Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses
Abstract Background Current 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...
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doaj-ab95f3076748430cb1ac34b97f6dc5892020-11-25T03:04:12ZengBMCMicrobiome2049-26182020-07-018111610.1186/s40168-020-00885-yCatabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocessesMasaru K. Nobu0Takashi Narihiro1Ran Mei2Yoichi Kamagata3Patrick K. H. Lee4Po-Heng Lee5Michael J. McInerney6Wen-Tso Liu7Department of Civil and Environmental Engineering, University of Illinois at Urbana-ChampaignDepartment of Civil and Environmental Engineering, University of Illinois at Urbana-ChampaignDepartment of Civil and Environmental Engineering, University of Illinois at Urbana-ChampaignBioproduction Research Institute, National Institute of Advanced Industrial Science and TechnologySchool of Energy and Environment, City University of Hong KongDepartment of Civil and Environmental Engineering, Imperial CollegeDepartment of Microbiology and Plant Biology, University of OklahomaDepartment of Civil and Environmental Engineering, University of Illinois at Urbana-ChampaignAbstract Background Current 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. Results To 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. Conclusion Integration 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. Video Abstracthttp://link.springer.com/article/10.1186/s40168-020-00885-yCatabolismInteractionsUncultured organismsEco-thermodynamicsMethanogenic bioprocesses |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Masaru K. Nobu Takashi Narihiro Ran Mei Yoichi Kamagata Patrick K. H. Lee Po-Heng Lee Michael J. McInerney Wen-Tso Liu |
spellingShingle |
Masaru K. Nobu Takashi Narihiro Ran Mei Yoichi Kamagata Patrick K. H. Lee Po-Heng Lee Michael J. McInerney Wen-Tso Liu Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses Microbiome Catabolism Interactions Uncultured organisms Eco-thermodynamics Methanogenic bioprocesses |
author_facet |
Masaru K. Nobu Takashi Narihiro Ran Mei Yoichi Kamagata Patrick K. H. Lee Po-Heng Lee Michael J. McInerney Wen-Tso Liu |
author_sort |
Masaru K. Nobu |
title |
Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses |
title_short |
Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses |
title_full |
Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses |
title_fullStr |
Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses |
title_full_unstemmed |
Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses |
title_sort |
catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses |
publisher |
BMC |
series |
Microbiome |
issn |
2049-2618 |
publishDate |
2020-07-01 |
description |
Abstract Background Current 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. Results To 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. Conclusion Integration 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. Video Abstract |
topic |
Catabolism Interactions Uncultured organisms Eco-thermodynamics Methanogenic bioprocesses |
url |
http://link.springer.com/article/10.1186/s40168-020-00885-y |
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