Biophysics and Quantum Limitation of Photoreceptive Processes

Biophysics and Quantum Limitation of Photoreceptive Processes: Comparison

Please note this is a comparison between Version 2 by Laura Barsanti and Version 1 by Laura Barsanti.

This entry paper is an attempt to explain how the discrete nature of light (energy discreteness in the form of photons) constrains the light detection process all along the evolutionary path, in the not-fully-understood photoreceptive systems of unicellular microorganisms (nonimaging systems) and in the complex and well-known visual system of higher organisms (imaging systems). All these systems are perfect examples of the interplay between physics and biology, i.e., they are the perfect topic of research for biophysicists. The paper describes how photoreceptive and visual systems achieve the goal of photon counting, which information is conveyed by a finite number of photons, and which noise factors limit light-detecting processes.

rhodopsin
retina
eye
Euglena gracilis
noise
information

It would be difficult to find a more perfect example of the interplay between physics and biology (a perfect topic for biophysical research) than light detection systems along the evolutionary path. Nature had coped with the hard constraint of the quantum nature of light until it came across the wondrous rhodopsin protein, an almost-noise-free photon counter. By means of this passé-partout, nature has succeeded in extracting and handling the maximum amount of information out of a limited amount of photons despite its statistical fluctuation (photon noise) ^[1].

We could say then that the final goal of a light-detecting system is to capture and count individual photons as nature mastered the art of counting photons as an early evolutionary adaptation. Incorporation of photosensitive proteins in the cell membrane can be traced back to Archaebacteria, such as Halobacterium halobium; in this prokaryote, bidimensionally oriented proteins span the cell membrane in almost all its surface, providing cells with a highly efficient photon-capturing device ^[2]. Successively, three-dimensional (3D) photosensitive structures evolved as light-receptor organelles consisting of a stack of many photosensitive membranes by adapting flagella for the purpose. The unicellular flagellate Euglena gracilis is a typical example of these 3D structures; in the apical part of the cell, there is a photoreceptive system composed of an intracellular screen, named eyespot, and a 3D crystalline photoreceptor, named paraflagellar body (PFB), located inside the membrane of the emerging flagellum, whose beating moves the cell into its search for light ^[3]. According to Eakin, the adaptation of a cilium (basal centriole + microtubular axoneme) as a light detector by the incorporation of a photopigment in its membrane suggests a common ancestry of the taxa bearing light-sensitive cilia ^[4]. He indicated Euglena, with its photoreceptive system, as the very early evolutionary step of the ciliary line leading to the complex vertebrate light sensor.

Photoreceptive and visual systems apparently achieved the goal of detecting (and using) incoming photons. If it was just a matter of detecting and using the energy of the incident photons, plants would have already solved the problem by developing the photosynthetic machinery, an almost perfectly efficient solar-to-chemical energy converter ^[5]. But the counting of photons entails not only their efficient absorption (hence, a dedicated pigment) but also other technical issues related to noise, sensitivity, and amplification.

Rhodopsin-like proteins (rhodopsin from hereon) are dedicated light-absorbing pigments whose sensitivity (e.g., how well their molecule absorbs light) corresponds to a molar absorption coefficient ε of about 40–60,000 M⁻¹·cm⁻¹ and an inherent noise (dark noise) approximately equal to zero. These values are at the best of the theoretical limits of any light-absorbing molecules [6,7]^[6][7].

The energy of an absorbed photon can modify only a single molecule, and this information cannot be conveyed beyond the point of absorption unless some sort of process transforms this tiny signal into a robust downstream signaling event, which will eventually increase the environmental sensitivity so critical for the survival and propagation of the species. This is the reason for the sophisticated process of amplification.

In the case of the photoreceptive process of microorganisms such as Euglena, knowledge of the amplification cascade that transforms the light perception in a cellular response is still incomplete and poorly understood, whereas the sequential amplification steps adopted by the visual system of higher organisms (e.g., the human eye) have been identified in almost all their details. In these systems, amplification is achieved by means of a cascade of nested reactions (the higher the number of nested reactions, the greater the amplification), each catalyzing the subsequent reaction [8,9,10]^[8][9][10].

In this paper, we describe the nonimaging photoreceptive process of Euglena and the visual imaging process of the human retina in their different biophysical aspects, analyzing the effect of quantum limitation on their efficiency and functioning.

References

Rose, A. Vision: Human and Electronic; Springer Science & Business Media: New York, NY, USA, 1973.
Oesterhelt, D.; Stoeckenius, W. Rhodopsin-like protein from the purple membrane of Halobacterium halobium. Nat. New Biol. 1971, 233, 149–152.
Rosati, G.; Verni, F.; Barsanti, L.; Passarelli, V.; Gualtieri, P. Ultrastructure of the apical zone of Euglena gracilis: Photoreceptors and motor apparatus. Electron Microsc. Rev. 1991, 4, 319–342.
Eakin, R.M. Evolution of photoreceptors. Cold Spring Harb. Symp. Quant. Biol. 1965, 30, 363–370.
Stirbet, A.; Lazár, D.; Guo, Y.; Govindjee, G. Photosynthesis: Basics, history and modelling. Ann. Bot. 2019, 126, 511–537.
Stryer, L. Biochemistry, 3rd ed.; W.H. Freeman: New York, NY, USA, 1988.
Gualtieri, P. A biological point of view on photoreception (no-imaging vision) in algae. J. Photochem. Photobiol. B Biol. 1993, 18, 95–97.
Holmes, R.M.; Victora, M.; Wang, R.F.; Kwiat, P.G. Testing the limits of human vision with quantum states of light: Past, present, and future experiments. In Advanced Photon Counting Techniques XII, 1065903, Proceedings of SPIE—The International Society for Optical Engineering, Orlando, FL, USA, 15–19 April 2018; Campbell, J.C., Itzler, M.A., Eds.; SPIE: Bellingham, WA, USA, 2018; Volume 10659.
Horrigan, D.M.; Makino, C.L. How Do We See? An Introduction to the Biophysics of Visual Transduction. Tutorial Posted on the Biophisical Society Web Page. 2023. Available online: https://www.biophysics.org/ (accessed on 17 November 2023).
Arshavsky, V.Y.; Burns, M.E. Current understanding of signal amplification in phototransduction. Cell. Logist. 2014, 4, e29390.