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Editor's Pick Research Article

Conductive Particles Enable Syntrophic Acetate Oxidation between Geobacter and Methanosarcina from Coastal Sediments

Amelia-Elena Rotaru, Federica Calabrese, Hryhoriy Stryhanyuk, Florin Musat, Pravin Malla Shrestha, Hannah Sophia Weber, Oona L. O. Snoeyenbos-West, Per O. J. Hall, Hans H. Richnow, Niculina Musat, Bo Thamdrup
Stephen J. Giovannoni, Editor
Amelia-Elena Rotaru
aDepartment of Biology, University of Southern Denmark, Odense, Denmark
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Federica Calabrese
bHelmholtz Centre for Environmental Research, Leipzig, Germany
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Hryhoriy Stryhanyuk
bHelmholtz Centre for Environmental Research, Leipzig, Germany
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Florin Musat
bHelmholtz Centre for Environmental Research, Leipzig, Germany
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Pravin Malla Shrestha
cEnergy Bioscience Institute, University of California Berkeley, Berkeley, USA
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Hannah Sophia Weber
aDepartment of Biology, University of Southern Denmark, Odense, Denmark
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Oona L. O. Snoeyenbos-West
aDepartment of Biology, University of Southern Denmark, Odense, Denmark
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Per O. J. Hall
dDepartment of Marine Sciences, University of Gothenburg, Gothenburg, Sweden
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Hans H. Richnow
bHelmholtz Centre for Environmental Research, Leipzig, Germany
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Niculina Musat
bHelmholtz Centre for Environmental Research, Leipzig, Germany
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Bo Thamdrup
aDepartment of Biology, University of Southern Denmark, Odense, Denmark
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Stephen J. Giovannoni
Oregon State University
Roles: Editor
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DOI: 10.1128/mBio.00226-18
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  • FIG 1 
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    FIG 1 

    CO2-reductive methanogenesis in the Bothnian Bay methanogenic zone. (a) The sampling site, RA2, was located off the Bothnian Bay northern coast. (b and c) Here, methane accumulated close to and sometimes over the saturation limit (b) and was strongly depleted in 13C (low δ13CH4), which indicated a high apparent fractionation (αC) characteristic of CO2-reductive methanogenesis (c). Previous studies showed an αC of ca. 1.05 (blue line) in Methanosarcina grown via CO2-reductive methanogenesis (85, 86). An αC of ca. 1.02 (orange line) was observed in Methanosarcina species grown by acetoclastic methanogenesis (87).

  • FIG 2 
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    FIG 2 

    Incubation mixtures with and without activated carbon and representative organisms. (a) Quantitative PCR in original sediment samples showed that Desulfuromonadales were the dominant electrogens in the original sediment and in sediment slurries with conductive particles, but this group was almost extinct in a first slurry transfer without conductive particles. The only methanogens detected by qPCR in the original sediments were DIET-associated Methanosarcina, which remained abundant in slurry incubation mixtures with or without conductive particles. (b) In mud-free incubation mixtures with conductive GAC (sixth consecutive mud-free transfer), acetate was completely depleted after 63 days, and it was converted to methane with a high stoichiometric recovery (82%). Methanosarcina was the only Archaea genus detected in these mud-free cultures. Together, Methanosarcina and Geobacter represented ca. half of the microbial community, as determined by CARD-FISH. (c) On the other hand, in control incubation mixtures without conductive materials (third consecutive mud-free transfer), acetate consumption was much slower. Acetate was depleted after 150 days and converted to methane, with only 40% stoichiometric recovery. In control incubation mixtures without conductive GAC, Geobacter and Methanosarcina were led to extinction (Fig. S5F). Instead Methanothrix-like filamentous Archaea carried acetate utilization in control incubation mixtures without GAC (Fig. S5F).

