Shino Suzuki

Abstract Ribosomes are essential for protein synthesis and require ribosome biogenesis factors (RBFs) for assembly. To uncover the evolutionary diversity of ribosome biogenesis, we analyzed over 30,000 bacterial genomes and revealed that Candidate Phyla Radiation (CPR), also known as the phylum Patescibacteria, characterized by reduced genomes and smaller ribosomes, has about half the average number of RBFs compared with non-CPR bacteria. Notably, key RBFs such as der, obgE, and rbfA, considered indispensable, are conserved in only around 20%–70% of CPR genomes. Since such repertoires were not observed in reduced genomes of other phyla, CPR presumably diverged early in bacterial evolution. We further confirmed that ribosomal structural changes correlate with reduced RBFs, evidencing co-evolution between RBFs and the ribosome. These findings suggest that ribosomal biogenesis is more flexible than recognized, and the small cell and genome sizes of CPR bacteria and their early divergence may influence the unusual repertoires of RBFs. Teaser Ribosome biogenesis in CPR bacteria was unexpectedly flexible, challenging traditional views of this essential process in evolution.

Serpentinization, a geochemical process found on modern and ancient Earth, provides an ultra-reducing environment that can support microbial methanogenesis and acetogenesis. Several groups of archaea, such as the order Methanocellales, are characterized by their ability to produce methane. Here, we generate metagenomic sequences from serpentinized springs in The Cedars, California, and construct a circularized metagenome-assembled genome of a Methanocellales archaeon, termed Met12, that lacks essential methanogenesis genes. The genome includes genes for an acetyl-CoA pathway, but lacks genes encoding methanogenesis enzymes such as methyl-coenzyme M reductase, heterodisulfide reductases and hydrogenases. In situ transcriptomic analyses reveal high expression of a multi-heme c-type cytochrome, and heterologous expression of this protein in a model bacterium demonstrates that it is capable of accepting electrons. Our results suggest that Met12, within the order Methanocellales, is not a methanogen but a CO2-reducing, electron-fueled acetogen without electron bifurcation.

Abstract Serpentinization of ultramafic rocks provides molecular hydrogen (H₂) 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 H₂-/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 H₂-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 H₂ 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.

Abstract Poly(3-hydroxybutyrate-co-3-hydroxyvalerate) (PHBV) and poly(butylene succinate-co-adipate) (PBSA) are typical biodegradable polyesters; however, their biodegradability in the ocean differs substantially. Herein, we focused on functional genes correlated with biodegradation in ocean environments using multi-meta-omics approaches to identify the microbial groups and esterase enzymes correlated with biodegradation. Within the PHBV plastispheres, five Gammaproteobacteria were abundant, several of which encoded over 10 different types of extracellular poly(3-hydroxybutyrate (PHB) depolymerases that are highly expressed in the ocean. Within PBSA plastispheres, ecosystems of microbes formed on plastics, only two species of Gammaproteobacteria genomes were highly abundant and expressed: one for hydrolyzing PBSA and the other for consuming cleaved monomers. The high diversity of degrading microorganisms and enzymes could be related to the stable biodegradability of PHBV, while the low biodiversity of PBSA-degraders and necessity of symbiotic relationships likely characterize the instability of the marine biodegradability of PBSA. These results provide fundamental knowledge for the development of biodegradable marine plastics.