A novel methoxydotrophic metabolism discovered in the hyperthermophilic archaeon Archaeoglobus fulgidus

Abstract

Methoxylated aromatic compounds (MACs) are important components of lignin found in significant amounts in the subsurface. Recently, the methanogenic archaeon Methermicoccus shengliensis was shown to be able to use a variety of MACs during methoxydotrophic growth. After a molecular survey, we found that the hyperthermophilic non-methanogenic archaeon Archaeoglobus fulgidus also encodes genes for a bacterial-like demethoxylation system. In this study, we performed growth and metabolite analysis, and used transcriptomics to investigate the response of A. fulgidus during growth on MACs in comparison to growth on lactate. We observed that A. fulgidus converts MACs to their hydroxylated derivatives with CO 2 as the main product and sulfate as electron acceptor. Furthermore, we could show that MACs improve the growth of A. fulgidus in the presence of organic substrates such as lactate. We also found evidence that other archaea such as Bathyarchaeota, Lokiarchaeota, Verstraetearchaeota, Korarchaeota, Helarchaeota and Nezhaarchaeota encode a demethoxylation system. In summary, we here describe the first non-methanogenic archaeon with the ability to grow on MACs indicating that methoxydotrophic archaea might play a so far underestimated role in the global carbon cycle.

Cultivation of widespreadBathyarchaeiareveals a novel methyltransferase system utilizing lignin-derived aromatics

“…We attempted to verify that the mode of lignin metabolism of strain DL1YTT001 is similar to that described for acetogenic Bacteria with the capability of O-demethylation from lignin-derived methoxylated aromatic compounds (ArOCH 3 ) instead of polymer depolymerization 26 . Known Bacterial-type methyltransferase systems previously identified both in Archaea and Bacteria 16, 17 were searched but were also absent in the DL1YTT001 MAG. We speculated that this strain might contain a novel transmethylation system different from those known Bacterial-type systems.…”

“…The operon encoding the gene cluster of O-demethylase/methyltransferase complexes. The O-demethylase/methyltransferase gene cluster (a) and the methyl-transfer pathway (b) of DL1YTT001 with guaiacol as the substrate; (c) shows the gene clusters encoding Acetobacterium dehalogenans vanillate O-demethylase system 14 , Methermicoccus shengliensis methoxybenzoate O-demethylase system 16 , and Archaeoglobus fulgidus 2-methoxyphenol O-demethylase system 17 . Co(I) and Co(III), corrinoid protein with cobalt in their respective valence states; H 4 MPT, tetrahydromethanopterin.…”

“…Anaerobic biodegradation of lignin in marine sediments, particularly in nearshore sediments, is likely a globally important microbial process and significant for the cycling of organic carbon. O-demethylation from lignin-derived methoxylated aromatic compounds (ArOCH 3 ) is an important step of lignin biodegradation likely performed by acetogenic Bacteria and several lineages of Archaea 17 . These microorganisms acquired and shared Bacterial-type methyltransferase systems by horizontal gene transfer 17 .…”

“…O-demethylation from lignin-derived methoxylated aromatic compounds (ArOCH 3 ) is an important step of lignin biodegradation likely performed by acetogenic Bacteria and several lineages of Archaea 17 . These microorganisms acquired and shared Bacterial-type methyltransferase systems by horizontal gene transfer 17 . Recently, one MAG of Bathyarchaeia has also been reported to carry a Bacterial-type methyltransferase system 17 .…”

“…Methyltransferases have been characterized in acetogenic Bacteria such as Moorella thermoacetica 13 , Acetobacterium dehalogenans 14 , Sporomusa termitida 15 , and Acetobacterium woodii 12 . In recent years, these Bacterial-type methyltransferase systems were also detected in Archaea, including an acetogenic archaeon Archaeoglobus fulgidus and a methanogenic archaeon Methermicoccus shengliensis 16,17 . Similar genes were also found in the genomes of some uncultured Archaea such as Bathyarchaeia, Lokiarchaeia, Methanomethylicia, Korarchaeia, Helarchaeota and Nezhaarchaeales 17 .…”