The Origins of Marine Bioluminescence: Turning Oxygen Defence Mechanisms Into Deep-Sea Communication Tools

Abstract

Bioluminescence, the emission of ecologically functional light by living organisms, emerged independently on several occasions, yet the evolutionary origins of most bioluminescent systems remain obscure. We propose that the luminescent substrates of the luminous reactions (luciferins) are the evolutionary core of most systems, while luciferases, the enzymes catalysing the photogenic oxidation of the luciferin, serve to optimise the expression of the endogenous chemiluminescent properties of the luciferin. Coelenterazine, a luciferin occurring in many marine bioluminescent groups, has strong antioxidative properties as it is highly reactive with reactive oxygen species such as the superoxide anion or peroxides. We suggest that the primary function of coelenterazine was originally the detoxification of the deleterious oxygen derivatives. The functional shift from its antioxidative to its light-emitting function might have occurred when the strength of selection for antioxidative defence mechanisms decreased. This might have been made possible when marine organisms began colonising deeper layers of the oceans, where exposure to oxidative stress is considerably reduced because of reduced light irradiance and lower oxygen levels. A reduction in metabolic activity with increasing depth would also have decreased the endogenous production of reactive oxygen species. Therefore, in these organisms, mechanisms for harnessing the chemiluminescence of coelenterazine in specialised organs could have developed, while the beneficial antioxidative properties were maintained in other tissues. The full range of graded irradiance in the mesopelagic zone, where the majority of organisms are bioluminescent, would have provided a continuum for the selection and improvement of proto-bioluminescence. Although the requirement for oxygen or reactive oxygen species observed in bioluminescent systems reflects the high energy required to produce visible light, it may suggest that oxygen-detoxifying mechanisms provided excellent foundations for the emergence of many bioluminescent systems.

Toxicity and Antioxidant Activity of Fullerenol C60,70 with Low Number of Oxygen Substituents

“…Hence, the decrease in ROS content at high fullerene concentrations can account for the inhibition of the bioluminescent reaction (reaction 2, Section 3.2). It was discussed earlier [65] that the oxygen-detoxifying function promoted the evolutionary emergence of a series of bioluminescence systems, including the bioluminescence systems of marine bacteria. The bacterial bioluminescence reaction (reaction 2, Section 3.2) is applied as a model of enzymatic oxygen-dependent reactions taking place in all living organisms.…”

Luciferins Under Construction: A Review of Known Biosynthetic Pathways

“…What selective pressures might have driven the emergence of luciferin biosynthetic pathways, and were the luciferins and their biosynthetic precursors of use in ancestral organisms? One hypothesis suggests that luciferins evolved from detoxification systems as some substrates show characteristics of strong antioxidants (Rees et al, 1998;Timmins et al, 2001;Dubuisson et al, 2004). Derived from tyrosine and cysteine, biosynthetic pathways of D-luciferin and Odontosyllis luciferin might have arisen from a mutation-induced deviation of the melanogenic pathways to provide photoprotection against free radical species, particularly reactive oxygen species (Napolitano et al, 2013).…”

Leaving the Dark Side? Insights Into the Evolution of Luciferases

“…As stated by Valiadi and Iglesias-Rodriguez (2013), the hypothesis of Wilson and Hastings is mainly based on the bioluminescence systems of bacteria and fireflies, but it is largely plausible for other bioluminescent organisms. In cell cultures, coelenterazine (i.e., the most common luciferin in the marine environment) has been shown to reduce the death of fibroblasts exposed to oxidative stress (Rees et al, 1998). Coelenterazine is detected not only in luminescent organs but is also found in the digestive tract and hepatopancreas of several luminous and non-luminous decapods, cephalopods and fishes (Shimomura, 1987;Mallefet and Shimomura, 1995;Thomson et al, 1997;Rees et al, 1998;Duchatelet et al, 2019).…”

“…In cell cultures, coelenterazine (i.e., the most common luciferin in the marine environment) has been shown to reduce the death of fibroblasts exposed to oxidative stress (Rees et al, 1998). Coelenterazine is detected not only in luminescent organs but is also found in the digestive tract and hepatopancreas of several luminous and non-luminous decapods, cephalopods and fishes (Shimomura, 1987;Mallefet and Shimomura, 1995;Thomson et al, 1997;Rees et al, 1998;Duchatelet et al, 2019). These observations support an anti-oxidative function of this kind of compound and luciferins might then be antioxidant molecules emitting light as a by-product of their "reactive oxygen scavenging chemical activity" (Rees et al, 1998;Haddock et al, 2010).…”

“…Coelenterazine is detected not only in luminescent organs but is also found in the digestive tract and hepatopancreas of several luminous and non-luminous decapods, cephalopods and fishes (Shimomura, 1987;Mallefet and Shimomura, 1995;Thomson et al, 1997;Rees et al, 1998;Duchatelet et al, 2019). These observations support an anti-oxidative function of this kind of compound and luciferins might then be antioxidant molecules emitting light as a by-product of their "reactive oxygen scavenging chemical activity" (Rees et al, 1998;Haddock et al, 2010). The presence of common light-emitting luciferins in luminous but also is non-luminous organisms (i.e., ecological notion of luciferin reservoir) led to the hypothesis of the "luciferin dietary acquisition" (Haddock et al, 2010;Shimomura, 2012): luminous organisms acquired their luciferin through their food, and those molecules can transit via the food chain (i.e., a predator can retrieve the luciferin produced by its prey) (demonstrated in some species: Barnes et al, 1973;Warner and Case, 1980;Frank et al, 1984;Thomson et al, 1997;Haddock et al, 2001;Mallefet et al, 2020).…”