Unique H2-utilizing lithotrophy in serpentinite-hosted systems

• Published in: The ISME Journal 2023-01, Vol.17 (1), p.95-104
• Main Authors: Nobu, Masaru Konishi, Nakai, Ryosuke, Tamazawa, Satoshi, Mori, Hiroshi, Toyoda, Atsushi, Ijiri, Akira, Suzuki, Shino, Kurokawa, Ken, Kamagata, Yoichi, Tamaki, Hideyuki
• Format: Article
• Language: English
• Subjects: 45/23; 631/326/171; 704/158/855; Autotrophic microorganisms; Autotrophy; Biomedical and Life Sciences; Carbon compounds; Carbon dioxide; Ecological adaptation; Ecology; Evolutionary Biology; Glycine; Glycine reductase; Homoacetogenesis; Life Sciences; Metabolism; Metagenomics; Microbial Ecology; Microbial Genetics and Genomics; Microbiology; Microbiomes; Microorganisms; Reductases; Ultramafic materials
• ISSN: 1751-7362; 1751-7370
• DOI: 10.1038/s41396-022-01197-9

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 -/CO 2 -dependent homoacetogenesis is thermodynamically unfavorable in situ due to picomolar CO 2 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 CO 2 , 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, CO 2 -poor conditions. Unique non-CO 2 -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.