Photoreceptor for Curling Behavior in Peranema trichophorum and Evolution of Eukaryotic Rhodopsins

Abstract

When it is gliding, the unicellular euglenoid Peranema trichophorum uses activation of the photoreceptor rhodopsin to control the probability of its curling behavior. From the curled state, the cell takes off in a new direction. In a similar manner, archaea such as Halobacterium use light activation of bacterio-and sensory rhodopsins to control the probability of reversal of the rotation direction of flagella. Each reversal causes the cell to change its direction. In neither case does the cell track light, as known for the rhodopsin-dependent eukaryotic phototaxis of fungi, green algae, cryptomonads, dinoflagellates, and animal larvae. Rhodopsin was identified in Peranema by its native action spectrum (peak at 2.43 eV or 510 nm) and by the shifted spectrum (peak at 3.73 eV or 332 nm) upon replacement of the native chromophore with the retinal analog n-hexenal. The in vivo physiological activity of n-hexenal incorporated to become a chromophore also demonstrates that charge redistribution of a short asymmetric chromophore is sufficient for receptor activation and that the following isomerization step is probably not required when the rest of the native chromophore is missing. This property seems universal among the Euglenozoa, Plant, and Fungus kingdom rhodopsins. The rhodopsins of animals have yet to be studied in this respect. The photoresponse appears to be mediated by Ca 2؉ influx.Since rhodopsins sharing sequence similarities are found in bacteria, archaea, eukaryotic microorganisms, and animals, it is possible to gain insight into the evolutionary progression and diversification leading to the receptor proteins of human visual photoreceptors as well as other photoreceptors. As part of this continuing project on the evolution and mechanisms of visual systems, the light-dependent responses of Peranema have been studied with respect to behavior, action spectra, the mechanism of activation, and signaling to the cell.Peranema trichophorum is a colorless eukaryotic phagotroph of the Euglenophyta that lives in fresh water (8). It does not have a chloroplast but rapidly deforms in shape and is very effective at capturing and eating prey (41). Peranema voraciously takes any particles into its body by phagocytosis (1). This "feeding behavior" is clearly and commonly observed under the microscope. Its life cycle is not well studied, but from light microscopic observations Peranema appears to have several distinct stages of growth. After the cells are put into fresh medium, which is initially low on waste products, one sees small round cells of about 10 to 15 m in diameter. These cells elongate into oval cells that swim freely in solution and fast in a helical euglenoid motion. Over 2 weeks, these cells elongate further to 25 to 70 m in length, remaining 10 m wide, and are seen to glide forward on a surface pulled by their leading anterior cilium, which is about the length of the cell body. (We use the word "cilium" rather than "eukaryotic flagellum" to describe the leading appendage that enables the cell to glide to e...

Evolution of phototaxis

“…However, Peranema lacks a stigma and is not capable of true phototactic orientation (Saranak & Foster 2005). …”

Evidence from Chlamydomonas on the Photoactivation of Rhodopsins without Isomerization of Their Chromophore

“…Trans -2-hexenal ( 2 ), a short acyclic aldehyde, restored rhodopsin-dependent phototaxis in a green alga Chlamydomonas (Foster et al, 1989; Nakanishi et al, 1989), in the chytridiomycete Allomyces reticulatus (Saranak and Foster, 1997), and the curling behavior in a euglenoid Peranema trichophorum (Saranak and Foster, 2005). Shape changes in the chromophore due to isomerization may not be crucial to receptor photoactivation in these three organisms in different eukaryotic Kingdoms.…”

“…Rhodopsins are membrane receptor proteins which use a light absorbing chromophore to capture the light and as a consequence of light absorption gain enzymatic activity. Rhodopsins are found in bacteria; archaea; eukaryotes such as Peranema (a euglenoid) (Saranak and Foster, 2005), Chlamydomonas (a green alga) (Foster et al, 1984), Allomyces (a chytrid motile fungus) (Saranak and Foster 1997); and animals. The existence of similar conserved amino acids in all rhodopsins in the region surrounding the chromophore (Saranak and Foster, 2005) indicates the likelihood of common or at least similar mechanisms of rhodopsin activation.…”

Origin and early evolution of neural circuits for the control of ciliary locomotion

“…Protists are capable of active predation [24], vectorial navigation such as phototaxis [25 -27] or gravitaxis [28 -30], and navigation along a gradient (chemotaxis; [31]). Simpler responses to mechanical [24] or light stimuli can also be present [32].…”