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

Abstract

Anaerobic lignin degradation is a major process in the global carbon cycle that would significantly influence estimates of carbon flux in both terrestrial and marine ecosystems. The ubiquitous Bathyarchaeia, one of the most abundant taxa in marine sediments, have been proposed to be key players in this process. However, the mechanism of Bathyarchaeial lignin degradation is unclear due to the lack of cultured strains. Here we report the cultivation of Candidatus Marisediminiarchaeum ligniniphilus DL1YTT001, a Bathyarchaeial representative from nearshore marine sediments that can grow with lignin as the sole organic carbon source under mesophilic and anaerobic conditions. Strain DL1YTT001 possesses and highly expresses a novel and specific methyltransferase system for O-demethylation of lignin-derived methoxylated aromatic compounds (ArOCH3). The key gene, methyltransferase 1 (MtgB), is not homologous to any other lineages. Enzymatic activity was confirmed through the heterologous expression of the MtgB gene, showing O-demethylation activity with guaiacol as the substrate. Considering that Bathyarchaeial lineages carrying this specific methyltransferase system are widely distributed in diverse anoxic environments, especially lignin-rich nearshore sediments, Bathyarchaeia-mediated O-demethylation is likely a key step in global anaerobic lignin remineralization.

Taxonomic and carbon metabolic diversification of Bathyarchaeia during its coevolution history with early Earth surface environment

“…This suggests that they could serve as a keystone species in the subseafloor microbial community by providing this essential cofactor for other members. In addition, some Baizosediminiarchaeum species could grow with lignin as the energy source by using a special O -demethylation methyltransferase (MT) system that require cobalamin-binding corrinoid protein ( 13 , 38 ), while the growth of certain Baizomonas species (assigned to subgroup 6) was substantially stimulated by different lignin-derived aldehydes with methoxy groups in enrichments ( 14 ). Overall, the cobalamin synthesis capability might be one of the key factors in explaining the ubiquitous distribution and predominance of genera Baizomonas and Baizosediminiarchaeum (previously subgroups 6/5bb and 8), even the whole class Bathyarchaeia, in global freshwater and marine sediments.…”

“…Moreover, our other work has also demonstrated that one Baizosediminiarchaeum species of the lignin-degrading clade used a special MT system to transfer the methyl groups from lignin-derived ArOCH 3 to H 4 MPT, which are either further oxidized to CO 2 or converted to acetate for energy production ( 38 ). This suggests that this Bathyarchaeia-specific MT system plays a key role in anaerobic lignin degradation, thus likely explaining their predominance in the lignin-enriched estuarine and nearshore sediments.…”

Taxonomic and carbon metabolic diversification of Bathyarchaeia during its co-evolution history with the early Earth surface environment

“…In comparison with Brockarchaeota ( 47 ), most of these Bathyarchaeia lineages possess an extra complete H 4 -MPT WLP and more methylamine-associated MT systems (Fig. 4), reflecting their more flexible methylotrophic strategy and substrate preference, the latter of which might facilitate their survival in the nutrient-limited deep subseafloor, as the amino residues released from methylamines are bioavailable nitrogen sources ( 53 ). Moreover, multiple methylated C1 compounds have been shown to be metabolized through methylotrophic methanogenesis and non-methanogenic methylotrophy in anoxic sulfate-reducing sediments ( 54 ), where Bathyarchaeia are also enriched ( 55 ).…”

Microbial community organization during anaerobic pulp and paper mill wastewater treatment

“…Members of this class have been associated with a variety of functions including methane metabolism, cellulose hydrolysis and fermentation, and reductive acetogenesis. [28][29][30][31] These non-methanogenic archaea have also been associated with lignin degradation 32,33 which would explain their high relative abundance in the mill digesters. Pulp mill wastewater contains high concentrations of lignin derived compounds as a result of the pulping process and the associated separation of lignin from wood.…”

“…Bathyarchaeia may produce hydrogen to be consumed by these methanogens, or they prefer similar conditions as these methanogens by utilizing hydrogen and/or methylated compounds. Yu et al 33 suggest Bathyarchaeia-mediated lignin demethylation as a key step in lignin degradation. have been associated with acetogenesis, [47][48][49] and Bacteroidetes_vadinHA17 has hydrolyzing capabilities.…”