Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses

Nobu, Masaru K.; Narihiro, Takashi; Mei, Ran; Kamagata, Yoichi; Lee, Patrick K. H.; Lee, Po-Heng; McInerney, Michael J.; Liu, Wen-Tso

doi:10.1186/s40168-020-00885-y

Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses

Journal Article · Fri Jul 24 00:00:00 EDT 2020 · Microbiome

DOI:https://doi.org/10.1186/s40168-020-00885-y· OSTI ID:1644640

Nobu, Masaru K. ^[1]; Narihiro, Takashi ^[2]; Mei, Ran ^[3]; Kamagata, Yoichi ^[4]; Lee, Patrick K. H. ^[5]; Lee, Po-Heng ^[6]; ^[7]; ^[3]

Univ. of Illinois at Urbana-Champaign, IL (United States); National Institute of Advanced Industrial Science and Technology, Tsukuba (Japan); University of Oklahoma
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)

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.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of Oklahoma, Norman, OK (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division

Grant/Contract Number:: FG02-96ER20214

OSTI ID:: 1644640

Journal Information:: Microbiome, Journal Name: Microbiome Journal Issue: 1 Vol. 8; ISSN 2049-2618

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
Catabolism
Eco-thermodynamics
Interactions
Methanogenic bioprocesses
Uncultured organisms

Additional file 1 of Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses Nobu, Masaru K.; Narihiro, Takashi; Mei, Ran https://doi.org/10.6084/m9.figshare.12715358 The current record is supplemented by this image	image	January 2020
Additional file 1 of Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses Nobu, Masaru K.; Narihiro, Takashi; Mei, Ran https://doi.org/10.6084/m9.figshare.12715358.v1 The current record is supplemented by this image	image	January 2020
Additional file 2 of Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses Nobu, Masaru K.; Narihiro, Takashi; Mei, Ran https://doi.org/10.6084/m9.figshare.12715361 The current record is supplemented by this image	image	January 2020
Additional file 2 of Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses Nobu, Masaru K.; Narihiro, Takashi; Mei, Ran https://doi.org/10.6084/m9.figshare.12715361.v1 The current record is supplemented by this image	image	January 2020
Additional file 3 of Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses Nobu, Masaru K.; Narihiro, Takashi; Mei, Ran https://doi.org/10.6084/m9.figshare.12715364 The current record is supplemented by this image	image	January 2020
Additional file 3 of Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses Nobu, Masaru K.; Narihiro, Takashi; Mei, Ran https://doi.org/10.6084/m9.figshare.12715364.v1 The current record is supplemented by this image	image	January 2020
Additional file 4 of Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses Nobu, Masaru K.; Narihiro, Takashi; Mei, Ran https://doi.org/10.6084/m9.figshare.12715367 The current record is supplemented by this image	image	January 2020
Additional file 4 of Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses Nobu, Masaru K.; Narihiro, Takashi; Mei, Ran https://doi.org/10.6084/m9.figshare.12715367.v1 The current record is supplemented by this image	image	January 2020
Additional file 5 of Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses Nobu, Masaru K.; Narihiro, Takashi; Mei, Ran https://doi.org/10.6084/m9.figshare.12715370 The current record is supplemented by this image	image	January 2020
Additional file 5 of Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses Nobu, Masaru K.; Narihiro, Takashi; Mei, Ran https://doi.org/10.6084/m9.figshare.12715370.v1 The current record is supplemented by this image	image	January 2020
Additional file 6 of Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses Nobu, Masaru K.; Narihiro, Takashi; Mei, Ran https://doi.org/10.6084/m9.figshare.12715376 The current record is supplemented by this dataset	dataset	January 2020
Additional file 6 of Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses Nobu, Masaru K.; Narihiro, Takashi; Mei, Ran https://doi.org/10.6084/m9.figshare.12715376.v1 The current record is supplemented by this dataset	dataset	January 2020
Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses Nobu, Masaru K.; Narihiro, Takashi; Mei, Ran https://doi.org/10.6084/m9.figshare.c.5073293 The current record is supplemented by this collection	collection	January 2020
Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses Nobu, Masaru K.; Narihiro, Takashi; Mei, Ran https://doi.org/10.6084/m9.figshare.c.5073293.v1 The current record is supplemented by this collection	collection	January 2020

Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses

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