Dataset Information

Complete genome sequence of Methanoculleus bourgensis strain MAB1, the syntrophic partner of mesophilic acetate-oxidising bacteria (SAOB).

ABSTRACT: Methanoculleus bourgensis strain MAB1 has been identified as the hydrogenotrophic partner of mesophilic acetate-oxidising bacteria, a syntrophic relationship operating close to the thermodynamic equilibrium and of considerable importance in ammonia-rich engineered biogas processes. Methanoculleus bourgensis strain MAB1 belongs to the order Methanomicrobiales, family Methanomicrobiaceae, within the phylum Euryarchaeota. The genome shows a total size of 2,859,299 bp encoding 3450 predicted protein-encoding genes, of which only 1472 (43 %) have been assigned tentative functions. The genome encodes further 44 tRNA genes and three rRNA genes (5S, 16S and 23S rRNA). This study presents assembling and annotation features as well as genomic traits related to ammonia tolerance and methanogenesis.

SUBMITTER: Manzoor S

PROVIDER: S-EPMC5062929 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Complete genome sequence of Methanoculleus bourgensis strain MAB1, the syntrophic partner of mesophilic acetate-oxidising bacteria (SAOB).

Manzoor Shahid S Schnürer Anna A Bongcam-Rudloff Erik E Müller Bettina B

Standards in genomic sciences 20161012

Methanoculleus bourgensis strain MAB1 has been identified as the hydrogenotrophic partner of mesophilic acetate-oxidising bacteria, a syntrophic relationship operating close to the thermodynamic equilibrium and of considerable importance in ammonia-rich engineered biogas processes. Methanoculleus bourgensis strain MAB1 belongs to the order Methanomicrobiales, family Methanomicrobiaceae, within the phylum Euryarchaeota. The genome shows a total size of 2,859,299 ...[more]

PMID: 27777650

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Project description:Syntrophaceticus schinkii is a mesophilic, anaerobic bacterium capable of oxidising acetate to CO2 and H2 in intimate association with a methanogenic partner, a syntrophic relationship which operates close to the energetic limits of microbial life. Syntrophaceticus schinkii has been identified as a key organism in engineered methane-producing processes relying on syntrophic acetate oxidation as the main methane-producing pathway. However, due to strict cultivation requirements and difficulties in reconstituting the thermodynamically unfavourable acetate oxidation, the physiology of this functional group is poorly understood. Genome-guided and whole transcriptome analyses performed in the present study provide new insights into habitat adaptation, syntrophic acetate oxidation and energy conservation. The working draft genome of Syntrophaceticus schinkii indicates limited metabolic capacities, with lack of organic nutrient uptake systems, chemotactic machineries, carbon catabolite repression and incomplete biosynthesis pathways. Ech hydrogenase, [FeFe] hydrogenases, [NiFe] hydrogenases, F1F0-ATP synthase and membrane-bound and cytoplasmic formate dehydrogenases were found clearly expressed, whereas Rnf and a predicted oxidoreductase/heterodisulphide reductase complex, both found encoded in the genome, were not expressed under syntrophic growth condition. A transporter sharing similarities to the high-affinity acetate transporters of aceticlastic methanogens was also found expressed, suggesting that Syntrophaceticus schinkii can potentially compete with methanogens for acetate. Acetate oxidation seems to proceed via the Wood-Ljungdahl pathway as all genes involved in this pathway were highly expressed. This study shows that Syntrophaceticus schinkii is a highly specialised, habitat-adapted organism relying on syntrophic acetate oxidation rather than metabolic versatility. By expanding its complement of respiratory complexes, it might overcome limiting bioenergetic barriers, and drive efficient energy conservation from reactions operating close to the thermodynamic equilibrium, which might enable S. schinkii to occupy the same niche as the aceticlastic methanogens. The knowledge gained here will help specify process conditions supporting efficient and robust biogas production and will help identify mechanisms important for the syntrophic lifestyle.

Project description:BackgroundSyntrophic acetate oxidation (SAO) is the predominant pathway for methane production in high ammonia anaerobic digestion processes. The bacteria (SAOB) occupying this niche and the metabolic pathway are poorly understood. Phylogenetic diversity and strict cultivation requirements hinder comprehensive research and discovery of novel SAOB. Most SAOB characterised to date are affiliated to the physiological group of acetogens. Formyltetrahydrofolate synthetase is a key enzyme of both acetogenic and SAO metabolism. The encoding fhs gene has therefore been identified as a suitable functional marker, using a newly designed primer pair. In this comparative study, we used a combination of terminal restriction fragment length polymorphism profiling, clone-based comparison, qPCR and Illumina amplicon sequencing to assess the bacterial community and acetogenic sub-community prevailing in high- and low-ammonia laboratory-scale digesters in order to delineate potential SAOB communities. Potential candidates identified were further tracked in a number of low-ammonia and high-ammonia laboratory-scale and large-scale digesters in order to reveal a potential function in SAO.ResultsAll methodical approaches revealed significant changes in the bacterial community composition concurrently with increasing ammonia and predominance of SAO. The acetogenic community under high ammonia conditions was revealed to be generally heterogeneous, but formed distinct phylogenetic clusters. The clusters differed clearly from those found under low-ammonia conditions and represented an acetogenic assemblage unique for biogas processes and recurring in a number of high-ammonia processes, indicating potential involvement in SAO.ConclusionsThe phylogenetic affiliation and population dynamics observed point to a key community, belonging mainly to the Clostridia class, in particular to the orders Clostridiales and Thermoanaerobacterales, which appear to specialise in SAO rather than being metabolically versatile. Overall, the results reported here provide evidence of functional importance of the bacterial families identified in high-ammonia systems and extend existing knowledge of bacterial and acetogenic assemblages at low and high ammonia levels. This information will be of help in monitoring and assessing the impacts on the SAOB community in order to identify characteristics of robust and productive high ammonia biogas processes.

