Metabolic dependency: A key to domesticate aquatic bacterioplankton

초록

Many prokaryotes in their natural environments exhibit metabolic dependence on other life forms’ metabolites, explaining why the majority of bacteria and archaea are unculturable. Here we present that the acI lineage, the predominant free-living bacterial group in freshwater environments, shows metabolic dependency on heme. Heme is an iron-based porphyrin ring and essential for respiration. Heme-auxotrophic microbes are known to be limited to pathogens, symbionts, or commensal microorganisms. Only recently two stable axenic strains in the acI lineage were obtained by supplying catalase as a critical growth supplement. However, further experimental observations and genomic studies suggested that detoxification of hydrogen peroxide might not be a key factor for the successful cultivation of the acI lineage. We found that two recently cultivated acI isolates require exogenous heme for growth. One of the cultured acI isolates also exhibited auxotrophy for riboflavin. Further, genomes of all acI strains isolated to date lacked essential enzymes necessary to synthesize heme, indicating that heme auxotrophy is a conserved trait in this lineage. Additionally, genome analyses using the Genome Taxonomy Database (GTDB) revealed that heme auxotrophy is unexpectedly widespread across abundant but not-yet-cultivated microbial groups, including Patescibacteria, Marinisomatota (SAR406), Actinomarinales (OM1), and Marine group IIb and III of Euryarchaeota. Our findings indicate that heme auxotrophy is a more common phenomenon than previously thought, and heme may be the focus of future research on the metabolic dependency.