Metabolism and Occurrence of Methanogenic and Sulfate-Reducing Syntrophic Acetate Oxidizing Communities in Haloalkaline Environments
Anaerobic syntrophic acetate oxidation (SAO) is a thermodynamically unfavorable process involving a syntrophic acetate oxidizing bacterium (SAOB) that forms interspecies electron carriers (IECs). These IECs are consumed by syntrophic partners, typically hydrogenotrophic methanogenic archaea or sulfa...
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Frontiers Media S.A.
2018-12-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2018.03039/full |
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| author | Peer H. A. Timmers Peer H. A. Timmers Charlotte D. Vavourakis Robbert Kleerebezem Jaap S. Sinninghe Damsté Jaap S. Sinninghe Damsté Gerard Muyzer Alfons J. M. Stams Alfons J. M. Stams Dimity Y. Sorokin Dimity Y. Sorokin Caroline M. Plugge Caroline M. Plugge |
| author_facet | Peer H. A. Timmers Peer H. A. Timmers Charlotte D. Vavourakis Robbert Kleerebezem Jaap S. Sinninghe Damsté Jaap S. Sinninghe Damsté Gerard Muyzer Alfons J. M. Stams Alfons J. M. Stams Dimity Y. Sorokin Dimity Y. Sorokin Caroline M. Plugge Caroline M. Plugge |
| author_sort | Peer H. A. Timmers |
| collection | DOAJ |
| description | Anaerobic syntrophic acetate oxidation (SAO) is a thermodynamically unfavorable process involving a syntrophic acetate oxidizing bacterium (SAOB) that forms interspecies electron carriers (IECs). These IECs are consumed by syntrophic partners, typically hydrogenotrophic methanogenic archaea or sulfate reducing bacteria. In this work, the metabolism and occurrence of SAOB at extremely haloalkaline conditions were investigated, using highly enriched methanogenic (M-SAO) and sulfate-reducing (S-SAO) cultures from south-western Siberian hypersaline soda lakes. Activity tests with the M-SAO and S-SAO cultures and thermodynamic calculations indicated that H2 and formate are important IECs in both SAO cultures. Metagenomic analysis of the M-SAO cultures showed that the dominant SAOB was ‘Candidatus Syntrophonatronum acetioxidans,’ and a near-complete draft genome of this SAOB was reconstructed. ‘Ca. S. acetioxidans’ has all genes necessary for operating the Wood–Ljungdahl pathway, which is likely employed for acetate oxidation. It also encodes several genes essential to thrive at haloalkaline conditions; including a Na+-dependent ATP synthase and marker genes for ‘salt-out‘ strategies for osmotic homeostasis at high soda conditions. Membrane lipid analysis of the M-SAO culture showed the presence of unusual bacterial diether membrane lipids which are presumably beneficial at extreme haloalkaline conditions. To determine the importance of SAO in haloalkaline environments, previously obtained 16S rRNA gene sequencing data and metagenomic data of five different hypersaline soda lake sediment samples were investigated, including the soda lakes where the enrichment cultures originated from. The draft genome of ‘Ca. S. acetioxidans’ showed highest identity with two metagenome-assembled genomes (MAGs) of putative SAOBs that belonged to the highly abundant and diverse Syntrophomonadaceae family present in the soda lake sediments. The 16S rRNA gene amplicon datasets of the soda lake sediments showed a high similarity of reads to ‘Ca. S. acetioxidans’ with abundance as high as 1.3% of all reads, whereas aceticlastic methanogens and acetate oxidizing sulfate-reducers were not abundant (≤0.1%) or could not be detected. These combined results indicate that SAO is the primary anaerobic acetate oxidizing pathway at extreme haloalkaline conditions performed by haloalkaliphilic syntrophic consortia. |
| first_indexed | 2024-12-14T00:53:34Z |
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| language | English |
| last_indexed | 2024-12-14T00:53:34Z |
| publishDate | 2018-12-01 |
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| series | Frontiers in Microbiology |
| spelling | doaj.art-21f8e2f7fc3848dfa0ebfd7d7b73a19e2022-12-21T23:23:42ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-12-01910.3389/fmicb.2018.03039425991Metabolism and Occurrence of Methanogenic and Sulfate-Reducing Syntrophic Acetate Oxidizing Communities in Haloalkaline EnvironmentsPeer H. A. Timmers0Peer H. A. Timmers1Charlotte D. Vavourakis2Robbert Kleerebezem3Jaap S. Sinninghe Damsté4Jaap S. Sinninghe Damsté5Gerard Muyzer6Alfons J. M. Stams7Alfons J. M. Stams8Dimity Y. Sorokin9Dimity Y. Sorokin10Caroline M. Plugge11Caroline M. Plugge12Laboratory of Microbiology, Wageningen University & Research, Wageningen, NetherlandsEuropean Centre of Excellence for Sustainable Water Technology, Wetsus, Leeuwarden, NetherlandsMicrobial Systems Ecology, Department of Freshwater and Marine Ecology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, NetherlandsDepartment of Biotechnology, Delft University of Technology, Delft, NetherlandsDepartment of Marine Microbiology and Biogeochemistry, NIOZ Netherlands Institute for Sea Research, Utrecht University, Utrecht, NetherlandsDepartment