Abstract
Short-chain fatty acid (SCFA) degradation is an important process in methanogenic ecosystems, and is usually catalyzed by SCFA-oxidizing bacteria in syntrophy with methanogens. Current knowledge of this functional guild is mainly based on isolates or enrichment cultures, but these may not reflect the true diversity and in situ activities of the syntrophs predominating in full-scale systems. Here we obtained 182 medium to high quality metagenome-assembled genomes (MAGs) from the microbiome of two full-scale anaerobic digesters. The transcriptomic response of individual MAG was studied after stimulation with low concentrations of acetate, propionate, or butyrate, separately. The most pronounced response to butyrate was observed for two MAGs of the recently described genus Candidatus Phosphitivorax (phylum Desulfobacterota), expressing a butyrate beta-oxidation pathway. For propionate, the largest response was observed for an MAG of a novel genus in the family Pelotomaculaceae, transcribing a methylmalonyl-CoA pathway. All three species were common in anaerobic digesters at Danish wastewater treatment plants as shown by amplicon analysis, and this is the first time their syntrophic features involved in SCFA oxidation were revealed with transcriptomic evidence. Further, they also possessed unique genomic features undescribed in well-characterized syntrophs, including the metabolic pathways for phosphite oxidation, nitrite and sulfate reduction.
Highlights
Microbial syntrophy describes the obligatory mutualistic metabolism that occurs between two or more microorganisms, where the metabolic end-product of the primary metabolizer is immediately consumed as substrate by the others
Our current knowledge of syntrophic bacteria involved in Short-chain fatty acid (SCFA) oxidation is mostly based on studies performed on a few model organisms such as Syntrophomonas wolfei, Syntrophobacter fumaroxidans, and Pelotomaculum thermopropionicum incubated as mono- or defined co-cultures [2, 12] or in enrichments [13]
A comprehensive dataset from this study enabled the discovery of novel syntrophic bacterial species, and manually curated genome annotation revealed the energy conservation metabolisms related to SCFA oxidation in the three most responsive members
Summary
Microbial syntrophy describes the obligatory mutualistic metabolism that occurs between two or more microorganisms, where the metabolic end-product of the primary metabolizer is immediately consumed as substrate by the others. Our current knowledge of syntrophic bacteria involved in SCFA oxidation is mostly based on studies performed on a few model organisms such as Syntrophomonas wolfei, Syntrophobacter fumaroxidans, and Pelotomaculum thermopropionicum incubated as mono- or defined co-cultures [2, 12] or in enrichments [13]. The functional importance of specific microbial taxa in complex communities can be characterized using a genomeguided metatranscriptomic approach This has previously been applied to identify taxa involved in the anaerobic degradation of cellulosic biomass [19] and oleate [20] using lab-scale enrichments. A comprehensive dataset from this study enabled the discovery of novel syntrophic bacterial species, and manually curated genome annotation revealed the energy conservation metabolisms related to SCFA oxidation in the three most responsive members
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