In:
Microbiome, Springer Science and Business Media LLC, Vol. 8, No. 1 ( 2020-12)
Abstract:
Current understanding of the carbon cycle in methanogenic environments involves trophic interactions such as interspecies H 2 transfer between organotrophs and methanogens. However, many metabolic processes are thermodynamically sensitive to H 2 accumulation and can be inhibited by H 2 produced from co-occurring metabolisms. Strategies for driving thermodynamically competing metabolisms in methanogenic environments remain unexplored. Results To uncover how anaerobes combat this H 2 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 H 2 -sensitive metabolisms through (i) metabolic coupling with concurrent H 2 -tolerant catabolism, (ii) forgoing H 2 generation in favor of interspecies transfer of formate and electrons (cytochrome- and pili-mediated) to avoid thermodynamic conflict, and (iii) integration of low-concentration O 2 metabolism as an ancillary thermodynamics-enhancing electron sink. Archaeal populations support these processes through unique methanogenic metabolisms—highly favorable H 2 oxidation driven by methyl-reducing methanogenesis and tripartite uptake of formate, electrons, and acetate. Conclusion Integration of omics and eco-thermodynamics revealed overlooked behavior and interactions of uncultured organisms, including coupling favorable and unfavorable metabolisms, shifting from H 2 to formate transfer, respiring low-concentration O 2 , performing direct interspecies electron transfer, and interacting with high H 2 -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.
Type of Medium:
Online Resource
ISSN:
2049-2618
DOI:
10.1186/s40168-020-00885-y
DOI:
10.21203/rs.3.rs-106057/v1
Language:
English
Publisher:
Springer Science and Business Media LLC
Publication Date:
2020
detail.hit.zdb_id:
2697425-3
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