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

Tanet, Lisa; Martini, Séverine; Casalot, Laurie; Tamburini, Christian

doi:10.5194/bg-17-3757-2020

Cited by 16 publications

(15 citation statements)

References 177 publications

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“…Bacteria Luciferases (Group I), the Most Ancient Type of Bioluminescent Proteins Shared by all Luminous Bacteria Bioluminescent bacteria (i.e., terrestrial or aquatic) are all distributed into seven genera belonging to three families of Gammaproteobacteria: Vibrionaceae, Shewanellaceae and Enterobacteriaceae (Brodl et al, 2018), and at least 28 luminous marine bacteria have been described (e.g., Vibrio harveyi, Photobacterium sp.) (Tanet et al, 2020). Symbiotic associations with luminescent bacteria have also been described in teleost fish and squids (Dunlap and Kita-Tsukamoto, 2006) and suggested as hypotheses, in other organisms (e.g., Mackie and Bone, 1978;Taylor et al, 1983).…”

Section: Diversity and Similarity Among Known Bioluminescent Proteinsmentioning

confidence: 95%

Leaving the Dark Side? Insights Into the Evolution of Luciferases

et al. 2021

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Bioluminescence—i.e., the emission of visible light by living organisms—is defined as a biochemical reaction involving, at least, a luciferin substrate, an oxygen derivative, and a specialised luciferase enzyme. In some cases, the enzyme and the substrate are durably associated and form a photoprotein. While this terminology is educatively useful to explain bioluminescence, it gives a false idea that all luminous organisms are using identical or homologous molecular tools to achieve light emission. As usually observed in biology, reality is more complex. To date, at least 11 different luciferins have indeed been discovered, and several non-homologous luciferases lato sensu have been identified which, all together, confirms that bioluminescence emerged independently multiple times during the evolution of living organisms. While some phylogenetically related organisms may use non-homologous luciferases (e.g., at least four convergent luciferases are found in Pancrustacea), it has also been observed that phylogenetically distant organisms may use homologous luciferases (e.g., parallel evolution observed in some cnidarians, tunicates and echinoderms that are sharing a homologous luciferase-based system). The evolution of luciferases then appears puzzling. The present review takes stock of the diversity of known “bioluminescent proteins,” their evolution and potential evolutionary origins. A total of 134 luciferase and photoprotein sequences have been investigated (from 75 species and 11 phyla), and our analyses identified 12 distinct types—defined as a group of homologous bioluminescent proteins. The literature review indicated that genes coding for luciferases and photoproteins have potentially emerged as new genes or have been co-opted from ancestral non-luciferase/photoprotein genes. In this latter case, the homologous gene’s co-options may occur independently in phylogenetically distant organisms.

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Section: Diversity and Similarity Among Known Bioluminescent Proteinsmentioning

confidence: 95%

Leaving the Dark Side? Insights Into the Evolution of Luciferases

et al. 2021

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“…For example, bioluminescent organisms and their predators are hypothesized to play a major role in the biological carbon pump, through preferential consumption of luminous particles by high-level consumers. This can affect the sinking rates of the former, their remineralization and their availability in the deeper waters (Tanet et al, 2020) or lead to higher success rates of visual predation for macro-organisms (Vacquié-Garcia et al, 2012).…”

Section: Capturing the Rhythmic Movements Of The Deep Scattering Layermentioning

confidence: 99%

Integrating Diel Vertical Migrations of Bioluminescent Deep Scattering Layers Into Monitoring Programs

