Direct utilization of long-chain fatty acid for methane production by thermophilic Archaeoglobi

The methanogenic degradation of long-chain fatty acids has traditionally been considered to occur through syntrophic partnerships between long-chain fatty acid degrading bacteria and methanogenic archaea. However, recent genomic evidence suggests that certain archaea may independently perform entire process. Here, we report the cultivation of an archaeon from the class Archaeoglobi, Candidatus (Ca.) Methanoglobus sphaerolipidus DLY3, from hot spring sediments in Tengchong, China. Using an integrated approach including targeted cultivation, growth experiments, microscopy, stable isotope tracing, metagenomics, and metatranscriptomics, we demonstrate that Ca. M. sphaerolipidus directly converts long-chain fatty acids to methane. This transformation involves the beta-oxidation pathway, the Wood-Ljungdahl pathway (WLP), and methanogenic methyl-coenzyme M reductase (MCR) and methyltransferases (MTR) complexes—a process we term liparotrophy. In addition to oleic acid, Ca. M. sphaerolipidus is also capable of utilizing methanol as a substrate for methanogenesis. Our findings expand the known substrate range for methanogenic archaea beyond CO₂ reduction, acetoclastic methanogenesis, methylotrophy, methyl reduction, methoxydotrophy, and the recently reported alkylotrophy.