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Metagenomic and Metatranscriptomic Analyses Revealed Uncultured Bacteroidales Populations as the Dominant Proteolytic Amino Acid Degraders in Anaerobic Digesters.

ABSTRACT: Current understanding of amino acid (AA) degraders in anaerobic digesters is mainly based on cultured species, whereas microorganisms that play important roles in a complex microbial community remain poorly characterized. This study investigated short-term enrichments degrading single AAs using metagenomics and metatranscriptomics. Metagenomic analysis revealed that populations related to cultured AA degraders had an abundance <2.5% of the sequences. In contrast, metagenomic-assembled bins related to uncultured Bacteroidales collectively accounted for >35% of the sequences. Phylogenetic analyses suggested that these Bacteroidales populations represented a yet-to-be characterized family lineage, i.e., Bacteroidetes vadinHA17. The bins possessed the genetic capacity related to protein degradation, including surface adhesion (3-7 genes), secreted peptidase (52-77 genes), and polypeptide-specific transporters (2-5 genes). Furthermore, metatranscriptomics revealed that these Bacteroidales populations expressed the complete metabolic pathways for degrading 16 to 17 types of AAs in enrichments fed with respective substrates. These characteristics were distinct from cultured AA degraders including Acidaminobacter and Peptoclostridium, suggesting the uncultured Bacteroidales were the major protein-hydrolyzing and AA-degrading populations. These uncultured Bacteroidales were further found to be dominant and active in full-scale anaerobic digesters, indicating their important ecological roles in the native habitats. "Candidatus Aminobacteroidaceae" was proposed to represent the previously uncharted family Bacteroidetes vadinHA17.

SUBMITTER: Mei R

PROVIDER: S-EPMC7661554 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Metagenomic and Metatranscriptomic Analyses Revealed Uncultured Bacteroidales Populations as the Dominant Proteolytic Amino Acid Degraders in Anaerobic Digesters.

Mei Ran R Nobu Masaru K MK Narihiro Takashi T Liu Wen-Tso WT

Frontiers in microbiology 20201030

Current understanding of amino acid (AA) degraders in anaerobic digesters is mainly based on cultured species, whereas microorganisms that play important roles in a complex microbial community remain poorly characterized. This study investigated short-term enrichments degrading single AAs using metagenomics and metatranscriptomics. Metagenomic analysis revealed that populations related to cultured AA degraders had an abundance <2.5% of the sequences. In contrast, metagenomic-assembled bins relat ...[more]

PMID: 33193263

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Project description:BackgroundThe expansion of renewable energy produced by windmills and photovoltaic panels has generated a considerable electricity surplus, which can be utilized in water electrolysis systems for hydrogen production. The resulting hydrogen can then be funneled to anaerobic digesters for biogas upgrading (biomethanation) purposes (power-to-methane) or to produce high value-added compounds such as short-chain fatty acids (power-to-chemicals). Genome-centric metagenomics and metatranscriptomic analyses were performed to better understand the metabolic dynamics associated with H2 injection in two different configurations of anaerobic digesters treating acidic wastes, specifically cheese manufacturing byproducts. These approaches revealed the key-genes involved in methanation and carbon fixation pathways at species level.ResultsThe biogas upgrading process in the single-stage configuration increased the CH4 content by 7%. The dominant methanogenic species responsible for the upregulation of the hydrogenotrophic pathway in this reactor was Methanothermobacter wolfeii UC0008. In the two-stage configuration, H2 injection induced an upregulation of CO2 fixation pathways producing short-chain fatty acids, mainly acetate and butyrate. In this configuration, the abundant species Anaerobaculum hydrogeniformans UC0046 and Defluviitoga tunisiensis UC0050 primarily upregulated genes related to electron transport chains, suggesting putative syntrophisms with hydrogen scavenger microbes. Interestingly, Tepidanaerobacter acetatoxydans UC0018 did not act as an acetate-oxidizer in either reactor configurations, and instead regulated pathways involved in acetate production and uptake. A putative syntrophic association between Coprothermobacter proteolyticus UC0011 and M. wolfeii UC0008 was proposed in the two-stage reactor. In order to support the transcriptomic findings regarding the hydrogen utilization routes, an advanced bioconversion model was adapted for the simulation of the single- and two-stage reactor setups.ConclusionsThis is the first study investigating biogas reactor metatranscriptome dynamics following hydrogen injection for biomethanation and carbon fixation to short-chain fatty acids purposes. The same microbes showed different patterns of metabolic regulation in the two reactor configurations. It was observed an effect of the specialized acidogenic reactor on the overall microbial consortium composition and activity in the two-stage digester. There were also suggested the main species responsible for methanation, short-chain fatty acids production, and electron transport chain mechanisms, in both reactor configurations.

Project description:Conventional anaerobic digesters (ADs) treating dairy manure are fed with raw or fermented manure rich in volatile fatty acids (VFAs). In contrast, pre-fermented AD (PF-AD) is fed with the more recalcitrant, fiber-rich fraction of manure that has been pre-fermented and depleted of VFAs. Thus, the substrate of PF-AD may be likened to a lean diet rich in fibers while the pre-fermentation stage fermenter is fed a relatively rich diet containing labile organic substances. Previous results have shown that conventional and pre-fermented ADs fed with raw or pre-fermented manure, respectively, produced comparable methane yields. The primary objective of this study was to characterize, using next-generation DNA sequencing, the bacterial communities in various bioreactors (pre-fermentation stage fermenter; various operational arrangements PF-AD; conventional single-stage AD; and a full scale AD) and compare the Firmicutes to Bacteroidetes (F/B) ratios in these different systems. Firmicutes and Bacteroidetes constituted the two most abundant phyla in all AD samples analyzed, as well as most of the samples analyzed in the fermenters and manure samples. Higher relative abundance of Bacteroidetes, ranging from 26% to 51% of bacteria, tended to be associated with PF-AD samples, while the highest relative abundance of Firmicutes occurred in the fermenter (maximum of 76% of bacteria) and manure (maximum of 66% of bacteria) samples. On average, primary stage fermenters exhibited microbiological traits linked to obesity: higher F/B ratios and a 'diet' that is less fibrous and more labile compared to that fed to PF-AD. On the other hand, microbial characteristics associated with leanness (lower F/B ratios combined with fibrous substrate) were associated with PF-AD. We propose that bacterial communities in AD shift depending on the quality of substrate, which ultimately results in maintaining VFA yields in PF-AD, similar to the role of bacterial communities and a high fiber diet in lean mice.

Dataset Information

Metagenomic and Metatranscriptomic Analyses Revealed Uncultured Bacteroidales Populations as the Dominant Proteolytic Amino Acid Degraders in Anaerobic Digesters.

Publications

Metagenomic and Metatranscriptomic Analyses Revealed Uncultured Bacteroidales Populations as the Dominant Proteolytic Amino Acid Degraders in Anaerobic Digesters.

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