  • FIG 3 
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    FIG 3 

    Maximum likelihood trees of Bacteria and Archaea enriched in a seventh mud-free transfer with acetate and GAC. (a) A maximum likelihood tree of representative bacterial sequences from a mud-free transfer with conductive particles (GAC), under conditions strictly promoting methanogenic respiration. Acetate-oxidizing Desulfuromonadales dominated the 16S rRNA clone library, with more than half displaying close relationships to Geobacter psychrophilus (97% identity) and the rest to Desulfuromonas michiganensis (98%). The only methanogens enriched on acetate and GAC were relatives of Methanosarcina subterranea (99% identity), as shown in the maximum likelihood tree in panel b.

  • FIG 4 
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    FIG 4 

    Experimental approach and evidence for SAO. (a) Experimental approach to distinguish between SAO and acetoclastic methanogenesis based on isotopic labeling. 13CH312COOH was provided as 10% of the total acetate, which played the role of the electron donor for SAO consortia from the Bothnian Bay. During SAO, acetate-oxidizing Geobacter cells are expected to produce 13CO2 (13C, depicted in orange) and to incorporate [13C]acetate. During SAO, 13CO2 will be diluted by the bicarbonate in the medium and should not generate significant 13CH4. However, acetoclastic methanogenesis by Methanosarcina cells will generate 13CH4 from 13CH312COOH, while cells incorporate [13C]acetate in their cell mass. Cells expected to incorporate [13C]acetate are encircled in orange. (b) SAO activity was validated by using labeled 13CO2 production from acetate, especially in SAO consortia provided with GAC (blue) versus cultures without GAC (orange). (c) An overview of acetate catabolism and how much is used for respiration by Geobacter versus acetoclastic methanogenesis by Methanosarcina.

  • FIG 5 
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    FIG 5 

    nanoSIMS identification of cells incorporating 13C-labeled acetate. (a and b) Highly abundant Geobacter cells (a) incorporated more 13CH312COOH per cell than Methanosarcina (b). Insets for panels a and b show percent assimilation in Geobacter (blue insets) and Methanosarcina (orange) over time. (c) Time-dependent distribution of cells labeled by Geobacter-specific probes compared with time-dependent incorporation of 13CH3COOH in Geobacter cells (see scales below images) and an overlay of 13C incorporation (red) to total biomass as detected by tracing 32S (green), using nanoSIMS. (d) Time-dependent distribution of cells labeled by Methanosarcina-specific probes compared with time-dependent incorporation of 13CH3COOH in Methanosarcina-cells (see scales below images) and an overlay of 13C incorporation (red) to total biomass as detected by tracing 32S (green) using nanoSIMS.

  • FIG 6 
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    FIG 6 

    Syntrophic acetate-oxidizing bacteria cannot grow alone on acetate and GAC; they require the methanogen. If conductive GAC were sufficient for SAO bacteria to carry out acetate oxidation, the methanogenic inhibitor bromoethane sulfonate (BES) would collapse the rates of both methanogenesis (a) and acetate oxidation (b), indicating that the two processes are coupled and that Geobacter cannot grow alone on acetate and GAC. Methane production (a) and acetate utilization (b) rates were measured in cultures spiked with BES, in contrast to controls lacking BES and (c) a simplified representation of the BES inhibition effect on methanogenesis.

  • FIG 7 
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    FIG 7 

    Model interactions with different treatments of a Baltic methanogenic community. Geobacter (green) and Methanosarcina (red) consortia competitively displaced Methanothrix-like (green) cells in Baltic sediments rich in iron-oxide minerals and in conductive particle-amended incubation mixtures. Geobacter was only present in incubation mixtures with conductive particles (Fig. S5F).

Supplemental Material

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  • FIG S1 

    Numbers of reads were sufficient in all three sediment cores, as indicated by the flattening rarefraction curves (a) and a similar pattern for the rare operational taxonomic units (OTUs) estimator, Chao1 (b). Download FIG S1, PDF file, 0.2 MB.

    Copyright © 2018 Rotaru et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S2 

    16S amplicon sequencing (a) showed that Deltaproteobacteria (including Geobacter) were the most abundant Proteobacteria, and (b) DIET-capable Methanosarcinales and the H2-dependent methanotroph Methanomassilicoccus were the dominant methanogens. The most abundant Deltaproteobacteria OTU had as its closest cultured relative Geobacter spp.,independent of the BLAST database used (NCBI or JGI). Download FIG S2, PDF file, 0.04 MB.

