Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses
Abstract
We currently understand the carbon cycle in methanogenic environments as trophic interactions revolving around interspecies H2 transfer between organotrophs and methanogens. However, many H2-generating processes are thermodynamically sensitive to H2 accumulation and can be inhibited by high H2 concentrations produced by other metabolisms. 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 15 anaerobic digesters, we recover 1343 high-quality metagenome-assembled genomes (MAGs) and corresponding gene expression profiles for diverse uncultured lineages spanning 66 phyla and reconstruct their individual metabolic capacities. We discover that diverse uncultured organotrophic populations can drive H2-sensitive degradation through (i) metabolic coupling with concurrent H2-tolerant catabolism, (ii) unprecedented shifts from H2 generation to CO2-reducing formate transfer and cytochrome/pili-mediated direct interspecies electron transfer for avoiding thermodynamic conflict, and (iii) integration of low-concentration O2 as an ancillary thermodynamics-enhancing electron sink. Archaeal populations in situ support the above processes through novel metabolisms distinct from conventional methanogenesis – high-affinity H2 oxidation driven by methyl-reducing methanogenesis and concomitant uptake of formate, electrons, and acetate from HS metabolism by Methanothrix. In total, synthesis of omics analyses andmore »
- Authors:
-
[6];
[2]
- Univ. of Illinois at Urbana-Champaign, IL (United States); National Institute of Advanced Industrial Science and Technology, Tsukuba (Japan)
- Univ. of Illinois at Urbana-Champaign, IL (United States)
- National Institute of Advanced Industrial Science and Technology, Tsukuba (Japan)
- City University of Hong Kong, Kowloon (Hong Kong)
- Imperial College, London (United Kingdom)
- Univ. of Oklahoma, Norman, OK (United States)
- Publication Date:
- Research Org.:
- Univ. of Oklahoma, Norman, OK (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division
- OSTI Identifier:
- 1644640
- Grant/Contract Number:
- FG02-96ER20214; AC02-05CH1123
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Microbiome
- Additional Journal Information:
- Journal Volume: 8; Journal Issue: 1; Journal ID: ISSN 2049-2618
- Publisher:
- BioMed Central
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Catabolism; Interactions; Uncultured organisms; Eco-thermodynamics; Methanogenic bioprocesses
Citation Formats
Nobu, Masaru K., Narihiro, Takashi, Mei, Ran, Kamagata, Yoichi, Lee, Patrick K. H., Lee, Po-Heng, McInerney, Michael J., and Liu, Wen-Tso. Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses. United States: N. p., 2020.
Web. doi:10.1186/s40168-020-00885-y.
Nobu, Masaru K., Narihiro, Takashi, Mei, Ran, Kamagata, Yoichi, Lee, Patrick K. H., Lee, Po-Heng, McInerney, Michael J., & Liu, Wen-Tso. Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses. United States. https://doi.org/10.1186/s40168-020-00885-y
Nobu, Masaru K., Narihiro, Takashi, Mei, Ran, Kamagata, Yoichi, Lee, Patrick K. H., Lee, Po-Heng, McInerney, Michael J., and Liu, Wen-Tso. Fri .
"Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses". United States. https://doi.org/10.1186/s40168-020-00885-y. https://www.osti.gov/servlets/purl/1644640.
@article{osti_1644640,
title = {Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses},
author = {Nobu, Masaru K. and Narihiro, Takashi and Mei, Ran and Kamagata, Yoichi and Lee, Patrick K. H. and Lee, Po-Heng and McInerney, Michael J. and Liu, Wen-Tso},
abstractNote = {We currently understand the carbon cycle in methanogenic environments as trophic interactions revolving around interspecies H2 transfer between organotrophs and methanogens. However, many H2-generating processes are thermodynamically sensitive to H2 accumulation and can be inhibited by high H2 concentrations produced by other metabolisms. 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 15 anaerobic digesters, we recover 1343 high-quality metagenome-assembled genomes (MAGs) and corresponding gene expression profiles for diverse uncultured lineages spanning 66 phyla and reconstruct their individual metabolic capacities. We discover that diverse uncultured organotrophic populations can drive H2-sensitive degradation through (i) metabolic coupling with concurrent H2-tolerant catabolism, (ii) unprecedented shifts from H2 generation to CO2-reducing formate transfer and cytochrome/pili-mediated direct interspecies electron transfer for avoiding thermodynamic conflict, and (iii) integration of low-concentration O2 as an ancillary thermodynamics-enhancing electron sink. Archaeal populations in situ support the above processes through novel metabolisms distinct from conventional methanogenesis – high-affinity H2 oxidation driven by methyl-reducing methanogenesis and concomitant uptake of formate, electrons, and acetate from HS metabolism by Methanothrix. In total, synthesis of omics analyses and eco-thermodynamics reveals overlooked metabolic behavior and interactions of uncultured organisms that address a central issue in methanogenic carbon cycling, thermodynamic conflict among diverse concurrent metabolic processes.},
doi = {10.1186/s40168-020-00885-y},
journal = {Microbiome},
number = 1,
volume = 8,
place = {United States},
year = {Fri Jul 24 00:00:00 EDT 2020},
month = {Fri Jul 24 00:00:00 EDT 2020}
}
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