growth on both HCAs. These findings provide evidence for functional redundancy in the degradation of HCAs inS. stellataE-37 and offer important insight into the genetic complexity of aromatic compound degradation in bacteria. IMPORTANCEHydroxycinnamates (HCAs) are essential components of lignin and are involved in various plant functions, including defense. In nature, microbial degradation of HCAs is influential to global carbon cycling. HCA degradation pathways are also of industrial relevance, as microbial transformation of the HCA, ferulate, can generate vanillin, a valuable flavoring compound. Yet, surprisingly little is known of the genetics underlying bacterial HCA degradation. Here, we make comparisons to previously characterized bacterial HCA degraders and use a genetic approach to characterize genes involved in catabolism and uptake of HCAs in the environmentally relevant marine bacteriumSagittula stellata. We provide evidence of overlapping substrate specificity between HCA degradation pathways and uptake proteins. We conclude thatS. stellatais uniquely poised to utilize HCAs found in the complex mixtures of plant-derived compounds in nature. This strategy may be common among marine bacteria residing in lignin-rich coastal waters and has potential relevance to biotechnology sectors.},
doi = {10.1128/aem.02027-18},
journal = {Applied and Environmental Microbiology},
issn = {0099-2240},
number = 23,
volume = 84,
place = {United States},
year = {2018},
month = {9}
}

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