Localisation and origin of the bacteriochlorophyll-derived photosensitizer in the retina of the deep-sea dragon fish Malacosteus niger

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.

Structural and Functional Consequences of the Weak Binding of Chlorin e6 to Bovine Rhodopsin

“…We suspect the presence of Ce6 and related compounds in the dragonfish retina is simply a consequence of diet, without a specific role in vision. The latter hypothesis is supported by recent localization studies that show these compounds to be distributed throughout all retinal layers in varying amounts, including the inner retina and the retinal plexiform layers (44). Lipid-soluble compounds such as Ce6 may be enriched in the plexiform layers due to their higher density membranes (44).…”

“…The latter hypothesis is supported by recent localization studies that show these compounds to be distributed throughout all retinal layers in varying amounts, including the inner retina and the retinal plexiform layers . Lipid‐soluble compounds such as Ce6 may be enriched in the plexiform layers due to their higher density membranes . Given that in darkness, even the human eye is able to detect dim red light of wavelengths >650 nm (and even longer wavelengths at higher light intensities), there is no need to invoke Ce6 binding as a requirement for rhodopsin activation.…”

Chlorophyll-Derivative Modulation of Rhodopsin Signaling Properties through Evolutionarily Conserved Interaction Pathways

“…It has been proposed that Ce6 plays a role in modifying the receptor-chromophore interactions in rhodopsin that adapts the Malacosteus niger ( M. niger ) dragon fish visual system (Douglas et al, 1998 , 1999 , 2016 ; Kenaley et al, 2014 ). Ce6-induced modification in intra- and inter-protein interactions permit the M. niger species to emit far-red light from suborbital photophores, in addition to the blue bioluminescence that is normally emitted by deep-sea dragon fish.…”

The biology of color

“…The way in which humans think about color is influenced by our own abilities and experience, but it is now widely appreciated that animals have different visual abilities: For example, insects and birds see UV, and birds have more than three retinal cones types; some fish even change their color vision with diet (31) and use chlorophyll in far-red sensing (32). We conceive of color as a percept with attributes of hue, saturation, and lightness, but other species may process receptor information differently.…”