Leptosphaeria rhodopsin: bacteriorhodopsin-like proton pump from a eukaryote.

Bacteriorhodopsin-like proteins provide archaea and eubacteria with a unique bioenergetic pathway comprising light-driven transmembrane proton translocation by a single retinal-binding protein. Recently, homologous proteins were found to perform photosensory functions in lower eukaryotes, but no active ion transport by eukaryotic rhodopsins was detected. By demonstrating light-driven proton pumping in a fungal rhodopsin from Leptosphaeria maculans, we present a case of a retinal-based proton transporter from a eukaryote. This result implies that in addition to oxidative phosphorylation and chlorophyll photosynthesis, some lower eukaryotes may have retained the archaeal route of building an electrochemical transmembrane gradient of protons.

[1]  R. Callender,et al.  Resonance Raman studies of the purple membrane. , 1977, Biochemistry.

[2]  D. Oesterhelt,et al.  Functions of a new photoreceptor membrane. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Andrei K. Dioumaev,et al.  Photochemical Reaction Cycle and Proton Transfers inNeurospora Rhodopsin* , 2001, The Journal of Biological Chemistry.

[4]  J. Lanyi Mechanism of base-catalyzed Schiff base deprotonation in halorhodopsin. , 1986, Biochemistry.

[5]  F. Young Biochemistry , 1955, The Indian Medical Gazette.

[6]  Oleg A. Sineshchekov,et al.  Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[7]  J. Spudich,et al.  A Fourier Transform Infrared Study of Neurospora Rhodopsin: Similarities with Archaeal Rhodopsins¶,† , 2002, Photochemistry and photobiology.

[8]  S. Waschuk,et al.  FTIR spectroscopy of the K photointermediate of Neurospora rhodopsin: structural changes of the retinal, protein, and water molecules after photoisomerization. , 2004, Biochemistry.

[9]  J. Spudich,et al.  A eukaryotic protein, NOP-1, binds retinal to form an archaeal rhodopsin-like photochemically reactive pigment. , 1999, Biochemistry.

[10]  Marion Leclerc,et al.  Proteorhodopsin phototrophy in the ocean , 2001, Nature.

[11]  D. Natvig,et al.  The nop-1 gene of Neurospora crassa encodes a seven transmembrane helix retinal-binding protein homologous to archaeal rhodopsins. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[12]  J. Spudich,et al.  Proton transport by sensory rhodopsins and its modulation by transducer-binding. , 2000, Biochimica et biophysica acta.

[13]  M. Saraste,et al.  FEBS Lett , 2000 .

[14]  B. Howlett,et al.  Characterization of an opsin gene from the ascomycete Leptosphaeria maculans. , 2001, Genome.

[15]  E. Bamberg,et al.  A defective proton pump, point‐mutated bacteriorhodopsin Asp96‐‐‐‐Asn is fully reactivated by azide. , 1989, The EMBO journal.

[16]  J. Rigaud,et al.  Use of the fluorescent pH probe pyranine to detect heterogeneous directions of proton movement in bacteriorhodopsin reconstituted large liposomes , 1985 .

[17]  J. Lanyi,et al.  Pathways of proton release in the bacteriorhodopsin photocycle. , 1992, Biochemistry.

[18]  B. Howlett,et al.  Leptosphaeria maculans, the causal agent of blackleg disease of Brassicas. , 2001, Fungal genetics and biology : FG & B.

[19]  D. Menick,et al.  The proton release group of bacteriorhodopsin controls the rate of the final step of its photocycle at low pH. , 1999, Biochemistry.

[20]  H. Khorana,et al.  Aspartic acid-96 is the internal proton donor in the reprotonation of the Schiff base of bacteriorhodopsin. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[21]  J. Heberle,et al.  Infrared Difference Spectra of the Intermediates L, M, N, and O of the Bacteriorhodopsin Photoreaction Obtained by Time-Resolved Attenuated Total Reflection Spectroscopy , 1997 .

[22]  E. Bamberg,et al.  Channelrhodopsin-1: A Light-Gated Proton Channel in Green Algae , 2002, Science.

[23]  Jureepan Saranak,et al.  Rhodopsin guides fungal phototaxis , 1997, Nature.

[24]  B. Honig,et al.  Correlation of vibrational frequencies with absorption maxima in polyenes, rhodopsin, bacteriorhodopsin, and retinal analogs , 1983 .

[25]  Csilla Gergely,et al.  Bacteriorhodopsin intermediate spectra determined over a wide pH range , 1997 .

[26]  J. Spudich,et al.  Retinylidene proteins: structures and functions from archaea to humans. , 2000, Annual review of cell and developmental biology.

[27]  L. Brown Fungal rhodopsins and opsin-related proteins: eukaryotic homologues of bacteriorhodopsin with unknown functions , 2004, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[28]  S. Grzesiek,et al.  Time‐course and stoichiometry of light‐induced proton release and uptake during the photocycle of bacteriorhodopsin , 1986 .