An evolutionary perspective on metabolic tradeoffs in bacteria
Central carbon metabolism provides the energy to fuel bacterial growth and survival. Thus, modeling cellular energy generation is a crucial aspect to understanding microbial growth behavior. We used gap-filling independent core metabolic models for 8,178 publicly available genomes to examine the presence and absence of 12 key energy-related metabolic pathways (EMP glycolysis, ED glycolysis, gluconeogenesis, pentose phosphate, and fermentations to the end products: ethanol, lactate, formate, acetate, acetone, butyrate, butanol, and 2,3-butanediol). We examined pathway co-occurrence patterns and then using a phylogenetic tree and Fritz’s D, we asked whether any of these individual pathways, or frequently occurring combinations of these pathways, were conserved. Finally, using a new set of sequenced soil bacterial isolates, we asked whether these patterns held within a single ecosystem and what influence pathway presence had on growth across 72 C substrates.
Our results show that overall central carbon metabolism is a highly redundant network, but that EMP and ED forms of glycolysis are negatively correlated with each other suggesting a robust difference in selection between these two pathways. This difference in selection likely represents an efficiency tradeoff between EMP and ED glycolysis. All pathways individually, as well as common combinations of pathways, show limited conservation and follow a Brownian model of evolution. Different ecosystems had different pathway co-occurrence patterns, suggesting a strong role of environment in shifting these pathways across lineages. In the soil environment, core metabolic composition influenced growth ability and rate across 72 C substrates, explaining an equal but only partially overlapping portion of variation as phylogenetic history. These results are discussed in terms of understanding the role of unculturable bacteria in their environment.