Cross-feeding options define eco-evolutionary dynamics of deep oligotrophic groundwater microbiome

Deep groundwaters populated by diverse and active microbes are among the most energy and nutrient-limited ecosystems. Characteristics of this ecosystem including nutrient and dispersal limitations, low cell densities, and episodic growth strategy interactively underpin the so far elusive eco-evolutionary dynamics of its microbiome. Here we applied a modular metabolic analyses on genome-resolved reconstructed community of disconnected deep groundwaters in the Fennoscandian Shield. In the community of deeper groundwaters despite their highly oligotrophic nature, lineages with larger genomes maintained larger populations which we hypothesize to be connected with their limited cross-feeding options. Thus providing an extension on the streamlining theory emphasizing the importance of ecological interactions in genome evolution which is further supported by the observed decrease in abundance of lineages with known metabolic dependencies, such as Patescibacteria and DPANN, with depth. The modular metabolic analyses showed that remarkably common niches based on same cross-feeding interactions are also available in different groundwaters, in addition to common niches for primary production. While these shared niches are critical for community assembly in this ecosystem, in different boreholes different lineages populated them. Our results provided new insights into the role of metabolic cross-feeding in genome evolution and community assembly of deep groundwater microbiome.