Unique H2-utilizing lithotrophy in serpentinite-hosted systems

Serpentinization of ultramafic rocks provides molecular hydrogen (H-2) that can support lithotrophic metabolism of microorganisms, but also poses extremely challenging conditions, including hyperalkalinity and limited electron acceptor availability. Investigation of two serpentinization-active systems reveals that conventional H-2-/CO2-dependent homoacetogenesis is thermodynamically unfavorable in situ due to picomolar CO2 levels. Through metagenomics and thermodynamics, we discover unique taxa capable of metabolism adapted to the habitat. This included a novel deep-branching phylum, Ca. Lithacetigenota, that exclusively inhabits serpentinite-hosted systems and harbors genes encoding alternative modes of H-2-utilizing lithotrophy. Rather than CO2, these putative metabolisms utilize reduced carbon compounds detected in situ presumably serpentinization-derived: formate and glycine. The former employs a partial homoacetogenesis pathway and the latter a distinct pathway mediated by a rare selenoprotein-the glycine reductase. A survey of microbiomes shows that glycine reductases are diverse and nearly ubiquitous in serpentinite-hosted environments. Ca. Lithacetigenota glycine reductases represent a basal lineage, suggesting that catabolic glycine reduction is an ancient bacterial innovation by Terrabacteria for gaining energy from geogenic H-2 even under hyperalkaline, CO2-poor conditions. Unique non-CO2-reducing metabolisms presented here shed light on potential strategies that extremophiles may employ for overcoming a crucial obstacle in serpentinization-associated environments, features potentially relevant to primordial lithotrophy in early Earth.

Automated summary

The serpentinization of ultramafic rocks can provide molecular hydrogen (H-2) for microorganisms, but the conditions in these environments are extremely challenging. Through metagenomics and thermodynamics, researchers have discovered unique microbial taxa in serpentinization-active systems that are adapted to these conditions. These microorganisms utilize alternative modes of H-2-utilizing lithotrophy, specifically using reduced carbon compounds rather than CO2. This research sheds light on potential strategies that extremophiles may employ in serpentinization-associated environments, which could also be relevant to primordial lithotrophy on early Earth.