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Methanogenic archaea and sulfate reducing bacteria co-cultured on acetate: teamwork or coexistence?

ABSTRACT: Acetate is a major product of fermentation processes and an important substrate for sulfate reducing bacteria and methanogenic archaea. Most studies on acetate catabolism by sulfate reducers and methanogens have used pure cultures. Less is known about acetate conversion by mixed pure cultures and the interactions between both groups. We tested interspecies hydrogen transfer and coexistence between marine methanogens and sulfate reducers using mixed pure cultures of two types of microorganisms. First, Desulfovibrio vulgaris subsp. vulgaris (DSM 1744), a hydrogenotrophic sulfate reducer, was cocultured together with the obligate aceticlastic methanogen Methanosaeta concilii using acetate as carbon and energy source. Next, Methanococcus maripaludis S2, an obligate H2- and formate-utilizing methanogen, was used as a partner organism to M. concilii in the presence of acetate. Finally, we performed a coexistence experiment between M. concilii and an acetotrophic sulfate reducer Desulfobacter latus AcSR2. Our results showed that D. vulgaris was able to reduce sulfate and grow from hydrogen leaked by M. concilii. In the other coculture, M. maripaludis was sustained by hydrogen leaked by M. concilii as revealed by qPCR. The growth of the two aceticlastic microbes indicated co-existence rather than competition. Altogether, our results indicate that H2 leaking from M. concilii could be used by efficient H2-scavengers. This metabolic trait, revealed from coculture studies, brings new insight to the metabolic flexibility of methanogens and sulfate reducers residing in marine environments in response to changing environmental conditions and community compositions. Using dedicated physiological studies we were able to unravel the occurrence of less obvious interactions between marine methanogens and sulfate-reducing bacteria.

SUBMITTER: Ozuolmez D

PROVIDER: S-EPMC4445324 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Methanogenic archaea and sulfate reducing bacteria co-cultured on acetate: teamwork or coexistence?

Ozuolmez Derya D Na Hyunsoo H Lever Mark A MA Kjeldsen Kasper U KU Jørgensen Bo B BB Plugge Caroline M CM

Frontiers in microbiology 20150527

Acetate is a major product of fermentation processes and an important substrate for sulfate reducing bacteria and methanogenic archaea. Most studies on acetate catabolism by sulfate reducers and methanogens have used pure cultures. Less is known about acetate conversion by mixed pure cultures and the interactions between both groups. We tested interspecies hydrogen transfer and coexistence between marine methanogens and sulfate reducers using mixed pure cultures of two types of microorganisms. F ...[more]

PMID: 26074892

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Project description:BackgroundOver three-fifths of the world's known crude oil cannot be recovered using state-of-the-art techniques, but microbial conversion of petroleum hydrocarbons trapped in oil reservoirs to methane is one promising path to increase the recovery of fossil fuels. The process requires cooperation between syntrophic bacteria and methanogenic archaea, which can be affected by sulfate-reducing prokaryotes (SRPs). However, the effects of sulfate on hydrocarbon degradation and methane production remain elusive, and the microbial communities involved are not well understood.ResultsIn this study, a methanogenic hexadecane-degrading enrichment culture was treated with six different concentrations of sulfate ranging from 0.5 to 25 mM. Methane production and maximum specific methane production rate gradually decreased to 44 and 56% with sulfate concentrations up to 25 mM, respectively. There was a significant positive linear correlation between the sulfate reduction/methane production ratio and initial sulfate concentration, which remained constant during the methane production phase. The apparent methanogenesis fractionation factor (αapp) gradually increased during the methane production phase in each treatment, the αapp for the treatments with lower sulfate (0.5-4 mM) eventually plateaued at ~1.047, but that for the treatment with 10-25 mM sulfate only reached ~1.029. The relative abundance levels of Smithella and Methanoculleus increased almost in parallel with the increasing sulfate concentrations. Furthermore, the predominant sulfate reducer communities shifted from Desulfobacteraceae in the low-sulfate cultures to Desulfomonile in the high-sulfate cultures.ConclusionThe distribution of hexadecane carbon between methane-producing and sulfate-reducing populations is dependent on the initial sulfate added, and not affected during the methane production period. There was a relative increase in hydrogenotrophic methanogenesis activity over time for all sulfate treatments, whereas the total activity was inhibited by sulfate addition. Both Smithella and Methanoculleus, the key alkane degraders and methane producers, can adapt to sulfate stress. Specifically, different SRP populations were stimulated at various sulfate concentrations. These results could help to evaluate interactions between sulfate-reducing and methanogenic populations during anaerobic hydrocarbon degradation in oil reservoirs.

Project 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.

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Methanogenic archaea and sulfate reducing bacteria co-cultured on acetate: teamwork or coexistence?

Publications

Methanogenic archaea and sulfate reducing bacteria co-cultured on acetate: teamwork or coexistence?

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