Ubiquitous genome streamlined Acidobacteriota in freshwater environments

Abstract Background Acidobacteriota are abundant in soil, peatlands and sediments, but there are so far only a few studies on those in freshwater environments. Genome streamlined bacteria have reduced genomes as an evolutionary process to adapt to oligotrophic environments such as oceans and lakes. UBA12189, an Acidobacteriota genus under the family Holophagaceae, is an uncultivated lineage with ultra-small genome size found in aquatic environments. So far, no detailed genomic analyses were done on this genome streamlined lineage. Here, we analyzed 66 MAGs of UBA12189 (metagenome assembled genomes; including 2 complete genomes) from freshwater lakes and rivers in Europe, North America and Asia, which is the first genome streamlined Acidobacteriota reported. Results UBA12189 have extremely small genome sizes (< 1.4Mbp), low GC content and a highly diverse pangenome. In freshwater lakes, this bacterial lineage is abundant from the surface waters (epilimnion) down to 300 meters depth (hypolimnion). UBA12189 appears to be free-living from CARD-FISH analysis, and there is no concrete evidence of host association. Comparative genome analysis shows that compared to other genome streamlined bacteria such as Nanopelagicales and Methylopumilus, genome reduction has caused UBA12189 to have a more limited metabolic repertoire in carbon, sulfur and nitrogen metabolisms, as well as a higher degree of auxotrophy to various amino acids, vitamins and reduced sulfur. UBA12189 also have very limited numbers of membrane transporters. Interestingly, UBA12189 has a higher proportion of unannotated genes (10% – 14%) and a diverse pangenome, suggesting an unknown trove of metabolic potential for environmental adaptation. Despite having reduced genomes, UBA12189 encodes proteorhodopsin, cbb3-type cytochrome c oxidases and complete biosynthesis pathways for heme, vitamin K2 and vitamin B2 (riboflavin). These genes may give a selective advantage during the genome streamlining process. We propose a new genus ‘Ca. Acidiparvus’ within the family Holophagaceae, with two new species named ‘A. lacustris’ and ‘A. fluvialis’. Acidiparvus is the first described genome streamlined lineage under the phylum Acidobacteriota, which is a free-living, slow-growing scavenger in freshwater environments. Conclusion This study explores the ecology and genomics of yet another genome streamlined freshwater bacterium. With limited metabolic repertoires and no co-occurring microorganisms observed, future studies on cultivated Acidiparvus are crucial. Metagenomics studies alone cannot identify non-canonical metabolic pathways, especially considering high numbers of unannotated genes in Acidiparvus.