Minimal and hybrid hydrogenases are active from archaea
Chris Greening, Princess R. Cabotaje, Luis E. Valentin-Alvarado, Pok Man Leung, Henrik Land, Thiago Rodrigues-Oliveira, Rafael I. Ponce-Toledo, Moritz Senger, Max A. Klamke, Michael Milton, Rachael Lappan, Susan Mullen, Jacob West-Roberts, Jie Mao, Jiangning Song, Marie C. Schoelmerich, Courtney W. Stairs, Christa Schleper, Rhys Grinter, Anja Spang, Jillian F. Banfield, Gustav Berggren
Abstract
Microbial hydrogen (H 2 ) cycling underpins the diversity and functionality of diverse anoxic ecosystems. Among the three evolutionarily distinct hydrogenase superfamilies responsible, [FeFe] hydrogenases were thought to be restricted to bacteria and eukaryotes. Here, we show that anaerobic archaea encode diverse, active, and ancient lineages of [FeFe] hydrogenases through combining analysis of existing and new genomes with extensive biochemical experiments. [FeFe] hydrogenases are encoded by genomes of nine archaeal phyla and expressed by H 2 -producing Asgard archaeon cultures. We report an ultraminimal hydrogenase in DPANN archaea that binds the catalytic H-cluster and produces H 2 . Moreover, we identify and characterize remarkable hybrid complexes formed through the fusion of [FeFe] and [NiFe] hydrogenases in ten other archaeal orders. Phylogenetic analysis and structural modeling suggest a deep evolutionary history of hybrid hydrogenases. These findings reveal new metabolic adaptations of archaea, streamlined H 2 catalysts for biotechnological development, and a surprisingly intertwined evolutionary history between the two major H 2 -metabolizing enzymes.