Direct utilization of polysaccharides for methane production by a single deep-sea methanogen

Methanogenesis has traditionally been associated with a limited range of low-molecular-weight (LMW) substrates (MW < 1,000 Da), including CO ₂ , acetate, methylated compounds (e.g., methanol, methylamines), methoxylated aromatic compounds, and alkanes. However, the direct utilization of high-molecular-weight (HMW) organic matter (MW > 1,000 Da), such as polysaccharides, for methane production by methanogens has not been reported. Here, we show that a novel deep-sea methanogenic archaeon, strain ZRKC1, can directly utilize polysaccharides, particularly methyl-esterified forms (e.g., pectin), for methane production. This discovery expands the known substrate range for methanogenesis and unveils a new metabolic pathway distinct from previously characterized mechanisms. Furthermore, strain ZRKC1 uniquely couples polysaccharide utilization with inorganic polyphosphate (polyP) metabolism, accumulating polyP from organic phosphates released during polysaccharide hydrolysis. Importantly, we demonstrate that polyP formation is essential for both growth and methanogenesis in strain ZRKC1, revealing a previously unrecognized metabolic dependency and suggesting that polyP regulates carbon flux in methanogens. This is the first report of polysaccharide- and polyP-dependent growth in methanogens, presenting a novel metabolic strategy for energy conservation and adaptation to nutrient-limited environments and underscoring the ecological significance of methanogens in global carbon and phosphorus cycles.