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Trimethylamine N-Oxide Metabolism by Abundant Marine Heterotrophic Bacteria

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Trimethylamine N-Oxide Metabolism by Abundant Marine Heterotrophic Bacteria Trimethylamine N-oxide metabolism by abundant marine heterotrophic bacteria Ian Lidburya, J. Colin Murrellb, and Yin Chena,1 aSchool of Life Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom; and bSchool of Environmental Sciences, University of East Anglia, Norwich NR4 7TJ, United Kingdom Edited* by Mary E. Lidstrom, University of Washington, Seattle, WA, and approved January 8, 2014 (received for review September 27, 2013) Trimethylamine N-oxide (TMAO) is a common osmolyte found in marine bacteria are not known. It has previously been suggested a variety of marine biota and has been detected at nanomolar that in Methylocella silvestris, a TMA-degrading soil bacterium, an concentrations in oceanic surface waters. TMAO can serve as an aminotransferase protein containing a conserved C-terminal tet- important nutrient for ecologically important marine heterotro- rahydrofolate (THF)-binding domain (Msil_3603) is probably in- phic bacteria, particularly the SAR11 clade and marine Roseobacter volved in the metabolism of TMAO, because this polypeptide was clade (MRC). However, the enzymes responsible for TMAO catab- highly enriched in TMA-grown cells and TMAO is a known in- termediate of TMA metabolism by TMA monooxygenase, Tmm, olism and the membrane transporter required for TMAO uptake + in this bacterium (TMA + NADPH + O + H → TMAO + H O + into microbial cells have yet to be identified. We show here that + 2 2 the enzyme TMAO demethylase (Tdm) catalyzes the first step in NADP ) (13). It is hypothesized that TMAO is further metab- TMAO degradation. This enzyme represents a large group of pro- olized to ammonium and formaldehyde, which serve as N and teins with an uncharacterized domain (DUF1989). The function C/energy sources, respectively, for this bacterium (13). ATP-binding cassette (ABC) transporters form one of the of TMAO demethylase in a representative from the SAR11 clade largest gene superfamilies found within many bacterial genomes (strain HIMB59) and in a representative of the MRC (Ruegeria pom- (14), and their expression is frequently detected in the marine eroyi DSS-3) was confirmed by heterologous expression of tdm environment (15–17). ABC transporters are essential for bacte- (the gene encoding Tdm) in Escherichia coli.InR. pomeroyi, muta- ria because they are responsible for the uptake of a wide range of genesis experiments confirmed that tdm is essential for growth on compounds, such as sugars, amino acids, metals, and vitamins, at TMAO. We also identified a unique ATP-binding cassette transporter the expense of ATP (18). They usually consist of three subunits: MICROBIOLOGY (TmoXWV) found in a variety of marine bacteria and experimentally a transmembrane domain that is bound to an inner membrane- confirmed its specificity for TMAO through marker exchange muta- bound ATP-binding domain and a periplasmic substrate-binding genesis and lacZ reporter assays of the promoter for genes encoding protein (SBP), which binds a given ligand. SBPs confer substrate this transporter. Both Tdm and TmoXWV are particularly abundant specificity and can bind their ligands with very high affinity (19, in natural seawater assemblages and actively expressed, as indi- 20). One group of ABC transporters specialize in the uptake of cated by a number of recent metatranscriptomic and metaproteomic compatible osmolytes and structurally related compounds, such studies. These data suggest that TMAO represents a significant, yet as glycine betaine (GBT), choline, carnitine, and proline betaine overlooked, nutrient for marine bacteria. (21, 22). These transporters either function in osmoregulation (23) or play a role in substrate catabolism (19). A bacterial ATP- TMAO transporter | nitrogenous osmolyte | methylated amine metabolism | dependent TMAO transporter has been identified (24), but the marine nitrogen cycle genes encoding this transport system are unknown. The SAR11 clade (Pelagibacteraceae) and the marine Rose- obacter clade (MRC, Rhodobacteraceae) are two groups of ma- rimethylamine N-oxide (TMAO) frequently occurs in the rine bacteria that differ in their ecology, but both play important Ttissues of a variety of marine biota (1) and is predicted to roles in marine C, S, and N cycles (25–27). Bacteria of the have a number of important physiological roles (2). In marine SAR11 clade bacteria dominate low-nutrient environments, elasmobranchs (sharks and rays), TMAO accumulates at high have streamlined genomes, are generally slow-growing and have concentrations (up to 500 mM), helping to offset the destabi- lizing effects of urea on cellular proteins (1, 3, 4). TMAO can be Significance metabolized to small methylated amines, for example, tri-, di-, and monomethylamine (TMA, DMA, and MMA, respectively). These volatile organic N compounds are precursors of marine Trimethylamine N-oxide (TMAO) is a nitrogen-containing osmo- aerosols and the potent greenhouse gas nitrous oxide in the lyte found in a wide variety