Rhodopsin-bestrophin fusion proteins from unicellular algae form gigantic pentameric ion channels

Andrey Rozenberg; Igor Kaczmarczyk; Donna Matzov; Johannes Vierock; Takashi Nagata; Masahiro Sugiura; Kota Katayama; Yuma Kawasaki; Masae Konno; Yujiro Nagasaka; Mako Aoyama; Ishita Das; Efrat Pahima; Jonathan Church; Suliman Adam; Veniamin A. Borin; Ariel Chazan; Sandra Augustin; Jonas Wietek; Julien Dine; Yoav Peleg; Akira Kawanabe; Yuichiro Fujiwara; Ofer Yizhar; Mordechai Sheves; Igor Schapiro; Yuji Furutani; Hideki Kandori; Keiichi Inoue; Peter Hegemann; Oded Béjà; Moran Shalev-Benami

doi:10.1038/s41594-022-00783-x

Rhodopsin-bestrophin fusion proteins from unicellular algae form gigantic pentameric ion channels

Andrey Rozenberg, Igor Kaczmarczyk, Donna Matzov, Johannes Vierock, Takashi Nagata, Masahiro Sugiura, Kota Katayama, Yuma Kawasaki, Masae Konno, Yujiro Nagasaka, Mako Aoyama, Ishita Das, Efrat Pahima, Jonathan Church, Suliman Adam, Veniamin A. Borin, Ariel Chazan, Sandra Augustin, Jonas Wietek, Julien DineYoav Peleg, Akira Kawanabe, Yuichiro Fujiwara, Ofer Yizhar, Mordechai Sheves, Igor Schapiro, Yuji Furutani, Hideki Kandori, Keiichi Inoue, Peter Hegemann, Oded Béjà, Moran Shalev-Benami

Technion - Israel Institute of Technology, Weizmann Institute of Science, The Hebrew University of Jerusalem

Research output: Contribution to journal › Article › peer-review

Abstract

Many organisms sense light using rhodopsins, photoreceptive proteins containing a retinal chromophore. Here we report the discovery, structure and biophysical characterization of bestrhodopsins, a microbial rhodopsin subfamily from marine unicellular algae, in which one rhodopsin domain of eight transmembrane helices or, more often, two such domains in tandem, are C-terminally fused to a bestrophin channel. Cryo-EM analysis of a rhodopsin-rhodopsin-bestrophin fusion revealed that it forms a pentameric megacomplex (~700 kDa) with five rhodopsin pseudodimers surrounding the channel in the center. Bestrhodopsins are metastable and undergo photoconversion between red- and green-absorbing or green- and UVA-absorbing forms in the different variants. The retinal chromophore, in a unique binding pocket, photoisomerizes from all-trans to 11-cis form. Heterologously expressed bestrhodopsin behaves as a light-modulated anion channel.

Original language	English
Pages (from-to)	592-603
Number of pages	12
Journal	Nature Structural and Molecular Biology
Volume	29
Issue number	6
DOIs	https://doi.org/10.1038/s41594-022-00783-x
State	Published - 16 Jun 2022

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 14 Life Below Water

Keywords

Bestrophins
Ion Channels
Rhodopsin/chemistry

All Science Journal Classification (ASJC) codes

Structural Biology
Molecular Biology

Access to Document

10.1038/s41594-022-00783-x

ms_Nature-Struc-Mole-Bio_Rhodopsin-bestrophin_AM_22.pdfAccepted author manuscript, 11.9 MBLicense: CC BY-NC

Cite this

Rozenberg, A., Kaczmarczyk, I., Matzov, D., Vierock, J., Nagata, T., Sugiura, M., Katayama, K., Kawasaki, Y., Konno, M., Nagasaka, Y., Aoyama, M., Das, I., Pahima, E., Church, J., Adam, S., Borin, V. A., Chazan, A., Augustin, S., Wietek, J., ... Shalev-Benami, M. (2022). Rhodopsin-bestrophin fusion proteins from unicellular algae form gigantic pentameric ion channels. Nature Structural and Molecular Biology, 29(6), 592-603. https://doi.org/10.1038/s41594-022-00783-x

@article{f565089dbfbe40fbb03a91b5a24df270,

title = "Rhodopsin-bestrophin fusion proteins from unicellular algae form gigantic pentameric ion channels",

abstract = "Many organisms sense light using rhodopsins, photoreceptive proteins containing a retinal chromophore. Here we report the discovery, structure and biophysical characterization of bestrhodopsins, a microbial rhodopsin subfamily from marine unicellular algae, in which one rhodopsin domain of eight transmembrane helices or, more often, two such domains in tandem, are C-terminally fused to a bestrophin channel. Cryo-EM analysis of a rhodopsin-rhodopsin-bestrophin fusion revealed that it forms a pentameric megacomplex (\textasciitilde{}700 kDa) with five rhodopsin pseudodimers surrounding the channel in the center. Bestrhodopsins are metastable and undergo photoconversion between red- and green-absorbing or green- and UVA-absorbing forms in the different variants. The retinal chromophore, in a unique binding pocket, photoisomerizes from all-trans to 11-cis form. Heterologously expressed bestrhodopsin behaves as a light-modulated anion channel.",

