Metabolic preferences of marine copiotrophs are explained by the structure of central metabolism*

Bacterial communities in the ocean collectively drive biogeochemical cycles by digesting complex organic matter and recycling essential nutrients. To understand the taxonomic distribution and patterns of metabolic niches in these bacteria, we catalogued the metabolic capabilities of a library of 160 marine heterotrophic bacteria across 64 substrates. We found that the metabolic niches were oriented along a primary axis corresponding to the relative preference for sugars (i.e., glycolytic substrates) and organic and amino acids (i.e., gluconeogenic substrates). This preference was roughly conserved at the order level, but with marked differences between clades, down to the genus level. Comparative genomics revealed that a preference for glycolytic substrates was strongly correlated with the number of carbohydrate-degrading enzymes and negatively correlated with whole-genome GC content. By contrast, we identified only a small number of genes and no central metabolic pathways that were correlated with metabolic preference. This suggests that the fundamental metabolic preference for sugars or acids are encoded in the regulatory network rather than gene content, a hypothesis supported by recent theory suggesting intrinsic trade-offs in central metabolism at the root of these preferences.