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Methane Seep in Shallow-Water Permeable Sediment Harbors High Diversity of Anaerobic Methanotrophic Communities, Elba, Italy.

Ruff SE, Kuhfuss H, Wegener G, Lott C, Ramette A, Wiedling J, Knittel K, Weber M - Front Microbiol (2016)

Bottom Line: Increased alkalinity, formation of free sulfide and nearly stoichiometric methane oxidation and sulfate reduction rates up to 200 nmol g(-1) day(-1) indicated the predominance of sulfate-coupled AOM.With up to 40 cm thickness the zones of AOM activity were unusually large and occurred in deeper sediment horizons (20-50 cm below seafloor) as compared to diffusion-dominated deep-sea seeps, which is likely caused by advective flow of pore water due to the shallow water depth and permeability of the sands.To link AOM phylotypes with seep habitats and to enable future meta-analyses we thus propose that seep environment ontology needs to be further specified.

View Article: PubMed Central - PubMed

Affiliation: Department for Molecular Ecology, Max Planck Institute for Marine MicrobiologyBremen, Germany; HGF MPG Group for Deep Sea Ecology and Technology, Max Planck Institute for Marine MicrobiologyBremen, Germany.

ABSTRACT
The anaerobic oxidation of methane (AOM) is a key biogeochemical process regulating methane emission from marine sediments into the hydrosphere. AOM is largely mediated by consortia of anaerobic methanotrophic archaea (ANME) and sulfate-reducing bacteria (SRB), and has mainly been investigated in deep-sea sediments. Here we studied methane seepage at four spots located at 12 m water depth in coastal, organic carbon depleted permeable sands off the Island of Elba (Italy). We combined biogeochemical measurements, sequencing-based community analyses and in situ hybridization to investigate the microbial communities of this environment. Increased alkalinity, formation of free sulfide and nearly stoichiometric methane oxidation and sulfate reduction rates up to 200 nmol g(-1) day(-1) indicated the predominance of sulfate-coupled AOM. With up to 40 cm thickness the zones of AOM activity were unusually large and occurred in deeper sediment horizons (20-50 cm below seafloor) as compared to diffusion-dominated deep-sea seeps, which is likely caused by advective flow of pore water due to the shallow water depth and permeability of the sands. Hydrodynamic forces also may be responsible for the substantial phylogenetic and unprecedented morphological diversity of AOM consortia inhabiting these sands, including the clades ANME-1a/b, ANME-2a/b/c, ANME-3, and their partner bacteria SEEP-SRB1a and SEEP-SRB2. High microbial dispersal, the availability of diverse energy sources and high habitat heterogeneity might explain that the emission spots shared few microbial taxa, despite their physical proximity. Although the biogeochemistry of this shallow methane seep was very different to that of deep-sea seeps, their key functional taxa were very closely related, which supports the global dispersal of key taxa and underlines strong selection by methane as the predominant energy source. Mesophilic, methane-fueled ecosystems in shallow-water permeable sediments may comprise distinct microbial habitats due to their unique biogeochemical and physical characteristics. To link AOM phylotypes with seep habitats and to enable future meta-analyses we thus propose that seep environment ontology needs to be further specified.

No MeSH data available.


Related in: MedlinePlus

Epifluorescence (A–J) and confocal laser scanning micrographs (B1–B4) of associations comprising ANME-1, ANME-2, and SRB visualized by CARD–FISH. (A–J) ANME-1 (red) and ANME-2 (yellow) cells. (B,E,G) ANME-1 (red), ANME-2 (yellow), and SEEP-SRB1a (green) cells. DAPI stain in blue. The scale bar is 2 μm.
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Figure 9: Epifluorescence (A–J) and confocal laser scanning micrographs (B1–B4) of associations comprising ANME-1, ANME-2, and SRB visualized by CARD–FISH. (A–J) ANME-1 (red) and ANME-2 (yellow) cells. (B,E,G) ANME-1 (red), ANME-2 (yellow), and SEEP-SRB1a (green) cells. DAPI stain in blue. The scale bar is 2 μm.

Mentions: In sediments of ES1 we found the highest morphological diversity. The analysis of 366 aggregates of ES1, ES3 and ES4 revealed that filamentous chain-type aggregates were the most relative abundant type of consortia (18%), followed by bubble- and mixed-type (each 12%) and by shell-type aggregates (11%), whereas woven-type aggregates were rare (1%) (Supplementary Figure S3). Monospecific aggregates of ANME or SRB accounted for 29% of all aggregations. In addition, at ES1a and ES1b we found many aggregates that contained cells of both ANME-1 and ANME-2 (Figures 8F and 9). These mixed ANME aggregates varied from loose associations to more tightly packed forms and were rather small being between 3 and 10 μm in diameter. The ANME-1 cells were mainly large and rod-shaped, while the ANME-2 cells were smaller and coccoid. ES3 and ES4 harbored microbial communities that were less phylogenetically and morphologically diverse. Here the community was dominated by shell-type aggregates and we did not detect any filament. At all emission spots we found monospecific aggregates of ANME or SEEP-SRB2. Monospecific ANME-2 aggregates (Figure 8G) had diameters from 6 μm to up to 90 μm and were frequently observed. ANME-1 monospecific aggregates were smaller (4–18 μm), less common and only occurred at ES1. Furthermore, we found ANME and SEEP-SRB single cells at all emission spots in low abundances. At the reference sites we did not detect any AOM consortia or monospecific ANME aggregates, but sporadically found single ANME or SEEP-SRB cells.


