Metagenomic data-mining reveals contrasting microbial populations responsible for trimethylamine formation in human gut and marine ecosystems

Abstract

Existing metagenome datasets from many different environments contain untapped potential for understanding metabolic pathways and their biological impact. Our interest lies in the formation of trimethylamine (TMA), a key metabolite in both human health and climate change. Here, we focus on bacterial degradation pathways for choline, carnitine, glycine betaine and trimethylamine N-oxide (TMAO) to TMA in human gut and marine metagenomes. We found the TMAO reductase pathway was the most prevalent pathway in both environments. Proteobacteria were found to contribute the majority of the TMAO reductase pathway sequences, except in the stressed gut, where Actinobacteria dominated. Interestingly, in the human gut metagenomes, a high proportion of the Proteobacteria hits were accounted for by the genera Klebsiella and Escherichia. Furthermore Klebsiella and Escherichia harboured three of the four potential TMA-production pathways (choline, carnitine and TMAO), suggesting they have a key role in TMA cycling in the human gut. In addition to the intensive TMAO–TMA cycling in the marine environment, our data suggest that carnitine-to-TMA transformation plays an overlooked role in aerobic marine surface waters, whereas choline-to-TMA transformation is important in anaerobic marine sediments. Our study provides new insights into the potential key microbes and metabolic pathways for TMA formation in two contrasting environments.

Microbial trimethylamine metabolism in marine environments

“…The cutC gene is more prevalent in anaerobic marine sediments. Among these functional genes, the torA gene is the most abundant in both open ocean and marine sediment datasets, which implies that TMA formation from the TMAO reduction pathway is prevalent and important in the oceans (Jameson et al ., ).…”

“…The cutC gene is more prevalent in anaerobic marine sediments. Among these functional genes, the torA gene is the most abundant in both open ocean and marine sediment datasets, which implies that TMA formation from the TMAO reduction pathway is prevalent and important in the oceans (Jameson et al, 2016). TMA production can also occur under aerobic conditions through oxidation of carnitine (Unemoto et al, 1966;Rebouche and Seim, 1998;Zhu et al, 2014), which may explain the presence of TMA in oxygenated marine surface waters (Carpenter et al, 2012).…”

Aliphatic amines at the Cape Verde Atmospheric Observatory: Abundance, origins and sea-air fluxes

“…Cree (2014) found that 7 of 10 primary pigments also correlated positively with GBT, including fucoxanthin, while a close relationship of both GBT and chl-a with phytoplankton carbon was observed. Although bacteria may be the primary source of methylamines in the water column (Lidbury et al, 2014;Lidbury et al, 2015a;2015b;Jameson et al, 2016), their short residence time (Cree et al, 2018) indicates that both phytoplankton and bacteria play a role in methylamine abundance and dynamics.…”

“…The degradation of TMAO has also been demonstrated in members of the Pelagibacterales bacteria (SAR11 clade) (Lidbury et al, 2014). In addition, marine metagenomics data-mining has identified the presence of genes encoding the production of trimethylamine from nitrogen osmolytes in the open ocean (Jameson et al, 2016). The methylated amines, mono-di-and trimethylamine (MMA, DMA and TMA, respectively), can provide a source of carbon and nitrogen for marine microorganisms (Taubert et al, 2017).…”

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

“…Marine or estuarine methanogens can also grow on nitrogenous osmolytes [15e17] indicating a link between quaternary amines and biological methane production in marine environments. Furthermore, marine metagenomic data-mining indicates the presence of genes encoding the production of trimethylamine from quaternary amines in the open ocean [18], providing a possible route and marine biogenic source of atmospheric amines [19], recently discovered to be important for new particle formation [20,21]. Despite their potential importance in the marine nitrogen cycle, particularly as a substrate for bacteria, and as potential precursors of climate-active compounds, little is known about the standing concentrations of GBT, choline and TMAO in seawater.…”