Biogeographic traits of dimethyl sulfide and dimethylsulfoniopropionate cycling in polar oceans

Abstract

Background: Dimethyl sulfide (DMS) is the dominant volatile organic sulfur in global oceans. The predominant source of oceanic DMS is the cleavage of dimethylsulfoniopropionate (DMSP), which can be produced by marine bacteria and phytoplankton. Polar oceans, which represent about one fifth of Earth's surface, contribute significantly to the global oceanic DMS sea-air flux. However, a global overview of DMS and DMSP cycling in polar oceans is still lacking and the key genes and the microbial assemblages involved in DMSP/DMS transformation remain to be fully unveiled.

Results: Here, we systematically investigated the biogeographic traits of 16 key microbial enzymes involved in DMS/DMSP cycling in 60 metagenomic samples from polar waters, together with 174 metagenome and 151 metatranscriptomes from non-polar Tara Ocean dataset. Our analyses suggest that intense DMS/DMSP cycling occurs in the polar oceans. DMSP demethylase (DmdA), DMSP lyases (DddD, DddP, and DddK), and trimethylamine monooxygenase (Tmm, which oxidizes DMS to dimethylsulfoxide) were the most prevalent bacterial genes involved in global DMS/DMSP cycling. Alphaproteobacteria (Pelagibacterales) and Gammaproteobacteria appear to play prominent roles in DMS/DMSP cycling in polar oceans. The phenomenon that multiple DMS/DMSP cycling genes co-occurred in the same bacterial genome was also observed in metagenome assembled genomes (MAGs) from polar oceans. The microbial assemblages from the polar oceans were significantly correlated with water depth rather than geographic distance, suggesting the differences of habitats between surface and deep waters rather than dispersal limitation are the key factors shaping microbial assemblages involved in DMS/DMSP cycling in polar oceans.

Conclusions: Overall, this study provides a global overview of the biogeographic traits of known bacterial genes involved in DMS/DMSP cycling from the Arctic and Antarctic oceans, laying a solid foundation for further studies of DMS/DMSP cycling in polar ocean microbiome at the enzymatic, metabolic, and processual levels. Video Abstract.

Keywords: DMS/DMSP cycling; Geographic distribution; Phylogenetic diversity; Polar oceans.

Fig. 1

The conceptual sketch of known key proteins and pathways involved in microbial DMS/DMSP cycling. The different catabolic pathways are marked in different colours and distinguished using numbers 1–7. The dotted arrow indicated that a series of enzymatic reactions are required to form the end product

Fig. 2

Geographic distribution of the sampling locations of the metagenomic (blue symbols) and metatranscriptomic (purple symbols) samples from polar (indicated by stars) and non-polar (indicated by dots) ocean

Fig. 3

Relative abundance of potential genes involved in bacterial DMS/DMSP cycling. a The relative abundances of DMS/DMSP cycling-related genes in 60 polar metagenomes (left panel) and 52 polar metatranscriptomes (right panel). b The relative abundances of DMS/DMSP cycling-related genes in 174 non-polar Tara Ocean samples (left panel) and 99 non-polar metatranscriptomes (right panel). Polar metagenomes were separated into Arctic-Surface (0–100 m), Arctic-Deep (300–3800 m), Antarctic-Surface (0 m), and Antarctic-Deep (300–3500 m). Polar metatranscriptomic samples were separated into two groups: Polar-surface (0–146 m) and Polar-deep (200–1000 m) groups. Tara metagenomes and metatranscriptomes were separated into Tara-Surface (5–188 m) and Tara-Deep (250–1000 m), and Non-polar surface (0–150 m) and Non-polar deep (200–3262 m), respectively. The relative abundance of each gene was normalized against the average abundance of the 10 selected bacterial marker genes. MetaG, metagenomes; MetaT, metatranscriptomes

Fig. 4

Analyses of inter-sample similarity among the polar and non-polar seawater samples. a Average relative abundance of DMS/DMSP-related genes in different metagenomic sample groups. Bray-Curtis dissimilarities of all (b), polar (c), and Tara (d) metagenomic samples illustrated by PCoA analysis based on the relative abundances of DMS/DMSP-related genes. The total abundance of each metagenomic sample was normalized to 1. The percentages of variation explained by the principal coordinates are indicated on the axes. RDA analyses of sampling sites and protein types of polar samples (e) and Tara samples (f). The ordination plot was constructed using the relative abundance of DMS/DMSP-related proteins. Proteins involved in DMS/DMSP cycling are indicated by black arrows. The percentages of variation are shown on the axes

Fig. 5

Phylogenetic diversity of DMS/DMSP cycling-related genes in the Arctic and Antarctic oceans. The taxonomic compositions of microbiota involved in DMS/DMSP cycling are displayed at the class level for sample groups (a) and proteins (b). c Taxonomic profiling of DMS/DMSP cycling-related microbiota in Alphaproteobacteria (Alpha) and Gammaproteobacteria (Gamma) classes. Pro, Proteobacteria; Act, Actinobacteria; Chl, Chloroflexi. d Alpha-diversity analyses of the polar microbiomes involved in DMS/DMSP cycling. Shannon and Simpson diversity was calculated based on the taxonomic composition of DMS/DMSP-related genes, with higher values representing higher biodiversity. e Bray-Curtis dissimilarities of polar metagenomic samples illustrated by PCoA analysis based on the taxonomic compositions of DMS/DMSP-related genes. The DMS/DMSP-related community composition of each metagenomic sample was normalized to 1. f Correlation between dissimilarity of DMS/DMSP-related bacterial community and water depth in polar oceans. The Bray-Curtis dissimilarity index was used. The correlation coefficients (r) and Spearman’s correlation P value (P) were indicated

Fig. 6

The gene frequency and taxonomic composition of polar metagenome assembled genomes (MAGs) involved in DMS/DMSP cycling in polar oceans. a Frequency of DMS/DMSP cycling-related genes in 143 (out of 214) polar MAGs. MAGs are separated into four groups with MAGs in groups 1 to 3 carrying 1 to 3 types of DMS/DMSP cycling-related genes, MAGs in group 4 contains more than 3 types of DMS/DMSP cycling-related genes. The co-occurrence networks of protein-protein (b, d) and pathway-pathway (c, e) coexistence modes in DMS/DMSP cycling in MAGs obtained from polar oceans (b, c) compared to all microbial genomes in the IMG/M database (d, e). The cluster of each network was shown in its lower left corner. Each node in the networks indicates one protein (b, d) or one pathway (c, e) involved in DMS/DMSP cycling. The proteins in the same catabolic pathway (as indicated in Table 1) are marked using the same colour, and different pathways are distinguished using numbers 1–7. The size of nodes and the thickness of edges represent the frequencies of genes and MAGs carrying multiple genes involved in DMS/DMSP cycling, respectively.

Fig. 7

The conceptual diagram of bacterial DMS/DMSP metabolism in polar and non-polar oceans based on the analysis of the relative abundance of the potential genes involved in DMS/DMSP cycles. The thickness of the edge represents the relative abundance of the potential genes in each pathway. The arrowheads indicate the flow directions of organic sulfur compounds. Potential genes contributing more than 20% of the total relative abundance in each pathway are shown