Methane Seep in Shallow-Water Permeable Sediment Harbors High Diversity of Anaerobic Methanotrophic Communities, Elba, Italy.

Ruff SE, Kuhfuss H, Wegener G, Lott C, Ramette A, Wiedling J, Knittel K, Weber M - Front Microbiol (2016)

Epifluorescence (A–J) and confocal laser scanning micrographs (B1–B4) of associations comprising ANME-1, ANME-2, and SRB visualized by CARD–FISH. (A–J) ANME-1 (red) and ANME-2 (yellow) cells. (B,E,G) ANME-1 (red), ANME-2 (yellow), and SEEP-SRB1a (green) cells. DAPI stain in blue. The scale bar is 2 μm.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4814501&req=5

Figure 9: Epifluorescence (A–J) and confocal laser scanning micrographs (B1–B4) of associations comprising ANME-1, ANME-2, and SRB visualized by CARD–FISH. (A–J) ANME-1 (red) and ANME-2 (yellow) cells. (B,E,G) ANME-1 (red), ANME-2 (yellow), and SEEP-SRB1a (green) cells. DAPI stain in blue. The scale bar is 2 μm.
Mentions: In sediments of ES1 we found the highest morphological diversity. The analysis of 366 aggregates of ES1, ES3 and ES4 revealed that filamentous chain-type aggregates were the most relative abundant type of consortia (18%), followed by bubble- and mixed-type (each 12%) and by shell-type aggregates (11%), whereas woven-type aggregates were rare (1%) (Supplementary Figure S3). Monospecific aggregates of ANME or SRB accounted for 29% of all aggregations. In addition, at ES1a and ES1b we found many aggregates that contained cells of both ANME-1 and ANME-2 (Figures 8F and 9). These mixed ANME aggregates varied from loose associations to more tightly packed forms and were rather small being between 3 and 10 μm in diameter. The ANME-1 cells were mainly large and rod-shaped, while the ANME-2 cells were smaller and coccoid. ES3 and ES4 harbored microbial communities that were less phylogenetically and morphologically diverse. Here the community was dominated by shell-type aggregates and we did not detect any filament. At all emission spots we found monospecific aggregates of ANME or SEEP-SRB2. Monospecific ANME-2 aggregates (Figure 8G) had diameters from 6 μm to up to 90 μm and were frequently observed. ANME-1 monospecific aggregates were smaller (4–18 μm), less common and only occurred at ES1. Furthermore, we found ANME and SEEP-SRB single cells at all emission spots in low abundances. At the reference sites we did not detect any AOM consortia or monospecific ANME aggregates, but sporadically found single ANME or SEEP-SRB cells.

Bottom Line: Increased alkalinity, formation of free sulfide and nearly stoichiometric methane oxidation and sulfate reduction rates up to 200 nmol g(-1) day(-1) indicated the predominance of sulfate-coupled AOM.With up to 40 cm thickness the zones of AOM activity were unusually large and occurred in deeper sediment horizons (20-50 cm below seafloor) as compared to diffusion-dominated deep-sea seeps, which is likely caused by advective flow of pore water due to the shallow water depth and permeability of the sands.To link AOM phylotypes with seep habitats and to enable future meta-analyses we thus propose that seep environment ontology needs to be further specified.

View Article: PubMed Central - PubMed

Affiliation: Department for Molecular Ecology, Max Planck Institute for Marine MicrobiologyBremen, Germany; HGF MPG Group for Deep Sea Ecology and Technology, Max Planck Institute for Marine MicrobiologyBremen, Germany.

ABSTRACT
The anaerobic oxidation of methane (AOM) is a key biogeochemical process regulating methane emission from marine sediments into the hydrosphere. AOM is largely mediated by consortia of anaerobic methanotrophic archaea (ANME) and sulfate-reducing bacteria (SRB), and has mainly been investigated in deep-sea sediments. Here we studied methane seepage at four spots located at 12 m water depth in coastal, organic carbon depleted permeable sands off the Island of Elba (Italy). We combined biogeochemical measurements, sequencing-based community analyses and in situ hybridization to investigate the microbial communities of this environment. Increased alkalinity, formation of free sulfide and nearly stoichiometric methane oxidation and sulfate reduction rates up to 200 nmol g(-1) day(-1) indicated the predominance of sulfate-coupled AOM. With up to 40 cm thickness the zones of AOM activity were unusually large and occurred in deeper sediment horizons (20-50 cm below seafloor) as compared to diffusion-dominated deep-sea seeps, which is likely caused by advective flow of pore water due to the shallow water depth and permeability of the sands. Hydrodynamic forces also may be responsible for the substantial phylogenetic and unprecedented morphological diversity of AOM consortia inhabiting these sands, including the clades ANME-1a/b, ANME-2a/b/c, ANME-3, and their partner bacteria SEEP-SRB1a and SEEP-SRB2. High microbial dispersal, the availability of diverse energy sources and high habitat heterogeneity might explain that the emission spots shared few microbial taxa, despite their physical proximity. Although the biogeochemistry of this shallow methane seep was very different to that of deep-sea seeps, their key functional taxa were very closely related, which supports the global dispersal of key taxa and underlines strong selection by methane as the predominant energy source. Mesophilic, methane-fueled ecosystems in shallow-water permeable sediments may comprise distinct microbial habitats due to their unique biogeochemical and physical characteristics. To link AOM phylotypes with seep habitats and to enable future meta-analyses we thus propose that seep environment ontology needs to be further specified.

No MeSH data available.


Related in: MedlinePlus