Trimethylamine N -oxide metabolism by abundant marine heterotrophic bacteria
Open accessAbstract
Trimethylamine N-oxide (TMAO) is a common osmolyte found in a variety of marine biota and has been detected at nanomolar concentrations in oceanic surface waters. TMAO can serve as an important nutrient for ecologically important marine heterotrophic bacteria, particularly the SAR11 clade and marine Roseobacter clade (MRC). However, the enzymes responsible for TMAO catabolism and the membrane transporter required for TMAO uptake into microbial cells have yet to be identified. We show here that the enzyme TMAO demethylase (Tdm) catalyzes the first step in TMAO degradation. This enzyme represents a large group of proteins with an uncharacterized domain (DUF1989). The function of TMAO demethylase in a representative from the SAR11 clade (strain HIMB59) and in a representative of the MRC (Ruegeria pomeroyi DSS-3) was confirmed by heterologous expression of tdm (the gene encoding Tdm) in Escherichia coli. In R. pomeroyi, mutagenesis experiments confirmed that tdm is essential for growth on TMAO. We also identified a unique ATP-binding cassette transporter (TmoXWV) found in a variety of marine bacteria and experimentally confirmed its specificity for TMAO through marker exchange mutagenesis and lacZ reporter assays of the promoter for genes encoding this transporter. Both Tdm and TmoXWV are particularly abundant in natural seawater assemblages and actively expressed, as indicated by a number of recent metatranscriptomic and metaproteomic studies. These data suggest that TMAO represents a significant, yet overlooked, nutrient for marine bacteria.
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TMAO is found in tissues of marine organisms including marine elasmobranch, where it protects against adverse effects of temperature, salinity, high urea and hydrostatic pressure.
“It is frequently found in the tissues of a variety of marine organisms [1] including marine elasmobranch, in which TMAO is known to protect against the adverse effects of temperature, salinity, high urea and hydrostatic pressure.”
From Trimethylamine N-oxide: the good, the bad and the unknown. (2016) · cites this paper as [1]
TMAO accumulates in the tissues of marine animals in high concentrations and protects against the protein-destabilizing effects of urea.
“It accumulates in the tissue of marine animals in high concentrations and protects against the protein-destabilizing effects of urea.”
From Trimethylamine N-oxide: the good, the bad and the unknown. (2016) · cites this paper as [1]
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Trimethylamine N-oxide: the good, the bad and the unknown.
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- Authors
- Lidbury, I., Murrell, J. C., & Chen, Y.
- Affiliations
- University of Warwick (GB)
- University of East Anglia (GB)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2014-02-03
- Volume
- 111
- Issue
- 7
- Pages
- 2710-2715
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3932874
- OpenAlex
- W2144909959
- Cited by
- 162
- References
- 53
- Citations by year
- 2026: 9 · 2025: 14 · 2024: 12 · 2023: 19 · 2022: 14 · 2021: 19 · 2020: 10 · 2019: 14 · 2018: 12 · 2017: 7 · 2016: 15 · 2015: 11 · 2014: 6
- FWCI
- 11.29
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Warwick Research Archive Portal (University of Warwick) (acceptedVersion)
- University of Birmingham Research Portal (University of Birmingham) (submittedVersion)
- UEA Digital Repository (University of East Anglia) (submittedVersion)
- Funders
- Natural Environment Research Council (NE/E011438/1, NE/H016236/1, 1094958)
- Topics
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial metabolism and enzyme function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- trimethylamine N-oxide, SAR11 clade, Ruegeria pomeroyi, ABC transporters, osmolyte metabolism, marine heterotrophic bacteria, heterologous expression
- MeSH terms
- Escherichia coli, Marine Biology, Methylamines, Oxidoreductases, N-Demethylating, Seawater, Mutagenesis, ATP-Binding Cassette Transporters, Alphaproteobacteria, Heterotrophic Processes
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