Abstract
BackgroundCurrent understanding of the carbon cycle in methanogenic environments involves trophic interactions such as interspecies H2 transfer between organotrophs and methanogens. However, many metabolic processes are thermodynamically sensitive to H2 accumulation and can be inhibited by H2 produced from co-occurring metabolisms. Strategies for driving thermodynamically competing metabolisms in methanogenic environments remain unexplored.ResultsTo uncover how anaerobes combat this H2 conflict in situ, we employ metagenomics and metatranscriptomics to revisit a model ecosystem that has inspired many foundational discoveries in anaerobic ecology—methanogenic bioreactors. Through analysis of 17 anaerobic digesters, we recovered 1343 high-quality metagenome-assembled genomes and corresponding gene expression profiles for uncultured lineages spanning 66 phyla and reconstructed their metabolic capacities. We discovered that diverse uncultured populations can drive H2-sensitive metabolisms through (i) metabolic coupling with concurrent H2-tolerant catabolism, (ii) forgoing H2 generation in favor of interspecies transfer of formate and electrons (cytochrome- and pili-mediated) to avoid thermodynamic conflict, and (iii) integration of low-concentration O2 metabolism as an ancillary thermodynamics-enhancing electron sink. Archaeal populations support these processes through unique methanogenic metabolisms—highly favorable H2 oxidation driven by methyl-reducing methanogenesis and tripartite uptake of formate, electrons, and acetate.ConclusionIntegration of omics and eco-thermodynamics revealed overlooked behavior and interactions of uncultured organisms, including coupling favorable and unfavorable metabolisms, shifting from H2 to formate transfer, respiring low-concentration O2, performing direct interspecies electron transfer, and interacting with high H2-affinity methanogenesis. These findings shed light on how microorganisms overcome a critical obstacle in methanogenic carbon cycles we had hitherto disregarded and provide foundational insight into anaerobic microbial ecology.7-KWLZT2hLDf6jAPRuutn9Video
Highlights
Current understanding of the carbon cycle in methanogenic environments involves trophic interactions such as interspecies H2 transfer between organotrophs and methanogens
Many H2-generating metabolic processes are thermodynamically favorable and can produce H2 at high concentrations (H2-tolerant, HT, [H2]max ≥ 100 Pa) (e.g., 1020 Pa for glucose degradation; Fig. 1b and S1), whilst others can be inhibited by much lower H2 concentrations (H2-sensitive, HS, [H2]max < < 100 Pa) (e.g., 2.8 Pa H2 for butyrate degradation; Fig. 1b and S1) [18,19,20]. (The concentration threshold was set at 100 Pa due to the large observed gap in H2 tolerances between 16 and 119 Pa; Fig. S1 and Table S1.) H2-scavenging methanogens can maintain low H2 concentrations to symbiotically support organisms performing HS metabolism, the high
Out of the obtained Metagenome-assembled genome (MAG), only 181 were assignable to cultured genera and the remaining belonged to various uncultured genus(289 MAGs), family- (303), order- (199), class- (110), and phylum-level lineages (261) (Fig. 2)
Summary
Current understanding of the carbon cycle in methanogenic environments involves trophic interactions such as interspecies H2 transfer between organotrophs and methanogens. Methanogenic bioprocesses are capable of converting municipal and industrial waste to methane and, are paramount for achieving a sustainable environment [1, 2] These processes have served as model ecosystems throughout the history of anaerobic microbiology, including the discovery of syntrophic bacteria [3,4,5], isolation of model H2- [6] and acetate-utilizing [7,8,9] methane-generating archaea, and characterization of novel modes of bacteria-archaea symbiosis [10, 11]. In the well-accepted scheme of methanogenic carboncycling, carbohydrate, AA, and FA degraders, all generate and transfer H2 to methanogens (Fig. 1a) due to the lack of favorable electron acceptors This H2 transfer is a critical component of methanogenic decomposition as many processes cannot proceed without H2 being maintained at low concentrations, an interaction known as “syntrophy” [18]. Many H2-generating metabolic processes are thermodynamically favorable and can produce H2 at high concentrations (H2-tolerant, HT, [H2]max ≥ 100 Pa) (e.g., 1020 Pa for glucose degradation; Fig. 1b and S1), whilst others can be inhibited by much lower H2 concentrations (H2-sensitive, HS, [H2]max < < 100 Pa) (e.g., 2.8 Pa H2 for butyrate degradation; Fig. 1b and S1) [18,19,20]. (The concentration threshold was set at 100 Pa due to the large observed gap in H2 tolerances between 16 and 119 Pa; Fig. S1 and Table S1.) H2-scavenging methanogens can maintain low H2 concentrations to symbiotically support organisms performing HS metabolism (an interaction known as “syntrophy”), the high
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