Abstract

Abstract. Around 30 species of marine bacteria can emit light, a critical characteristic in the oceanic environment is mostly 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 organs 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 considering the role of bioluminescent bacteria and reconsidering 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 nonluminous 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.

Highlights

  • Darkness constitutes the main feature of the ocean

  • We propose considering the role of bioluminescent bacteria and reconsidering the biological carbon pump, taking into account the bioluminescence effect (“bioluminescence shunt hypothesis”)

  • Considering that fish and squid housing luminous bacteria are never found without symbionts in nature, the symbiosis appears obligatory for hosts (Haygood, 1993)

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Summary

Introduction

Darkness constitutes the main feature of the ocean. the dark ocean represents more than 94 % of the Earth’s habitable volume (Haddock et al, 2017). Endowed with important motility and chemotactic abilities, luminous bacteria are able to colonize a large variety of habitats (as symbionts with macroorganisms, free-living in seawater or attached to particles) (e.g., Dunlap and Kita-tsukamoto, 2006, and references therein) In their symbiotic forms, bioluminescent bacteria are mostly known to colonize light organs and guts, in which they find better growing conditions than in the open ocean. One of the consequences of these symbioses, in both light organs and guts, is a massive quantity of bioluminescent bacteria dispersed daily in the ocean Based on this statement, we claim and demonstrate that bioluminescent bacteria have an ecological and a biogeochemical importance in the biological carbon pump.

Symbiotic bioluminescent bacteria in light organs
Symbiont selection and colonization of the light organ
Light organs are under well-established controls
Enteric associations in marine-fish guts
Luminous bacteria and the biological carbon pump
Bioluminescent bacteria in the water column
Bioluminescent bacteria attached to particles
Bioluminescent bacteria in the sediments
How do bioluminescent bacteria impact the biological carbon pump?
Past and future instrumentation for bioluminescence assays
Assessment of the global importance of bioluminescence in the oceans
Findings
Conclusions

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