et al. 2021

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The deep sea (i.e., >200 m depth) is a highly dynamic environment where benthic ecosystems are functionally and ecologically connected with the overlying water column and the surface. In the aphotic deep sea, organisms rely on external signals to synchronize their biological clocks. Apart from responding to cyclic hydrodynamic patterns and periodic fluctuations of variables such as temperature, salinity, phytopigments, and oxygen concentration, the arrival of migrators at depth on a 24-h basis (described as Diel Vertical Migrations; DVMs), and from well-lit surface and shallower waters, could represent a major response to a solar-based synchronization between the photic and aphotic realms. In addition to triggering the rhythmic behavioral responses of benthic species, DVMs supply food to deep seafloor communities through the active downward transport of carbon and nutrients. Bioluminescent species of the migrating deep scattering layers play a not yet quantified (but likely important) role in the benthopelagic coupling, raising the need to integrate the efficient detection and quantification of bioluminescence into large-scale monitoring programs. Here, we provide evidence in support of the benefits for quantifying and continuously monitoring bioluminescence in the deep sea. In particular, we recommend the integration of bioluminescence studies into long-term monitoring programs facilitated by deep-sea neutrino telescopes, which offer photon counting capability. Their Photo-Multiplier Tubes and other advanced optical sensors installed in neutrino telescope infrastructures can boost the study of bioluminescent DVMs in concert with acoustic backscatter and video imagery from ultra-low-light cameras. Such integration will enhance our ability to monitor proxies for the mass and energy transfer from the upper ocean into the deep-sea Benthic Boundary Layer (BBL), a key feature of the ocean biological pump and crucial for monitoring the effects of climate-change. In addition, it will allow for investigating the role of deep scattering DVMs in the behavioral responses, abundance and structure of deep-sea benthic communities. The proposed approach may represent a new frontier for the study and discovery of new, taxon-specific bioluminescence capabilities. It will thus help to expand our knowledge of poorly described deep-sea biodiversity inventories and further elucidate the connectivity between pelagic and benthic compartments in the deep-sea.

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“…Bacteria luciferases (Group I), the most ancient type of bioluminescent proteins shared by all luminous bacteria Bioluminescent bacteria (i.e., terrestrial or aquatic) are all distributed into seven genera belonging to three families of Gammaproteobacteria: Vibrionaceae, Shewanellaceae and Enterobacteriaceae (Brodl et al, 2018), and at least 28 luminous marine bacteria have been described (e.g., Vibrio harveyi, Photobacterium sp) (Tanet et al 2020). Symbiotic associations with luminescent bacteria have also been described in teleost fish and squids (Dunlap and Kita-Tsukamoto, 2006) and suggested in other organisms (e.g., Taylor et al, 1983;Mackie and Bone, 1978).…”

Section: Supplementary Tablementioning

confidence: 99%

Leaving the Dark Side? Insights Into the Evolution of Luciferases

Delroisse¹,

Duchatelet²,

Flammang³

et al. 2021

Preprint

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Bioluminescence – i.e., the emission of visible light by living organisms - is defined as a biochemical reaction involving, at least, a luciferin substrate, an oxygen derivative, and a specialised luciferase enzyme. In some cases, the enzyme and the substrate are durably associated and form a photoprotein. While this terminology is educatively useful to explain bioluminescence, it gives a false idea that all luminous organisms are using identical or homologous molecular tools to achieve light emission. As usually observed in biology, reality is more complex. To date, 11 different luciferins have indeed been discovered, and several non-homologous luciferases lato sensu have been identified which, all together, confirms that bioluminescence emerged independently multiple times during the evolution of living organisms. While some phylogenetically related organisms may use non-homologous luciferases (e.g., at least four convergent luciferases are found in Pancrustacea), it has also been observed that phylogenetically distant organisms may use homologous luciferases (e.g., parallel evolution observed in some cnidarians, tunicates and echinoderms that are sharing a homologous luciferase-based system). The evolution of luciferases then appears puzzling. The present review takes stock of the diversity of known “bioluminescent proteins”, their evolution and potential evolutionary origins. A total of 134 luciferase and photoprotein sequences have been investigated (from 75 species and 11 phyla), and our analyses identified 12 distinct types – defined as a group of homologous bioluminescent proteins. The literature review indicated that genes coding for luciferases and photoproteins have potentially emerged as new genes or have been co-opted from ancestral non-luciferase/photoprotein genes. In this latter case, the homologous gene’s co-options may occur independently in phylogenetically distant organisms.

show abstract

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

Cited by 16 publications

References 177 publications

Leaving the Dark Side? Insights Into the Evolution of Luciferases

Leaving the Dark Side? Insights Into the Evolution of Luciferases

Integrating Diel Vertical Migrations of Bioluminescent Deep Scattering Layers Into Monitoring Programs

Leaving the Dark Side? Insights Into the Evolution of Luciferases

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