Diel dynamics of dissolved organic matter and heterotrophic prokaryotes reveal enhanced growth at the ocean's mesopelagic fish layer during daytime

Contrary to epipelagic waters, where biogeochemical processes closely follow the light and dark periods, little is known about diel cycles in the oceans mesopelagic realm. Here, we monitored the dynamics of dissolved organic matter (DOM) and planktonic heterotrophic prokaryotes every 2 h for one day at 0 and 550 m (a depth occupied by vertically migrating fish during light hours) in oligotrophic waters of the central Red Sea. We additionally performed predator-free seawater incubations of samples collected from the same site both at midnight and at noon. Comparable in situ variability in microbial biomass and dissolved organic carbon concentration suggests a diel supply of fresh DOM in both layers. The presence of fish in the mesopelagic zone during daytime promoted a sustained, longer growth of larger prokaryotic cells. The specific growth rates were consistently higher in the noon experiments from both depths (surface: 0.34 vs. 0.18 d-1, mesopelagic: 0.16 vs. 0.09 d-1). Heterotrophic bacteria and archaea in the mesopelagic fish layer were also more efficient at converting DOM into new biomass. These results suggest that the oceans twilight zone receives a consistent diurnal supply of labile DOM from diel vertical migrating fishes, enabling an unexpectedly active community of heterotrophic prokaryotes.