Linking extracellular enzymes to phylogeny indicates a predominately particle-associated lifestyle of deep-sea prokaryotes

Heterotrophic prokaryotes express extracellular hydrolytic enzymes to cleave large organic molecules prior to uptake of the cleavage products. In the deep ocean, the average age of the dissolved organic carbon (DOC) is about 5000 years and therefore, deep-ocean DOC is considered recalcitrant to prokaryotic degradation. According to the foraging theory, extracellular enzymes should be cell-associated in diluted systems such as the deep ocean while in diffusion-limited systems extracellular enzymes should be freely dissolved. However, the extracellular enzymes in the deep ocean are found mainly dissolved in the water rather than cell-associated. Here we aim at resolving this enigma using a global survey of peptidases and the carbohydrate-active enzymes (CAZymes), two key enzyme groups initiating organic matter assimilation, in an integrated meta-genomics, -transcriptomics and -proteomics approach. The abundance, percentage and the diversity of genes encoding secretory enzymes consistently increased from epipelagic to bathypelagic waters as did the corresponding enzymes, indicating that prokaryotic metabolism is predominately particle-associated in the bathypelagic realm.