Diverse electron carriers drive syntrophic interactions in an enriched anaerobic acetate-oxidizing consortium.
Journal
The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086
Informations de publication
Date de publication:
Dec 2023
Dec 2023
Historique:
received:
31
05
2023
accepted:
11
10
2023
revised:
09
10
2023
medline:
4
12
2023
pubmed:
26
10
2023
entrez:
25
10
2023
Statut:
ppublish
Résumé
In many anoxic environments, syntrophic acetate oxidation (SAO) is a key pathway mediating the conversion of acetate into methane through obligate cross-feeding interactions between SAO bacteria (SAOB) and methanogenic archaea. The SAO pathway is particularly important in engineered environments such as anaerobic digestion (AD) systems operating at thermophilic temperatures and/or with high ammonia. Despite the widespread importance of SAOB to the stability of the AD process, little is known about their in situ physiologies due to typically low biomass yields and resistance to isolation. Here, we performed a long-term (300-day) continuous enrichment of a thermophilic (55 °C) SAO community from a municipal AD system using acetate as the sole carbon source. Over 80% of the enriched bioreactor metagenome belonged to a three-member consortium, including an acetate-oxidizing bacterium affiliated with DTU068 encoding for carbon dioxide, hydrogen, and formate production, along with two methanogenic archaea affiliated with Methanothermobacter_A. Stable isotope probing was coupled with metaproteogenomics to quantify carbon flux into each community member during acetate conversion and inform metabolic reconstruction and genome-scale modeling. This effort revealed that the two Methanothermobacter_A species differed in their preferred electron donors, with one possessing the ability to grow on formate and the other only consuming hydrogen. A thermodynamic analysis suggested that the presence of the formate-consuming methanogen broadened the environmental conditions where ATP production from SAO was favorable. Collectively, these results highlight how flexibility in electron partitioning during SAO likely governs community structure and fitness through thermodynamic-driven mutualism, shedding valuable insights into the metabolic underpinnings of this key functional group within methanogenic ecosystems.
Identifiants
pubmed: 37880541
doi: 10.1038/s41396-023-01542-6
pii: 10.1038/s41396-023-01542-6
pmc: PMC10689502
doi:
Substances chimiques
Acetates
0
Hydrogen
7YNJ3PO35Z
Formates
0
Methane
OP0UW79H66
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2326-2339Subventions
Organisme : Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada (Conseil de Recherches en Sciences Naturelles et en Génie du Canada)
ID : RGPIN-2018-04585
Organisme : Genome British Columbia
ID : SIP06
Organisme : DOE | SC | Biological and Environmental Research (BER)
ID : DE-AC05-76RL01830
Informations de copyright
© 2023. The Author(s).
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