Reviews and syntheses: Bacterial bioluminescence – ecology and impact in the biological carbon pump

Abstract

Abstract. Around thirty species of marine bacteria can emit light, a critical characteristic in the oceanic environment where the major part is deprived of sunlight. In this article, we first review current knowledge on bioluminescent bacteria symbiosis in light organs. Then, focusing on gut-associated bacteria, we highlight that recent works, based on omics methods, confirm previous claims about the prominence of bioluminescent bacterial species in fish guts. Such host-symbiont relationships are relatively well established and represent important knowledge in the bioluminescence field. However, the consequences of bioluminescent bacteria continuously released from light organ and through the digestive tracts to the seawater have been barely taken into account at the ecological and biogeochemical level. For too long neglected, we propose to consider the role of bioluminescent bacteria, and to reconsider the biological carbon pump taking into account the bioluminescence effect (bioluminescence shunt hypothesis). Indeed, it has been shown that marine snow and fecal pellets are often luminous due to microbial colonization, which makes them a visual target. These luminous particles seem preferentially consumed by organisms of higher trophic levels in comparison to non-luminous ones. As a consequence, the sinking rate of consumed particles could be either increased (due to repackaging) or reduced (due to sloppy feeding or coprophagy/coprorhexy) which can imply a major impact on global biological carbon fluxes. Finally, we propose a strategy, at a worldwide scale, relying on recently developed instrumentation and methodological tools to quantify the impact of bioluminescent bacteria in the biological carbon pump.

Fear and loathing in the pelagic: How the seascape of fear impacts the biological carbon pump

“…Considering the time scale on which carbon is sequestered when it reaches depths deeper than ~1000 m, a precise mechanistic description of deep‐water processes rather than a constant (or, in best cases, temperature dependent) bacterial degradation rate would increase the confidence in estimations of carbon sequestration in the ocean's interior. For example, including bioluminescence and its trade‐offs in mechanistic models may be of importance for the biological pump (Tanet et al 2020). Is there a simple way to account for a behavioral response?…”

“…These can result in bioluminescent particulate organic carbon release, and luminous bacteria growing on particulate matter may produce enough light to be visible by other organisms, resulting in a higher consumption of luminous particles. This process, termed the "bioluminescent shunt" was recently reviewed by Tanet et al (2020). Whether the extra consumption would come from lower trophic levels degrading the matter through sloppy feeding and coprorhexy (fragmentation of pellets) or higher trophic levels repackaging detritus, thus increasing their sinking speed and the pump efficiency, is unknown.…”

Acquisition of bioluminescent trait by non-luminous organisms from luminous organisms through various origins

“…Ingestion: in the second case, several marine organisms in the ocean obtain either luciferin [2,12] or both luciferin and luciferase [8] from their diet to produce light. Symbiosis: in the third case, ingestion of or colonization by luminous bacteria results in the host macro-organism acquiring bioluminescence [13][14][15][16][17][18][19].…”