keywords = "Bestrophins, Ion Channels, Rhodopsin/chemistry",

author = "Andrey Rozenberg and Igor Kaczmarczyk and Donna Matzov and Johannes Vierock and Takashi Nagata and Masahiro Sugiura and Kota Katayama and Yuma Kawasaki and Masae Konno and Yujiro Nagasaka and Mako Aoyama and Ishita Das and Efrat Pahima and Jonathan Church and Suliman Adam and Borin, \{Veniamin A.\} and Ariel Chazan and Sandra Augustin and Jonas Wietek and Julien Dine and Yoav Peleg and Akira Kawanabe and Yuichiro Fujiwara and Ofer Yizhar and Mordechai Sheves and Igor Schapiro and Yuji Furutani and Hideki Kandori and Keiichi Inoue and Peter Hegemann and Oded B{\'e}j{\`a} and Moran Shalev-Benami",

note = "{\textcopyright} 2022. The Author(s), under exclusive licence to Springer Nature America, Inc.",

year = "2022",

month = jun,

day = "16",

doi = "10.1038/s41594-022-00783-x",

language = "الإنجليزيّة",

volume = "29",

pages = "592--603",

journal = "Nature Structural and Molecular Biology",

issn = "1545-9993",

publisher = "Nature Research",

number = "6",

}

Rozenberg, A, Kaczmarczyk, I, Matzov, D, Vierock, J, Nagata, T, Sugiura, M, Katayama, K, Kawasaki, Y, Konno, M, Nagasaka, Y, Aoyama, M, Das, I, Pahima, E, Church, J, Adam, S, Borin, VA, Chazan, A, Augustin, S, Wietek, J, Dine, J, Peleg, Y, Kawanabe, A, Fujiwara, Y, Yizhar, O , Sheves, M , Schapiro, I, Furutani, Y, Kandori, H, Inoue, K, Hegemann, P, Béjà, O & Shalev-Benami, M 2022, 'Rhodopsin-bestrophin fusion proteins from unicellular algae form gigantic pentameric ion channels', Nature Structural and Molecular Biology, vol. 29, no. 6, pp. 592-603. https://doi.org/10.1038/s41594-022-00783-x

TY - JOUR

T1 - Rhodopsin-bestrophin fusion proteins from unicellular algae form gigantic pentameric ion channels

AU - Rozenberg, Andrey

AU - Kaczmarczyk, Igor

AU - Matzov, Donna

AU - Vierock, Johannes

AU - Nagata, Takashi

AU - Sugiura, Masahiro

AU - Katayama, Kota

AU - Kawasaki, Yuma

AU - Konno, Masae

AU - Nagasaka, Yujiro

AU - Aoyama, Mako

AU - Das, Ishita

AU - Pahima, Efrat

AU - Church, Jonathan

AU - Adam, Suliman

AU - Borin, Veniamin A.

AU - Chazan, Ariel

AU - Augustin, Sandra

AU - Wietek, Jonas

AU - Dine, Julien

AU - Peleg, Yoav

AU - Kawanabe, Akira

AU - Fujiwara, Yuichiro

AU - Yizhar, Ofer

AU - Sheves, Mordechai

AU - Schapiro, Igor

AU - Furutani, Yuji

AU - Kandori, Hideki

AU - Inoue, Keiichi

AU - Hegemann, Peter

AU - Béjà, Oded

AU - Shalev-Benami, Moran

PY - 2022/6/16

Y1 - 2022/6/16

N2 - Many organisms sense light using rhodopsins, photoreceptive proteins containing a retinal chromophore. Here we report the discovery, structure and biophysical characterization of bestrhodopsins, a microbial rhodopsin subfamily from marine unicellular algae, in which one rhodopsin domain of eight transmembrane helices or, more often, two such domains in tandem, are C-terminally fused to a bestrophin channel. Cryo-EM analysis of a rhodopsin-rhodopsin-bestrophin fusion revealed that it forms a pentameric megacomplex (~700 kDa) with five rhodopsin pseudodimers surrounding the channel in the center. Bestrhodopsins are metastable and undergo photoconversion between red- and green-absorbing or green- and UVA-absorbing forms in the different variants. The retinal chromophore, in a unique binding pocket, photoisomerizes from all-trans to 11-cis form. Heterologously expressed bestrhodopsin behaves as a light-modulated anion channel.

AB - Many organisms sense light using rhodopsins, photoreceptive proteins containing a retinal chromophore. Here we report the discovery, structure and biophysical characterization of bestrhodopsins, a microbial rhodopsin subfamily from marine unicellular algae, in which one rhodopsin domain of eight transmembrane helices or, more often, two such domains in tandem, are C-terminally fused to a bestrophin channel. Cryo-EM analysis of a rhodopsin-rhodopsin-bestrophin fusion revealed that it forms a pentameric megacomplex (~700 kDa) with five rhodopsin pseudodimers surrounding the channel in the center. Bestrhodopsins are metastable and undergo photoconversion between red- and green-absorbing or green- and UVA-absorbing forms in the different variants. The retinal chromophore, in a unique binding pocket, photoisomerizes from all-trans to 11-cis form. Heterologously expressed bestrhodopsin behaves as a light-modulated anion channel.

KW - Bestrophins

KW - Ion Channels

KW - Rhodopsin/chemistry

UR - http://www.scopus.com/inward/record.url?scp=85132206207&partnerID=8YFLogxK

U2 - 10.1038/s41594-022-00783-x

DO - 10.1038/s41594-022-00783-x

M3 - مقالة

C2 - 35710843

SN - 1545-9993

VL - 29

SP - 592

EP - 603

JO - Nature Structural and Molecular Biology

JF - Nature Structural and Molecular Biology

IS - 6

ER -

Rhodopsin-bestrophin fusion proteins from unicellular algae form gigantic pentameric ion channels

Abstract

UN SDGs

Keywords

All Science Journal Classification (ASJC) codes

Access to Document

Other files and links

Fingerprint

Cite this