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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–G) and confocal laser scanning micrographs (A1–A4) of ANME and SRB associations visualized by CARD–FISH. The woven-type consortia (A,A1–A4,B) consisted of ANME-1 or -2 (red, pooled probe: ANME-1/ANME-2) and SRB (green, probe: DSS658). Mixed-type (C), shell-type (D), and bubble-type (E) aggregates of ANME-2 (red, probe: ANME2-647) and SEEP-SRB1a (green, probe: SEEP1a-1441). Filamentous chain-type aggregate (F) of ANME-1 (red, probe: ANME1–350) and ANME-2 (yellow, probe: ANME2–538). Monospecific aggregate (G) of ANME-2 (red, probe: ANME2–538. Nucleic acids were stained with DAPI (blue). The scale bars are 2 μm.
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Figure 8: Epifluorescence (A–G) and confocal laser scanning micrographs (A1–A4) of ANME and SRB associations visualized by CARD–FISH. The woven-type consortia (A,A1–A4,B) consisted of ANME-1 or -2 (red, pooled probe: ANME-1/ANME-2) and SRB (green, probe: DSS658). Mixed-type (C), shell-type (D), and bubble-type (E) aggregates of ANME-2 (red, probe: ANME2-647) and SEEP-SRB1a (green, probe: SEEP1a-1441). Filamentous chain-type aggregate (F) of ANME-1 (red, probe: ANME1–350) and ANME-2 (yellow, probe: ANME2–538). Monospecific aggregate (G) of ANME-2 (red, probe: ANME2–538. Nucleic acids were stained with DAPI (blue). The scale bars are 2 μm.

Mentions: The relative cell abundance of ANME-1, ANME-2, SEEP-SRB1a, and SEEP-SRB2 as determined by CARD–FISH varied substantially between seep sites and sediment layers. At all seeps the layer with the highest total cell abundance coincided with the highest relative abundance of anaerobic methanotrophs and sulfate reducers. These layers were between 10 and 40 cmbsf (cm below sea floor) and were highly dominated by ANME and SEEP-SRB (Figure 7). The CARD–FISH results confirmed that ES1a and ES1b were dominated by ANME-1 (∼20% of total cells; up to ∼9.5 × 107 cells ml-1 sediment) and SEEP-SRB2 (∼25% of total cells). ES4 was dominated by ANME-2 (∼20% of total cells, up to ∼5 × 107 cells ml-1 sediment) and SEEP-SRB1a (∼15% of total cells). ES4 had a similar community as ES3. At ES3 and ES4 we did not detect ANME-1 cells, indicating that this clade was entirely absent, as confirmed by both 16S rRNA gene libraries and pyrosequencing. Most of the ANME and SEEP-SRB formed conspicuous AOM consortia (Figure 8). Although we found all combinations, generally, ANME-1 was associated to SEEP-SRB2 and ANME-2 was associated to SEEP-SRB1a (Figure 8).


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–G) and confocal laser scanning micrographs (A1–A4) of ANME and SRB associations visualized by CARD–FISH. The woven-type consortia (A,A1–A4,B) consisted of ANME-1 or -2 (red, pooled probe: ANME-1/ANME-2) and SRB (green, probe: DSS658). Mixed-type (C), shell-type (D), and bubble-type (E) aggregates of ANME-2 (red, probe: ANME2-647) and SEEP-SRB1a (green, probe: SEEP1a-1441). Filamentous chain-type aggregate (F) of ANME-1 (red, probe: ANME1–350) and ANME-2 (yellow, probe: ANME2–538). Monospecific aggregate (G) of ANME-2 (red, probe: ANME2–538. Nucleic acids were stained with DAPI (blue). The scale bars are 2 μm.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4814501&req=5

Figure 8: Epifluorescence (A–G) and confocal laser scanning micrographs (A1–A4) of ANME and SRB associations visualized by CARD–FISH. The woven-type consortia (A,A1–A4,B) consisted of ANME-1 or -2 (red, pooled probe: ANME-1/ANME-2) and SRB (green, probe: DSS658). Mixed-type (C), shell-type (D), and bubble-type (E) aggregates of ANME-2 (red, probe: ANME2-647) and SEEP-SRB1a (green, probe: SEEP1a-1441). Filamentous chain-type aggregate (F) of ANME-1 (red, probe: ANME1–350) and ANME-2 (yellow, probe: ANME2–538). Monospecific aggregate (G) of ANME-2 (red, probe: ANME2–538. Nucleic acids were stained with DAPI (blue). The scale bars are 2 μm.
Mentions: The relative cell abundance of ANME-1, ANME-2, SEEP-SRB1a, and SEEP-SRB2 as determined by CARD–FISH varied substantially between seep sites and sediment layers. At all seeps the layer with the highest total cell abundance coincided with the highest relative abundance of anaerobic methanotrophs and sulfate reducers. These layers were between 10 and 40 cmbsf (cm below sea floor) and were highly dominated by ANME and SEEP-SRB (Figure 7). The CARD–FISH results confirmed that ES1a and ES1b were dominated by ANME-1 (∼20% of total cells; up to ∼9.5 × 107 cells ml-1 sediment) and SEEP-SRB2 (∼25% of total cells). ES4 was dominated by ANME-2 (∼20% of total cells, up to ∼5 × 107 cells ml-1 sediment) and SEEP-SRB1a (∼15% of total cells). ES4 had a similar community as ES3. At ES3 and ES4 we did not detect ANME-1 cells, indicating that this clade was entirely absent, as confirmed by both 16S rRNA gene libraries and pyrosequencing. Most of the ANME and SEEP-SRB formed conspicuous AOM consortia (Figure 8). Although we found all combinations, generally, ANME-1 was associated to SEEP-SRB2 and ANME-2 was associated to SEEP-SRB1a (Figure 8).

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