Global dispersion and local diversification of the methane seep microbiome

Abstract

Methane seeps are widespread seafloor ecosystems shaped by the emission of gas from seabed reservoirs. The microorganisms inhabiting methane seeps transform the chemical energy in methane to products that sustain rich benthic communities around the gas leaks. Despite the biogeochemical relevance of microbial methane removal at seeps, the global diversity and dispersion of seep microbiota remain unknown. Here we determined the microbial diversity and community structure of 23 globally distributed methane seeps and compared these to the microbial communities of 54 other seafloor ecosystems, including sulfate-methane transition zones, hydrothermal vents, coastal sediments, and deep-sea surface and subsurface sediments. We found that methane seep communities show moderate levels of microbial richness compared with other seafloor ecosystems and harbor distinct bacterial and archaeal taxa with cosmopolitan distribution and key biogeochemical functions. The high relative sequence abundance of ANME (anaerobic methanotrophic archaea), as well as aerobic Methylococcales, sulfate-reducing Desulfobacterales, and sulfide-oxidizing Thiotrichales, matches the most favorable microbial metabolisms at methane seeps in terms of substrate supply and distinguishes the seep microbiome from other seafloor microbiomes. The key functional taxa varied in relative sequence abundance between different seeps due to the environmental factors, sediment depth and seafloor temperature. The degree of endemism of the methane seep microbiome suggests a high local diversification in these heterogeneous but long-lived ecosystems. Our results indicate that the seep microbiome is structured according to metacommunity processes and that few cosmopolitan microbial taxa mediate the bulk of methane oxidation, with global relevance to methane emission in the ocean.

Keywords: ANME; anaerobic methane oxidation; deep-sea seafloor ecosystems; environmental selection; microbial community ecology.

Fig. 1.

Map of seafloor ecosystems. Datasets with spatially distributed sites are numbered (e.g., NZS1-10). Abbreviations of methane seeps (orange) and subsurface sulfate methane transition zones (SMTZ; purple) stand for ANT, Low-activity Antarctic seep; BS, Black Sea microbial reef; DS, Gulf of Cadiz mud volcanoes; GB, Guaymas Basin hot seeps; GoM, Gulf of Mexico seeps; HMMV, Håkon Mosby mud volcano; HR, Hydrate Ridge seeps; JAP, Japanese Trench seep; KO, Congo Basin (REGAB) seep; NS, North Sea seep; NZ, New Zealand seeps; QS, Quepos Slide seep (Costa Rica); and ST, Storegga Slide seep (Norway). Other abbreviations are as follows. Deep-sea surface sediments (brown): SMS, Station M; NZS, New Zealand. Coastal sediments (green): AGW, Amazon–Guiana Waters; CR, Hawaiian Coral Reef; LCR, Latin American Coastal Regions; MM, North Sea Intertidal Microbial Mat; VAG, Chilean Coast sediment. Subsurface sediments (blue): DS4/ODP, Peru Margin Ocean Drilling Core. Hydrothermal Vents (red): ASV, Azores Shallow Vents; LC, Lost City Vent Field; LV, Lau Vent Field.

Fig. 2.

Richness estimates and NMDS ordinations based on archaeal and bacterial OTU_0.03. (A) The symbols represent the mean of 100 Chao1 richness calculations for each of the 77 investigated sampling sites, with each calculation based on rarefaction of 3,000 randomly chosen sequences without replacement. No archaeal data were available for deep-sea surface sediments. (B and C) Similarity of archaeal (B, 48 samples) and bacterial (C, 77 samples) communities visualized by nonmetric multidimensional scaling (NMDS). Each sample (dot) is connected to the weighted averaged mean of the within group distances. Ellipses represent one SD of the weighted averaged mean. All groups were significantly different as tested with a subsampling-based Redundancy Analysis approach (see also SI Appendix). The color code is identical to A.

Fig. 3.

Relative sequence abundance of archaeal and bacterial classes. The graph shows the relative sequence abundance of the most abundant archaeal (A) and bacterial (B) classes in different seafloor ecosystems sorted according to average relative abundance across all samples. Sampling sites and ecosystems are ordered from high (Left) to low (Right) Chao1 richness. The archaeal class Methanomicrobia is shown in the lower panel of A, with subdivisions for the major methanotrophic (ANME) as well as methanogenic (Methanosarcinales; other Methanomicrobia) clades.

Fig. 4.

Network graph of 23 methane seeps based on occurrence of ANME OTU_0.03. The colored nodes (circles) represent all 1,765 ANME OTU_0.03 that were found in this study. The colors indicate the taxonomic assignment of each ANME OTU_0.03. Nodes marked as circles with black crosses represent the 23 investigated methane seeps to which the gray lines connect their respective ANME OTU_0.03. The distance between methane seep nodes reflects their OTU_0.03 connectivity;_, e.g., methane seeps that share many ANME OTU_0.03 are plotted close to each other, whereas those that share less are more distant. ANME OTU_0.03 that occurred at many seeps are shown as larger nodes found in the middle of the plot, whereas OTU_0.03 that occurred only at one seep are small nodes on the periphery. There are 10 nodes with numbers from 1 to 10, which represent the 10 most sequence-abundant ANME OTU_0.03. These 10 OTU_0.03 were responsible for around 85% of all sequenced ANME reads and had a cosmopolitan distribution. The majority of the ANME diversity, however, was rare and locally restricted.