Diversity and ecological dynamics of bioluminescent bacteria in the mesopelagic zone

Mesopelagic ecosystems, located between 200 and 1000 meters deep are poorly studied. They are characterized by complete darkness, driving organisms to develop specialized adaptive strategies1. One of the most remarkable of these adaptations is bioluminescence, enabling organisms to produce light for communication, camouflage, prey attraction, or defence2. Mesopelagic fish, such as myctophids, dominate this zone in terms of biomass (65%) and diversity and are capable of emitting light3. They produce light either through endogenous photophores or via symbiosis with bioluminescent bacteria like Vibrionaceae. These microorganisms may also be found on their skin and in their gut or liver 2,4. These fishes perform diel vertical migrations (DVM): they ascend to feed near the surface at night and descend to deeper waters during the day to avoid predators3. By this process, they can transport organic matter and nutrients through the water column. Indeed, they are capable of releasing consumed organic matter in the form of fecal pellets that can be glowing (as they carry bioluminescent bacteria).  This feature might play a key role in structuring deep-sea trophic networks.This study aims to analyse prokaryotic composition across different tissues of several mesopelagic fish species and to identify correlations between the presence of bioluminescent bacteria, migratory capacity, and diet. A total of 160 samples from gut, liver, and skin were collected during the APERO cruise in July 2023 in the Northeast Atlantic. Microbial diversity was assessed via 16S metabarcoding, considering site, depth, and fish traits.The results reveal significant microbial variations across the three most-sampled fish families (n = 142): Myctophidae, Stomiidae, and Sternoptychidae. Bioinformatic analyses show two distinct clusters, with skin samples clearly separated from liver and gut. Bacterial composition varied by tissue, with Pseudoalteromonadaceae dominating the skin (25% of the community) and Vibrionaceae and Enterobacteriaceae prevalent in liver and gut (52% and 24%). Within Vibrionaceae, Photobacterium and Vibrio (including many bioluminescent species5) comprised about half of the gut bacterial community, indicating their abundance in this tissue. Correlations emerged between bacterial composition, diet, and migratory abilities in Myctophidae and Sternoptychidae. Migratory, zooplanktivorous, and bioluminescent fish had a microbial composition largely composed of Photobacterium and Vibrio (Vibrionaceae), in contrast to other fish. These findings highlight the importance of studying microbial diversity in mesopelagic fishes and provide a strong foundation for understanding interactions between fish microbiomes and deep-sea ecological processes.1 Robison, B. H. Conservation of deep pelagic biodiversity. Conservation Biology 23, n°4 (2009): 847-858. https://doi.org/10.1111/j.1523-1739.2009.01219.x2 Haddock, S.H.D., M. A. Moline, and J. F. Case. Bioluminescence in the Sea. Annual Review of Marine Science 2, no 1 (2010):443‑93. https://doi.org/10.1146/annurev-marine-120308-081028.3 Irigoien, X., T. A. Klevjer, A. Røstad, et al. Large Mesopelagic Fishes Biomass and Trophic Efficiency in the Open Ocean. Nature Communications 5, no 1 (2014):3271. https://doi.org/10.1038/ncomms4271.4 Widder, Edith. Bioluminescence and the Pelagic Visual Environment. Marine and Freshwater Behaviour and Physiology 35 (2002):1‑26. https://doi.org/10.1080/10236240290025581.5 Tanet, L., S. Martini, L. Casalot, and C. Tamburini. Reviews and Syntheses: Bacterial Bioluminescence – Ecology and Impact in the Biological Carbon Pump. Biogeosciences 17, no 14 (2020):3757‑78. https://doi.org/10.5194/bg-17-3757-2020.