of Earth Sciences, Faculty of Geosciences, Utrecht University, Utrecht, NetherlandsMicrobial Systems Ecology, Department of Freshwater and Marine Ecology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, NetherlandsLaboratory of Microbiology, Wageningen University & Research, Wageningen, NetherlandsCentre of Biological Engineering, University of Minho, Braga, PortugalDepartment of Biotechnology, Delft University of Technology, Delft, NetherlandsWinogradsky Institute of Microbiology, Research Centre of Biotechnology, Russian Academy of Sciences, Moscow, RussiaLaboratory of Microbiology, Wageningen University & Research, Wageningen, NetherlandsEuropean Centre of Excellence for Sustainable Water Technology, Wetsus, Leeuwarden, NetherlandsAnaerobic syntrophic acetate oxidation (SAO) is a thermodynamically unfavorable process involving a syntrophic acetate oxidizing bacterium (SAOB) that forms interspecies electron carriers (IECs). These IECs are consumed by syntrophic partners, typically hydrogenotrophic methanogenic archaea or sulfate reducing bacteria. In this work, the metabolism and occurrence of SAOB at extremely haloalkaline conditions were investigated, using highly enriched methanogenic (M-SAO) and sulfate-reducing (S-SAO) cultures from south-western Siberian hypersaline soda lakes. Activity tests with the M-SAO and S-SAO cultures and thermodynamic calculations indicated that H2 and formate are important IECs in both SAO cultures. Metagenomic analysis of the M-SAO cultures showed that the dominant SAOB was ‘Candidatus Syntrophonatronum acetioxidans,’ and a near-complete draft genome of this SAOB was reconstructed. ‘Ca. S. acetioxidans’ has all genes necessary for operating the Wood–Ljungdahl pathway, which is likely employed for acetate oxidation. It also encodes several genes essential to thrive at haloalkaline conditions; including a Na+-dependent ATP synthase and marker genes for ‘salt-out‘ strategies for osmotic homeostasis at high soda conditions. Membrane lipid analysis of the M-SAO culture showed the presence of unusual bacterial diether membrane lipids which are presumably beneficial at extreme haloalkaline conditions. To determine the importance of SAO in haloalkaline environments, previously obtained 16S rRNA gene sequencing data and metagenomic data of five different hypersaline soda lake sediment samples were investigated, including the soda lakes where the enrichment cultures originated from. The draft genome of ‘Ca. S. acetioxidans’ showed highest identity with two metagenome-assembled genomes (MAGs) of putative SAOBs that belonged to the highly abundant and diverse Syntrophomonadaceae family present in the soda lake sediments. The 16S rRNA gene amplicon datasets of the soda lake sediments showed a high similarity of reads to ‘Ca. S. acetioxidans’ with abundance as high as 1.3% of all reads, whereas aceticlastic methanogens and acetate oxidizing sulfate-reducers were not abundant (≤0.1%) or could not be detected. These combined results indicate that SAO is the primary anaerobic acetate oxidizing pathway at extreme haloalkaline conditions performed by haloalkaliphilic syntrophic consortia.https://www.frontiersin.org/article/10.3389/fmicb.2018.03039/fullsyntrophic acetate oxidationhaloalkaliphilessoda lakessyntrophySAOBsyntrophic acetate oxidizing bacteria |
| spellingShingle | Peer H. A. Timmers Peer H. A. Timmers Charlotte D. Vavourakis Robbert Kleerebezem Jaap S. Sinninghe Damsté Jaap S. Sinninghe Damsté Gerard Muyzer Alfons J. M. Stams Alfons J. M. Stams Dimity Y. Sorokin Dimity Y. Sorokin Caroline M. Plugge Caroline M. Plugge Metabolism and Occurrence of Methanogenic and Sulfate-Reducing Syntrophic Acetate Oxidizing Communities in Haloalkaline Environments Frontiers in Microbiology syntrophic acetate oxidation haloalkaliphiles soda lakes syntrophy SAOB syntrophic acetate oxidizing bacteria |
| title | Metabolism and Occurrence of Methanogenic and Sulfate-Reducing Syntrophic Acetate Oxidizing Communities in Haloalkaline Environments |
| title_full | Metabolism and Occurrence of Methanogenic and Sulfate-Reducing Syntrophic Acetate Oxidizing Communities in Haloalkaline Environments |
| title_fullStr | Metabolism and Occurrence of Methanogenic and Sulfate-Reducing Syntrophic Acetate Oxidizing Communities in Haloalkaline Environments |
| title_full_unstemmed | Metabolism and Occurrence of Methanogenic and Sulfate-Reducing Syntrophic Acetate Oxidizing Communities in Haloalkaline Environments |
| title_short | Metabolism and Occurrence of Methanogenic and Sulfate-Reducing Syntrophic Acetate Oxidizing Communities in Haloalkaline Environments |
| title_sort | metabolism and occurrence of methanogenic and sulfate reducing syntrophic acetate oxidizing communities in haloalkaline environments |
| topic | syntrophic acetate oxidation haloalkaliphiles soda lakes syntrophy SAOB syntrophic acetate oxidizing bacteria |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2018.03039/full |
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