Project description:Syntrophic acetate oxidation operates close to the thermodynamic equilibrium and very little is known about the participating organisms and their metabolism. Clostridium ultunense is one of the most abundant syntrophic acetate-oxidising bacteria (SAOB) that are found in engineered biogas processes operating with high ammonia concentrations. It has been proven to oxidise acetate in cooperation with hydrogenotrophic methanogens. There is evidence that the Wood-Ljungdahl (WL) pathway plays an important role in acetate oxidation. In this study, we analysed the physiological and metabolic capacities of C. ultunense strain Esp and strain BST on genome scale and conducted a comparative study of all the known characterised SAOB, namely Syntrophaceticus schinkii, Thermacetogenium phaeum, Tepidanaerobacter acetatoxydans, and Pseudothermotoga lettingae. The results clearly indicated physiological robustness to be beneficial for anaerobic digestion environments and revealed unexpected metabolic diversity with respect to acetate oxidation and energy conservation systems. Unlike S. schinkii and Th. phaeum, C. ultunense clearly does not employ the oxidative WL pathway for acetate oxidation, as its genome (and that of P. lettingae) lack important key genes. In both of those species, a proton motive force is likely formed by chemical protons involving putative electron-bifurcating [Fe-Fe] hydrogenases rather than proton pumps. No genes encoding a respiratory Ech (energy-converting hydrogenase), as involved in energy conservation in Th. phaeum and S. schinkii, were identified in C. ultunense and P. lettingae. Moreover, two respiratory complexes sharing similarities to the proton-translocating ferredoxin:NAD⁺ oxidoreductase (Rnf) and the Na⁺ pumping NADH:quinone hydrogenase (NQR) were predicted. These might form a respiratory chain that is involved in the reduction of electron acceptors rather than protons. However, involvement of these complexes in acetate oxidation in C. ultunense and P. lettingae needs further study. This genome-based comparison provides a solid platform for future meta-proteomics and meta-transcriptomics studies and for metabolic engineering, control, and monitoring of SAOB.

Project description:Microbial inhibition by high ammonia concentrations is a recurring problem that significantly restricts methane formation from intermediate acids, i.e., propionate and acetate, during anaerobic digestion of protein-rich waste material. Studying the syntrophic communities that perform acid conversion is challenging, due to their relatively low abundance within the microbial communities typically found in biogas processes and disruption of their cooperative behavior in pure cultures. To overcome these limitations, this study examined growth parameters and microbial community dynamics of highly enriched mesophilic and ammonia-tolerant syntrophic propionate and acetate-oxidizing communities and analyzed their metabolic activity and cooperative behavior using metagenomic and metatranscriptomic approaches. Cultivation in batch set-up demonstrated biphasic utilization of propionate, wherein acetate accumulated and underwent oxidation before complete degradation of propionate. Three key species for syntrophic acid degradation were inferred from genomic sequence information and gene expression: a syntrophic propionate-oxidizing bacterium (SPOB) "Candidatus Syntrophopropionicum ammoniitolerans", a syntrophic acetate-oxidizing bacterium (SAOB) Syntrophaceticus schinkii and a novel hydrogenotrophic methanogen, for which we propose the provisional name "Candidatus Methanoculleus ammoniitolerans". The results revealed consistent transcriptional profiles of the SAOB and the methanogen both during propionate and acetate oxidation, regardless of the presence of an active propionate oxidizer. Gene expression indicated versatile capabilities of the two syntrophic bacteria, utilizing both molecular hydrogen and formate as an outlet for reducing equivalents formed during acid oxidation, while conserving energy through build-up of sodium/proton motive force. The methanogen used hydrogen and formate as electron sources. Furthermore, results of the present study provided a framework for future research into ammonia tolerance, mobility, aggregate formation and interspecies cooperation.

Dataset Information

Complete genome sequence of Methanoculleus bourgensis strain MAB1, the syntrophic partner of mesophilic acetate-oxidising bacteria (SAOB).

Publications

Complete genome sequence of <i>Methanoculleus bourgensis</i> strain MAB1, the syntrophic partner of mesophilic acetate-oxidising bacteria (SAOB).

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