In absolute darkness, the CNG channel current of rod photoreceptor outer segments exhibits fluctuations. Some of the fluctuations, occurring about once per 100 s in mammalian rods, have a time course and amplitude that makes them indistinguishable from the single-photon response (SPR)—the electrical response of the rod to the isomerization of a single rhodopsin molecule (Baylor et al., 1980, 1984; Pugh, 2018). While the evidence is compelling that these spontaneous “photon-like” events arise from activation of rhodopsin and consequently phototransduction, the physical mechanism of rhodopsin activation is somewhat controversial. Specifically, recent publications have proposed the hypothesis that spontaneous ultraweak photon emission (UPE) in the eye is the mechanism underlying the photon-like CNG current fluctuations of dark-adapted rods (Bókkon and Vimal, 2009; Wang et al., 2011; Salari et al., 2015, 2016; Li and Dai, 2016). In this issue of the Journal of General Physiology, Govardovskii et al. provide evidence very important for resolving this debate.
Bioluminescence is known to be exhibited by diverse organisms ranging from bacteria to dinoflagellates, angler fish, and fireflies (Wilson and Hastings, 2013; Thouand, 2014). Less widely known is that virtually all living tissues, from yeast to plants and humans, generate low level bioluminescence (Boveris et al., 1980; Quickenden et al., 1985; Calcerrada and Garcia-Ruiz, 2018). This latter UPE is generally understood to arise from chemiluminescence that is inherent in various biological redox reactions, including in particular lipid peroxidation (Boveris et al., 1981; Niggli, 1992; Sharov et al., 1996; Thar and Kühl, 2004; Catalá, 2006; Rastogi and Pospísil, 2011; Tryka, 2011). As rod outer segments comprise dense stacks of lipid membranes as well as the machinery of rod phototransduction, it was reasonable to hypothesize that UPE from outer segment lipid peroxidation could underlie the spontaneous photon-like CNG current fluctuations (Salari et al., 2016; Fig. 1).
Govardovskii et al. (2019) provide compelling evidence and analysis that reject the hypothesis that UPE is the mechanism of rod photon-like dark noise in frogs (Rana bidibunda) and sterlets (sturgeons; Acipenser ruthenus) at room temperature. They do so by directly measuring UPE in isolated retinas from the two species, and comparing this with recordings of spontaneous photon-like events in rods under the same conditions and SPRs of rods to carefully measured illumination. The total UPE measured in the experiments from a waveband ranging from 300 nm to 600 nm was ∼2,700 photons s−1 cm−2 of retina per 4π steradians, roughly consistent with prior measurements (Fig. 1). Relatively straightforward calculations, based on the well-established absorbance of rhodopsin and its measured density in the rods, then establish that the UPE is ∼100-fold weaker than necessary to account for the measured “photon-like” dark noise of the rods.
The ability of rods to respond reliably to single photons is an extraordinary capability—one that clearly expanded the photic environment in which vertebrates could survive. No doubt this was achieved by evolutionary selection pressure on the rhodopsin molecule itself, on the biochemistry of rod phototransduction, and on retinal cell types and circuitry (Pugh, 2018). The findings of Govardovskii et al. (2019) indirectly lend support to the long-standing idea that the spontaneous activation of rhodopsin arises from an intrinsic susceptibility of the rhodopsin chromophore in situ to thermal activation (Luo et al., 2011), a susceptibility that the evolution of rhodopsin was unable to eliminate, despite greatly lowering its rate relative to the rate of thermal isomerization in vitro (Kim et al., 2003). Amazingly, this greatly reduced thermal isomerization rate still dictates the absolute sensitivity of night vision by setting a floor of noise, the Eigengrau, of the entire visual system (Hecht et al., 1942; Barlow, 1956; Naarendorp et al., 2010). While the work of Govardovskii et al. (2019) makes it clear that this floor of noise is not set by the UPE, it nonetheless focuses attention on an interesting, ubiquitous photonic feature of biological systems.
Merritt C. Maduke served as editor.