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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

Relative sequence abundances of archaeal and bacterial 16S rRNA genes at emission spot 1a (ES1a) and 3 (ES3). The number of analyzed clones is given above the columns. The nomenclature of uncultivated groups is according to SILVA taxonomy.
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Figure 3: Relative sequence abundances of archaeal and bacterial 16S rRNA genes at emission spot 1a (ES1a) and 3 (ES3). The number of analyzed clones is given above the columns. The nomenclature of uncultivated groups is according to SILVA taxonomy.

Mentions: The sediment horizons of ES1a (30–40 cm) and ES3 (10–20 cm) that showed the highest AOM activity were used for the construction of archaeal and bacterial 16S rRNA gene libraries. Despite the proximity and the observed geochemical similarity of the seep sites we found striking differences in their microbial richness and community composition (Figure 3). The libraries of ES1a were dominated by ANME-1 and SEEP-SRB2, and showed a high diversity of ANME clades, including ANME-2ab, ANME-2c, ANME-1a, and ANME-1b. The libraries of ES3 were dominated by ANME-2ab and SEEP-SRB1 and we did not detect any other ANME clades. In addition, only ES1a harbored sulfate reducers of the clade Sva0081, whereas only at ES3 we found Desulfarculales. The ANME and SRB at both seep sites were closely related to those found at other seeps worldwide (Figures 4 and 5). Pyrosequencing was performed with DNA from subsurface sediments of ES1a (30–40 cm), ES1b (20–30 cm), and ES3 (10–20 cm) to complement and extend the findings obtained by the gene libraries. As references we used subsurface sediments from three sites that showed no indication for methane seepage (Ref1–3). The numbers of observed archaeal and bacterial OTU0.02 (S) as well as estimated richness (Chao1) were similar at all emission and reference spots (Table 1), except for Ref2 that had a much lower S and Chao1. The highest archaeal and bacterial Inverse Simpson diversity (D) was found at ES1b, whereas ES3 showed an exceptionally low bacterial D compared to all other sediments. Despite their close proximity the emission spots harbored very distinct archaeal and bacterial communities and shared few OTU0.02. In general the turnover of OTU0.02 was lower within emission spots and within reference spots than between emission spots and reference spots (Supplementary Table S4), showing that emission spots were more similar to each other than the surrounding sediment. Eighty-three percent of all archaeal and 81% of all bacterial OTU0.02 occurred only at one location and we did not find one archaeal OTU0.02 that occurred in all six samples (Supplementary Figure S2). This high amount of uniqueness was found at emission spots and reference sites. The archaeal community at ES1a seemed to be dominated by ANME-2a, but also comprised ANME-2b, ANME-2c, ANME-1a, and ANME-1b (Figure 6). The bacterial community of the ES1a sample was dominated by SEEP-SRB2, but also contained SEEP-SRB1 and many Anaerolineales. ES1b was very similar to ES1a in its microbial composition. In contrast, the sample of ES3 was clearly dominated by ANME-2a, had sequences affiliated to ANME-3, but lacked ANME-2c and ANME-1. Here, the bacterial community was dominated by SEEP-SRB1.


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)

Relative sequence abundances of archaeal and bacterial 16S rRNA genes at emission spot 1a (ES1a) and 3 (ES3). The number of analyzed clones is given above the columns. The nomenclature of uncultivated groups is according to SILVA taxonomy.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 3: Relative sequence abundances of archaeal and bacterial 16S rRNA genes at emission spot 1a (ES1a) and 3 (ES3). The number of analyzed clones is given above the columns. The nomenclature of uncultivated groups is according to SILVA taxonomy.
Mentions: The sediment horizons of ES1a (30–40 cm) and ES3 (10–20 cm) that showed the highest AOM activity were used for the construction of archaeal and bacterial 16S rRNA gene libraries. Despite the proximity and the observed geochemical similarity of the seep sites we found striking differences in their microbial richness and community composition (Figure 3). The libraries of ES1a were dominated by ANME-1 and SEEP-SRB2, and showed a high diversity of ANME clades, including ANME-2ab, ANME-2c, ANME-1a, and ANME-1b. The libraries of ES3 were dominated by ANME-2ab and SEEP-SRB1 and we did not detect any other ANME clades. In addition, only ES1a harbored sulfate reducers of the clade Sva0081, whereas only at ES3 we found Desulfarculales. The ANME and SRB at both seep sites were closely related to those found at other seeps worldwide (Figures 4 and 5). Pyrosequencing was performed with DNA from subsurface sediments of ES1a (30–40 cm), ES1b (20–30 cm), and ES3 (10–20 cm) to complement and extend the findings obtained by the gene libraries. As references we used subsurface sediments from three sites that showed no indication for methane seepage (Ref1–3). The numbers of observed archaeal and bacterial OTU0.02 (S) as well as estimated richness (Chao1) were similar at all emission and reference spots (Table 1), except for Ref2 that had a much lower S and Chao1. The highest archaeal and bacterial Inverse Simpson diversity (D) was found at ES1b, whereas ES3 showed an exceptionally low bacterial D compared to all other sediments. Despite their close proximity the emission spots harbored very distinct archaeal and bacterial communities and shared few OTU0.02. In general the turnover of OTU0.02 was lower within emission spots and within reference spots than between emission spots and reference spots (Supplementary Table S4), showing that emission spots were more similar to each other than the surrounding sediment. Eighty-three percent of all archaeal and 81% of all bacterial OTU0.02 occurred only at one location and we did not find one archaeal OTU0.02 that occurred in all six samples (Supplementary Figure S2). This high amount of uniqueness was found at emission spots and reference sites. The archaeal community at ES1a seemed to be dominated by ANME-2a, but also comprised ANME-2b, ANME-2c, ANME-1a, and ANME-1b (Figure 6). The bacterial community of the ES1a sample was dominated by SEEP-SRB2, but also contained SEEP-SRB1 and many Anaerolineales. ES1b was very similar to ES1a in its microbial composition. In contrast, the sample of ES3 was clearly dominated by ANME-2a, had sequences affiliated to ANME-3, but lacked ANME-2c and ANME-1. Here, the bacterial community was dominated by SEEP-SRB1.

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