March 14, 2024
Journal Article

Diverse electron carriers drive syntrophic interactions in an enriched anaerobic acetate-oxidizing consortium

Abstract

In many anoxic environments, syntrophic acetate oxidation (SAO) is a key pathway mediating 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. Over 80% of the enriched bioreactor metagenome collectively belonged to a three-member consortium, including an acetate-oxidizing bacterium affiliated with DTU068 encoding for CO2, H2, 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.

Published: March 14, 2024

Citation

Mcdaniel E.A., M. Scarborough, D. Mulat, X. Lin, P. Sampara, H.M. Olson, and R.P. Young, et al. 2023. Diverse electron carriers drive syntrophic interactions in an enriched anaerobic acetate-oxidizing consortium. The ISME Journal 17, no. 12:2326–2339. PNNL-SA-186718. doi:10.1038/s41396-023-01542-6

Research topics