Diel cycles in the twilight ocean: novel interactions between mesopelagic fishes and heterotrophic prokaryotes

We might not expect strong diel patterns in the biogeochemistry of the twilight zone as opposed to the upper ocean, where processes closely follow the alternance between day and night. Here, we review our current knowledge about the interactions between the diel vertical migration of mesopelagic fishes and heterotrophic prokaryotes (bacteria and archaea) in the deep scattering layer (DSL) of the Red Sea. The DSL, located at ca. 550 m, is occupied by lanternfishes (mostly Benthosema pterotum) during daytime hours. High frequency monitoring of dissolved organic matter (DOM) and prokaryotic standing stocks and cellular properties were complemented by predator-free incubations of seawater, which was sampled at midnight and at noon. Our findings suggest that, similarly to epipelagic waters, there is a diel supply of fresh and labile DOM in the DSL. Large prokaryotic cells were able to grow for a longer period when mesopelagic fishes were present. Specific growth rates could even be higher in the DSL than at the surface, and they were almost double during daytime, indicating higher amounts of bioavailable DOM likely due to fish activity. Heterotrophic bacteria and archaea in the DSL were also more efficient at converting DOM into new living biomass. A detailed latitudinal study of 16S rRNA-based prokaryotic community composition along the Red Sea demonstrated the existence of seasonality at the DSL. 41% of prokaryotic diversity in the mesopelagic was associated to the diel vertical migration of fishes, with 22% of all species found exclusive to the DSL. These results suggest that the ocean’s twilight zone receives a continuous diurnal supply of labile DOM from migrating fishes, enabling an unexpectedly active and unique community of heterotrophic prokaryotes.