Trimethylamine and trimethylamine N-oxide are supplementary energy sources for a marine heterotrophic bacterium: implications for marine carbon and nitrogen cycling

Abstract

Bacteria of the marine Roseobacter clade are characterised by their ability to utilise a wide range of organic and inorganic compounds to support growth. Trimethylamine (TMA) and trimethylamine N-oxide (TMAO) are methylated amines (MA) and form part of the dissolved organic nitrogen pool, the second largest source of nitrogen after N 2 gas, in the oceans. We investigated if the marine heterotrophic bacterium, Ruegeria pomeroyi DSS-3, could utilise TMA and TMAO as a supplementary energy source and whether this trait had any beneficial effect on growth. In R. pomeroyi, catabolism of TMA and TMAO resulted in the production of intracellular ATP which in turn helped to enhance growth rate and growth yield as well as enhancing cell survival during prolonged energy starvation. Furthermore, the simultaneous use of two different exogenous energy sources led to a greater enhancement of chemoorganoheterotrophic growth. The use of TMA and TMAO primarily as an energy source resulted in the remineralisation of nitrogen in the form of ammonium, which could cross feed into another bacterium. This study provides greater insight into the microbial metabolism of MAs in the marine environment and how it may affect both nutrient flow within marine surface waters and the flux of these climatically important compounds into the atmosphere.

Ecological Genomics of the Uncultivated Marine Roseobacter Lineage CHAB-I-5

“…This differential presence of potential CO oxidizers was similarly observed in the cultured pelagic roseobacters (Table 4). In contrast, a nearly complete gene cluster for the oxidation of sulfide or thiosulfate (soxRSVWXYZABCDEGH), a more productive process for energy generation (62), is present in all uncultivated lineages, in contrast to its occurrence in only one-half of the six cultured pelagic strains (Table 4). Carbon and nutrient metabolism.…”

“…In contrast, only one of the six analyzed genomes of the less abundant pelagic Roseobacter lineages encodes these genetic potentials. Genes encoding other energy-producing processes, such as the oxidation of "energy-rich" reduced-sulfur compounds and trimethylamine (62), are similarly more common in the four mostly uncultured lineages. Moreover, these uncultivated lineages are more versatile in the uptake and catabolism of various carbohydrate compounds, methylated osmolytes, and key currencies underlying the trophic interactions between bacteria and phytoplankton.…”

“…But this is not the case for the utilization of many methylated compounds. For instance, the complete genetic pathway (tmm, tmoXVW, tdm, gmaS, mgsABC) for the uptake and catabolism of MAs (62,64) is consistently present in operon structures in the four uncultivated lineages but missing in a majority of the cultured strains ( Table 4). The MAs are often utilized as C and energy source by roseobacters (e.g., Roseovarius sp.…”

Quantification of glycine betaine, choline and trimethylamine N-oxide in seawater particulates: Minimisation of seawater associated ion suppression

“…The capacity for choline catabolism is widespread in marine heterotrophs of the marine Roseobacter clade (MRC [11]), and model organisms of the MRC can grow on choline and GBT as a sole carbon source [11] resulting in remineralisation of osmolyte nitrogen to ammonia. Similarly, MRC have been shown to use TMAO as an energy source which also resulted in ammonia production [12], and the capacity for TMAO binding in MRC is thought to be widespread [13]. Members of the Pelagibacterales bacteria (SAR11 clade) also have the capacity to degrade TMAO [14].…”

Mechanistic Insight into Trimethylamine N -Oxide Recognition by the Marine Bacterium Ruegeria pomeroyi DSS-3

“…TMAO serves as an important nutrient for ecologically important marine heterotrophic bacteria, particularly those in the marine Roseobacter clade (MRC) (32), which is abundant in marine environments and is an important participant in marine C, S, and N cycles (33,34). Because some ecologically relevant representatives of the MRC are amenable to genetic manipulation, they have become model organisms to investigate bacterial ecophysiology in the marine environment (6).…”