    Copyright © 2018 Rotaru et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S3 

    Accumulation of methane and acetate in slurry incubation mixtures after 27 days of growth on different substrates. Methane (a) and acetate (b) accumulated in slurries provided with GAC (black), in controls amended with nonconductive glass beads (gray pattern), and in controls free of GAC (white). Download FIG S3, PDF file, 0.05 MB.

    Copyright © 2018 Rotaru et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S4 

    Magnetite stimulates methanogenesis more than GAC. An RA2 enrichment pregrown with GAC plus acetate was transferred with conductive magnetite (red), GAC (black),or without minerals (gray, dashed). The enrichment was grown in triplicate with a 20% inoculate. Download FIG S4, PDF file, 0.03 MB.

    Copyright © 2018 Rotaru et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S5 

    Geobacter targets could not be detected during nanoSIMS analyses of GAC-free cultures. Methanosarcina targets were also seldom detected (a) but could be detected during nanoSIMS (encircled in both the 13C fraction [b]) and by 32S, which showed the total biomass fraction (c). However, in these GAC-free incubation mixtures, Methanothrix-like filaments dominated (b and c), and incorporated [13C]acetate. Eubacteria (d) and Geobacter (e) targets could not be detected after SAO consortia were taken off conductive GAC for a single transfer. Only Methanosarcina cells persisted (d and e) in medium without conductive particles. Images are representative epifluorescence micrographs of 6 to 10 randomly selected fields. Download FIG S5, PDF file, 1.2 MB.

    Copyright © 2018 Rotaru et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S6 

    Methane production from acetate in mud-free enrichments spiked with spent filtrate (gray) or autoclaved spent filtrate (blue) versus control cultures without spent medium addition. Download FIG S6, PDF file, 0.03 MB.

    Copyright © 2018 Rotaru et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TEXT S1 

    Additional information regarding our methods. Download TEXT S1, DOCX file, 0.2 MB.

    Copyright © 2018 Rotaru et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S1 

    Primers used in this study. Download TABLE S1, DOCX file, 0.1 MB.

    Copyright © 2018 Rotaru et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S2 

    Read count and quality parameters for 16S rRNA gene amplicon sequencing of methanogenic zones (30 to 36 cm) from three Baltic Sea cores at station RA2. N (%) indicates the N-base percentage in the sequence reads; GC (%) is the GC content of the sequence reads as a percentage; Q20 and Q30 show the percentage bases for which the phred quality score was above 20 or 30, respectively. Download TABLE S2, DOCX file, 0.05 MB.

    Copyright © 2018 Rotaru et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Conductive Particles Enable Syntrophic Acetate Oxidation between Geobacter and Methanosarcina from Coastal Sediments
Amelia-Elena Rotaru, Federica Calabrese, Hryhoriy Stryhanyuk, Florin Musat, Pravin Malla Shrestha, Hannah Sophia Weber, Oona L. O. Snoeyenbos-West, Per O. J. Hall, Hans H. Richnow, Niculina Musat, Bo Thamdrup
mBio May 2018, 9 (3) e00226-18; DOI: 10.1128/mBio.00226-18

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Conductive Particles Enable Syntrophic Acetate Oxidation between Geobacter and Methanosarcina from Coastal Sediments
Amelia-Elena Rotaru, Federica Calabrese, Hryhoriy Stryhanyuk, Florin Musat, Pravin Malla Shrestha, Hannah Sophia Weber, Oona L. O. Snoeyenbos-West, Per O. J. Hall, Hans H. Richnow, Niculina Musat, Bo Thamdrup
mBio May 2018, 9 (3) e00226-18; DOI: 10.1128/mBio.00226-18
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    • ABSTRACT
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KEYWORDS

Desulfuromonadales
Geobacter
Methanosarcina
nanoSIMS
activated carbon
competitive exclusion
direct interspecies electron transfer
syntrophic acetate oxidation

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