The ecological success of freshwater microorganisms is mediated by streamlining and biotic interactions

Abstract

Genome size is known to reflect aspects of the eco-evolutionary history of prokaryotic species, including their lifestyle, environmental preferences, and habitat breadth. However, it remains uncertain how strongly genome size is linked to microbial prevalence, relative abundance and co-occurrence in the environment. To address this gap, we present a systematic and global-scale evaluation of the relationship between genome size, relative abundance and prevalence in freshwater ecosystems, including 80,561 medium-to-high quality genomes. We identified 9,028 species (defined by ANI >95%) across a manually curated dataset of 636 freshwater metagenomes and calculated their relative abundance. Our results show that prokaryotes with reduced genomes exhibited higher prevalence and relative abundance, and a greater prevalence than expected based on their mean abundance, suggesting that genome streamlining may promote cosmopolitanism. Furthermore, our network analysis revealed that prokaryotes with reduced genomes are found in co-occurrent groups comprising up to 295 species. The species in these groups potentially possess a diminished capacity for synthesizing essential metabolites such as vitamins, amino acids and nucleotides, which may foster complex metabolic interdependencies within the community. Moreover, the fitness advantage of losing biosynthetic functions appears to be frequency dependent: while nucleotide biosynthesis is the most retained biosynthetic function, amino acid and then vitamin biosynthesis are more frequently lost. Our study finds that genome size is linked to microbial community structure and ecological adaptation to freshwaters. Our results underscore genome streamlining as a central ecological and evolutionary strategy that both shapes and is shaped by community dynamics, ultimately fostering interdependences among prokaryotes.