of marine biota and has been de- marine atmosphere (5). In anoxic sediments or pockets of hyp- tected at nanomolar concentrations in surface seawaters. This oxic conditions, such as in marine snow, they are precursors for study provides the first genetic and biochemical evidence for the potent greenhouse gas methane (6). In marine surface uptake and catabolism of TMAO by marine heterotrophic bac- waters, TMAO concentrations can reach up to 79 nM; however, teria that are abundant in the oceans. The genes conferring the owing to the technical difficulties associated with quantifying ability of bacteria to catabolize TMAO we identified in this study TMAO in seawater, reports of in situ concentrations of TMAO are highly expressed in the marine environment and can be used are limited (7, 8). In a previously published study in which as functional biomarkers to better understand oceanic microbial- TMAO and TMA were quantified in the marine environment, mediated carbon and nitrogen cycles. Our data suggest that TMAO had a higher average concentration throughout the water TMAO represents a significant, yet overlooked, nutrient for ma- column and over a seasonal cycle (8). rine bacteria in the surface oceans. TMAO is a well-studied terminal electron acceptor for an- aerobic microbial respiration (9, 10), but its catabolism in aer- Author contributions: Y.C. designed research; I.L. performed research; I.L., J.C.M., and Y.C. obic surface seawater is not well understood. Recent studies have analyzed data; and I.L., J.C.M., and Y.C. wrote the paper. shown that TMAO in the Sargasso Sea is predominantly oxidized The authors declare no conflict of interest. by bacterioplankton as an energy source (11) and that the marine *This Direct Submission article had a prearranged editor. methylotrophic bacterium Methylophilales sp. HTCC2181 oxidizes 1To whom correspondence should be addressed. E-mail: [email protected]. TMAO to CO2 to generate energy (12). However, the genes and This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. enzymes responsible for the metabolism and uptake of TMAO by 1073/pnas.1317834111/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1317834111 PNAS Early Edition | 1of6 Downloaded by guest on September 26, 2021 distinct auxotrophic requirements for certain compounds (28–30). cells expressing the putative Tdm from R. pomeroyi produced 984 ± In contrast, bacteria of the MRC have larger genomes, display high 45 μM DMA in the culture medium (Fig. 2B), confirming that metabolic versatility, can live a particle-associated lifestyle, and SPO1562 does indeed encode for a Tdm. E. coli cells transformed often represent a large proportion of the metabolically active with vector, pET28a alone, did not produce DMA. bacterial community in coastal oceans (25, 31–34). Ecologically To determine whether SPO1562 is required for growth of R. relevant representatives of the MRC are readily cultivated and pomeroyi on TMAO, this gene was mutated. As predicted, the amenable to genetic manipulation, thereby making them good mutant (Δtdm::Gm) could not grow on TMAO or its upstream model organisms to investigate bacterial ecophysiology in the ma- precursor TMA (Fig. 1B), although it could grow on DMA and rine environment. Ruegeria pomeroyi DSS-3, isolated off the coast MMA (Table S1). To confirm whether tdm is essential in R. of Oregon in the United States (35), is the best characterized pomeroyi, tdm was cloned along with its promoter from R. model marine organism in this clade (32, 36–39). pomeroyi into the broad-host-range plasmid pBBR1MCS-km Δ Here, we identify a TMAO-specific microbial ABC trans- (40), which was then mobilized into the tdm::Gm mutant via porter and the TMAO demethylase, Tdm (TMAO → DMA + conjugation. Complementation of the mutant with the native tdm formaldehyde), from key marine heterotrophs, including bacteria gene from R. pomeroyi reversed the phenotype, restoring growth from the SAR11 clade and the MRC. This transporter and Tdm on both TMAO and TMA as a sole N source (Fig. 1D). Com- are highly expressed in the marine environment, as indicated by plementation of this mutant with the vector pBBR1MCS-km a number of recent metatranscriptomic and metaproteomic alone did not result in growth on TMA and TMAO (Fig. 1C). studies. Therefore, our data suggest that TMAO is an important, yet overlooked, nutrient for marine bacteria. Distribution of Tdm Homologs in Other Marine Bacteria. To test the importance of the tdm gene and to investigate its occurrence in the Results marine environment, we further investigated the distribution of R. pomeroyi Tdm in the genomes of isolated marine bacteria. The Tdm from Identification and Confirmation of a Functional Tdm in . R. pomeroyi was used as the query sequence to generate a BLASTP We used R. pomeroyi DSS-3 as the model organism to study TMAO database using the Integrated Microbial Genomes system at the metabolism.Thisbacteriumcangrowonmethylatedamines,in- Joint Genome Institute. Closely related homologs (E value = 0.0) cluding TMAO, as a sole N source (Fig. 1A). In the genome se- of Tdm were retrieved from representatives of the SAR11 clade quence of R.
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