Abstract
Green fluorescent proteins (GFPs) and calcium-activated photoproteins of the aequorin/clytin family, now widely used as research tools, were originally isolated from the hydrozoan jellyfish Aequora victoria. It is known that bioluminescence resonance energy transfer (BRET) is possible between these proteins to generate flashes of green light, but the native function and significance of this phenomenon is unclear. Using the hydrozoan Clytia hemisphaerica, we characterized differential expression of three clytin and four GFP genes in distinct tissues at larva, medusa and polyp stages, corresponding to the major in vivo sites of bioluminescence (medusa tentacles and eggs) and fluorescence (these sites plus medusa manubrium, gonad and larval ectoderms). Potential physiological functions at these sites include UV protection of stem cells for fluorescence alone, and prey attraction and camouflaging counter-illumination for bioluminescence. Remarkably, the clytin2 and GFP2 proteins, co-expressed in eggs, show particularly efficient BRET and co-localize to mitochondria, owing to parallel acquisition by the two genes of mitochondrial targeting sequences during hydrozoan evolution. Overall, our results indicate that endogenous GFPs and photoproteins can play diverse roles even within one species and provide a striking and novel example of protein coevolution, which could have facilitated efficient or brighter BRET flashes through mitochondrial compartmentalization.
Highlights
Both bioluminescence and fluorescence are widespread natural phenomena, in the marine environment [1,2,3]
Green light flashes in the hydrozoan jellyfish Aequora victoria are generated by two famous proteins acting together, the calcium-sensitive photoprotein aequorin and green fluorescent protein (GFP)
In the case of Aequora, aequorin generates blue light with a broad emission peak centred around a wavelength of 460 nm, which directly excites GFP molecules to be re-emitted as green light with a much sharper peak centred at 508 nm [6,7,8,9,10]
Summary
Both bioluminescence and fluorescence are widespread natural phenomena, in the marine environment [1,2,3]. Green light flashes in the hydrozoan jellyfish Aequora victoria are generated by two famous proteins acting together, the calcium-sensitive photoprotein aequorin and green fluorescent protein (GFP). These proteins and their engineered derivatives are today used for a vast range of applications, including subcellular calcium imaging, cell lineage tracing, gene regulation analysis and detecting protein –protein interactions [4]. Fluorescence involves light emission from a fluorophore following energy absorption, usually from light of a shorter, higher energy wavelength. In the case of Aequora, aequorin generates blue light with a broad emission peak centred around a wavelength of 460 nm, which directly excites GFP molecules to be re-emitted as green light with a much sharper peak centred at 508 nm [6,7,8,9,10]
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