Widespread Bathyarchaeia encode a novel methyltransferase utilizing lignin-derived aromatics

Area of Science:

• Microbial Ecology
• Biogeochemistry
• Molecular Biology

Background:

• Lignin degradation is crucial for the global carbon cycle in terrestrial and marine environments.
• Bathyarchaeia are abundant marine microorganisms suspected to mediate anaerobic lignin breakdown.
• The precise mechanism of lignin degradation by Bathyarchaeia is not well understood.

Purpose of the Study:

• To investigate the mechanism of anaerobic lignin degradation by marine Bathyarchaeia.
• To identify and characterize the enzymes involved in lignin monomer O-demethylation.
• To determine the prevalence and activity of lignin-degrading Bathyarchaeia in coastal sediments.

Main Methods:

• Enrichment culture of Bathyarchaeia from coastal sediments.
• Growth experiments using lignin as the sole carbon source under anoxic conditions.
• Gene expression analysis and heterologous expression of a novel methyltransferase (MT1).
• Metagenomic analysis of environmental DNA from various coastal sediments.

Main Results:

• An enrichment culture, *Candidatus* Baizosediminiarchaeum ligniniphilus (Ca. B. ligniniphilus), was established, utilizing lignin as its sole carbon source.
• Ca. B. ligniniphilus highly expresses a novel methyltransferase (MT1, mtgB) responsible for O-demethylation of lignin monomers.
• MT1 enzymes are unique to Bathyarchaeia and confirmed to possess O-demethylation activity.
• The *mtgB* gene is widespread in coastal sediments and highly expressed in the East China Sea sediments.

Conclusions:

• Bathyarchaeia possess and utilize novel methyltransferases (MT1) for O-demethylation of lignin monomers.
• These findings reveal a key mechanism for anaerobic lignin degradation mediated by Bathyarchaeia.
• Bathyarchaeia are ubiquitous and active lignin degraders in coastal marine ecosystems, contributing significantly to the carbon cycle.