Methanomethylovorans are the dominant dimethylsulfide-degrading methanogens in gravel and sandy river sediment microcosms

Abstract

Background: Rivers and streams are important components of the global carbon cycle and methane budget. However, our understanding of the microbial diversity and the metabolic pathways underpinning methylotrophic methane production in river sediments is limited. Dimethylsulfide is an important methylated compound, found in freshwater sediments. Yet, the magnitude of DMS-dependent methanogenesis nor the methanogens carrying out this process in river sediments have been explored before. This study addressed this knowledge gap in DMS-dependent methanogenesis in gravel and sandy river sediments.

Results: Significant methane production via DMS degradation was found in all sediment microcosms. Sandy, less permeable river sediments had higher methane yields (83 and 92%) than gravel, permeable sediments (40 and 48%). There was no significant difference between the methanogen diversity in DMS-amended gravel and sandy sediment microcosms, which Methanomethylovorans dominated. Metagenomics data analysis also showed the dominance of Methanomethylovorans and Methanosarcina. DMS-specific methyltransferase genes (mts) were found in very low relative abundances whilst the methanol-, trimethylamine- and dimethylamine-specific methyltransferase genes (mtaA, mttB and mtbB) had the highest relative abundances, suggesting their involvement in DMS-dependent methanogenesis.

Conclusions: This is the first study demonstrating a significant potential for DMS-dependent methanogenesis in river sediments with contrasting geologies. Methanomethylovorans were the dominant methylotrophic methanogen in all river sediment microcosms. Methyltransferases specific to methylotrophic substrates other than DMS are likely key enzymes in DMS-dependent methanogenesis, highlighting their versatility and importance in the methane cycle in freshwater sediments, which would warrant further study.

Keywords: Dimethylsulfide; Metagenomics; Methylotrophic methanogenesis; River sediments.

Fig. 1

The UK map and the location of the rivers sampled for this study. Colour indicates sediment grainsize. Light grey: Gravel, black: Sandy. The coordinates for the rivers are: River Pant—52.0044, 0.316916; River Rib—51.83917, − 0.02936; River Medway—51.26798, 0.518439; River Nadder—51.04385, − 2.11182

Fig. 2

A Average DMS and methane concentrations in river sediment microcosms using DMS as the only energy and carbon source. Rivers Pant and Rib have gravel-dominated riverbeds, whereas Rivers Medway and Nadder have sand-dominated riverbeds. Error bars were omitted to make the graph legible. Black line: DMS concentrations, red line: Methane concentrations. B Total concentrations of DMS degraded, and methane and CO₂ produced at the end of the incubation period. Error bars represent standard error above and below the average of five replicates

Fig. 3

A Average relative abundance of the methanogens at the genus level in five original river sediment samples and five replicated DMS microcosms per site as determined via the amplification of the mcrA gene. B Principal Coordinate Analysis (PCoA) plots of the mcrA sequences based on Bray–Curtis dissimilarity metrics. Ellipses indicate 95% confidence intervals according to treatment data. Colours indicate treatment. Shapes indicate sampling sites. C Mean copy number of the mcrA gene per gram of sediment. Ori: Original sediment samples. Con: Sediment samples from the control microcosms. DMS: Sediment samples from the DMS-amended microcosms. Error bars represent standard error above and below the average of five replicates

Fig. 4

A Heatmap showing the abundance of genes involved in methylotrophic methanogenesis in River Pant sediment microcosm with DMS. CPM: Copies per million reads. MMA: Monomethylamine, DMA: Dimethylamine, TMA: Trimethylamine, DMS: Dimethylsulfide, MT: Methanethiol, Me: Methanol B Bubble graph showing the abundance of the methanogens affiliated with methylotrophic methanogenesis-related genes in River Pant sediment microcosm with DMS. Other: Genera with a gene copy number < 50