Photobiology of microorganisms: how photosensors catch a photon to initialize signalling

Abstract

Photobiological processes are relevant for microorganisms for energy generation, protection against excess and/or damaging radiation, and for signalling. In this review we give an overview of the knowledge on the functioning of photosensors in microorganisms, with special emphasis on the conformational changes that lead to signal generation and transduction. Light is absorbed by specific chromophores, which are tuned, by their proteinaceous environment, to function optimally. These chromophores belong to three classes: tetrapyrroles, polyenes and aromatics. The chemical structure of photosensing pigment/protein complexes has been resolved for many of the photobiological processes that have a characteristic sensitivity in the visible and infrared part of the spectrum of (solar) radiation. However, knowledge about the structure of photoreceptors responsible for several physiologically well‐characterized photoresponses to UV‐ and blue light is still lacking. For a limited number of phototransduction processes, the details of light‐induced signal transfer are beginning to be understood in atomic detail. This applies particularly to two photosensors involved in phototactic responses in bacteria: sensory rhodopsin I (SR‐I) from Halobacterium salinarium and photoactive yellow protein (PYP) from Ectothiorhodospira halophila. The SR‐I system is of special interest because the transducer accepting the signal from SR‐I was recently identified as Htr‐I, a homologue of the methyl‐accepting chemotaxis proteins which have been characterized in Escherichia coli. PYP, on the other hand, may be the first photosensor to actually reveal all relevant details of the kinetics, thermodynamics, and molecular motion of light‐induced signal generation, through an understanding of how the photo‐isomerization of the chromophore forces the sensor protein into the signalling state. Here we compare these photosensors and discuss common themes in the initiation of photosensory signal transduction in microorganisms in terms of the molecular properties of photosensors and their signalling state.

trans / cis ( Z / E ) photoisomerization of the chromophore of photoactive yellow protein is not a prerequisite for the initiation of the photocycle of this photoreceptor protein

“…In contrast, the CAO group of the chromophore of hybrid I does reach a similar position as in holoPYP, which therefore subsequently leads to disruption of the hydrogenbonding network of the phenolate oxygen and to partial unfolding of hybrid I into a pB-like signaling state (39). Return from this state may be dependent on interaction with, and catalysis by, side chains from the apoprotein (40). Subångström changes in the mutual distance of the atoms involved can already dramatically slow down this catalytic function (41), which may explain why the overall recovery reaction of hybrid I is 1,000-fold retarded, even though this process in hybrid I does not require the reisomerization of a double bond.…”

On the absorbance changes in the photocycle of the photoactive yellow protein: A quantum-chemical analysis

“…The term bleaching of protein is associated with the formation of the colorless PYP M , because its absorption maximum moves out of the visible range of electromagnetic radiation. Because of the relatively long lifetime, PYP M is assumed to be the signaling species (9,26). The original conformation of the (dark) ground state (PYP G ) is recovered with a rate constant of about 2-3 s Ϫ1 (9).…”

Spectral Tuning, Fluorescence, and Photoactivity in Hybrids of Photoactive Yellow Protein, Reconstituted with Native or Modified Chromophores

“…PYP homologues have been detected in several eubacteria (8 -11). Thus, it has been proposed to refer to this novel family of blue-light photoreceptors as Xanthopsins (11,12).…”