Summary
Propionate is an important intermediate in the anaerobic mineralization of organic matter. In methanogenic environments, its degradation relies on syntrophic associations between syntrophic propionate‐oxidizing bacteria (SPOB) and
Archaea
. However, only 10 isolated species have been identified as SPOB so far. We report syntrophic propionate oxidation in thermophilic enrichments of
Candidatus
Syntrophosphaera thermopropionivorans, a novel representative of the candidate phylum
Cloacimonetes
. In enrichment culture, methane was produced from propionate, while
Ca
. S. thermopropionivorans contributed 63% to total bacterial cells. The draft genome of
Ca
. S. thermopropionivorans encodes genes for propionate oxidation via methymalonyl‐CoA. Phylogenetically,
Ca
. S. thermopropionivorans affiliates with the uncultured
Cloacimonadaceae
W5 and is more distantly related (86.4% 16S rRNA gene identity) to
Ca
. Cloacimonas acidaminovorans. Although
Ca
. S. thermopropionivorans was enriched from a thermophilic biogas reactor,
Ca
. Syntrophosphaera was in particular associated with mesophilic anaerobic digestion systems. 16S rRNA gene amplicon sequencng and a novel genus‐specific quantitative PCR assay consistently identified
Ca
. Syntrophosphaera/
Cloacimonadaceae
W5 in 9 of 12 tested full‐scale biogas reactors thereby outnumbering other SPOB such as
Pelotomaculum
,
Smithella
and
Syntrophobacter
. Taken together the ubiquity and abundance of
Ca
. Syntrophosphaera, those SPOB might be key players for syntrophic propionate metabolism that have been overlooked before.