A global genomic survey of prokaryotic carbon fixation reveals an oxygen-tolerant rTCA cycle in the surface ocean

A comprehensive survey of global prokaryotic carbon fixation has uncovered an oxygen-tolerant reductive TriCarboxylic Acid (rTCA) cycle in the surface ocean. Autotrophic carbon fixation, the conversion of inorganic carbon into biomass, is fundamental to life on Earth. Prokaryotes utilize at least seven distinct biochemical pathways for this process, yet the phylogenetic and environmental distribution of many of them remains unclear.

By screening approximately 40 billion genes across reference genomes, metagenome-assembled genomes (MAGs) and unbinned metagenomic contigs, researchers have conducted a global assessment of the phylogeny and ecophysiology of prokaryotic autotrophs. Most pathway marker genes were found in unbinned contigs and low-quality MAGs, indicating phylogenetically distinct lineages that are absent from isolate genomes and quality-filtered MAGs.

Established autotrophs comprised the majority of pathway detections in quality-filtered MAGs, largely aligning with known biology from cultivated model organisms. Interestingly, the rTCA cycle, previously believed to be restricted to anoxic environments, was discovered in three phylogenetically distinct Campylobacterota lineages dwelling in oxygenated surface seawater.

This suggests a novel and unforeseen habitat for this pathway. All three MAGs share a variant enzyme, previously observed in other oxygen-tolerant lineages, which likely enables their existence in the oxygenated surface ocean. Mapping reads across global ocean metagenomes suggests that these organisms may be more prevalent than the limited number of recovered MAGs alone would imply.

These findings reveal that our understanding of global autotrophic carbon fixation is largely influenced by the capabilities of genome-resolved methods, while the actual phylogenetic and ecological distribution of autotrophic carbon fixation appears to be considerably broader.