Abstract
Most deep-sea fish have a single visual pigment maximally sensitive at short wavelengths, approximately matching the spectrum of both downwelling sunlight and bioluminescence. However, Malcosteus niger produces far-red bioluminescence and its longwave retinal sensitivity is enhanced by red-shifted visual pigments, a longwave reflecting tapetum and, uniquely, a bacteriochlorophyll-derived photosensitizer. The origin of the photosensitizer, however, remains unclear. We investigated whether the bacteriochlorophyll was produced by endosymbiotic bacteria within unusual structures adjacent to the photoreceptors that had previously been described in this species. However, microscopy, elemental analysis and SYTOX green staining provided no evidence for such localised retinal bacteria, instead the photosensitizer was shown to be distributed throughout the retina. Furthermore, comparison of mRNA from the retina of Malacosteus to that of the closely related Pachystomias microdon (which does not contain a bacterichlorophyll-derived photosensitzer) revealed no genes of bacterial origin that were specifically up-regulated in Malacosteus. Instead up-regulated Malacosteus genes were associated with photosensitivity and may relate to its unique visual ecology and the chlorophyll-based visual system. We also suggest that the unusual longwave-reflecting, astaxanthin-based, tapetum of Malacosteus may protect the retina from the potential cytotoxicity of such a system.
Highlights
Most deep-sea fish have a single visual pigment maximally sensitive at short wavelengths, approximately matching the spectrum of both downwelling sunlight and bioluminescence
An exception are three genera of stomiid dragon fish, that produce longwave bioluminescence[3,4,5] and have longwave-shifted visual pigments compared to other deep-sea animals[1,6,7,8,9,10,11,12,13]
Bacteriochlorophylls c&d are only known to be produced by photosynthetic green sulphur bacteria
Summary
Most deep-sea fish have a single visual pigment maximally sensitive at short wavelengths, approximately matching the spectrum of both downwelling sunlight and bioluminescence. Brauer[20] described an unusual layer of structures between the retinal pigment epithelium (RPE) and the rod outer segments (see Supplementary File S1) Since these retinal structures appear to be unique to Malacosteus, the only species proven to contain a bacteriochlorophyll-derived retinal photosensitizer, and as they are adjacent to the photoreceptor outer segments where the bacteriochlorophyll has its physiological effect, it appears possible they may in some way be involved with bacteriochlorophyll storage/production. They might, for example, be the location of endosymbiotic bacteria
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