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Title: Structure-based analysis of CysZ-mediated cellular uptake of sulfate

Sulfur, most abundantly found in the environment as sulfate (SO 4 2-), is an essential element in metabolites required by all living cells, including amino acids, co-factors and vitamins. However, current understanding of the cellular delivery of SO 4 2- at the molecular level is limited. CysZ has been described as a SO 4 2- permease, but its sequence family is without known structural precedent. Based on crystallographic structure information, SO 4 2- binding and flux experiments, we provide insight into the molecular mechanism of CysZ-mediated translocation of SO 4 2- across membranes. CysZ structures from three different bacterial species display a hitherto unknown fold and have subunits organized with inverted transmembrane topology. CysZ from Pseudomonas denitrificans assembles as a trimer of antiparallel dimers and the CysZ structures from two other species recapitulate dimers from this assembly. In conclusion, mutational studies highlight the functional relevance of conserved CysZ residues.
Authors:
 [1] ;  [2] ; ORCiD logo [1] ;  [1] ;  [1] ;  [1] ;  [3] ;  [4] ;  [4] ;  [4] ;  [5] ;  [6] ;  [6] ;  [7] ;  [3] ;  [1] ;  [8] ; ORCiD logo [1]
  1. Columbia Univ., New York, NY (United States)
  2. Brookhaven National Lab. (BNL), Upton, NY (United States)
  3. Virginia Commonwealth Univ. School of Medicine, Richmond, VA (United States)
  4. New York Structural Biology Center, New York, NY (United States)
  5. Univ. Pierre et Marie Curie, Paris (France)
  6. Cornell Univ., NE-CAT, Argonne, IL (United States)
  7. Technical Univ. of Munich, Munich (Germany)
  8. Columbia Univ., New York, NY (United States); Univ. Pierre et Marie Curie, Paris (France)
Publication Date:
Report Number(s):
BNL-205770-2018-JAAM
Journal ID: ISSN 2050-084X
Grant/Contract Number:
SC0012704
Type:
Accepted Manuscript
Journal Name:
eLife
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 2050-084X
Publisher:
eLife Sciences Publications, Ltd.
Research Org:
Brookhaven National Laboratory (BNL), Upton, NY (United States)
Sponsoring Org:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES
OSTI Identifier:
1454809

Assur Sanghai, Zahra, Liu, Qun, Clarke, Oliver B., Belcher-Dufrisne, Meagan, Wiriyasermkul, Pattama, Giese, M. Hunter, Leal-Pinto, Edgar, Kloss, Brian, Tabuso, Shantelle, Love, James, Punta, Marco, Banerjee, Surajit, Rajashankar, Kanagalaghatta R., Rost, Burkhard, Logothetis, Diomedes, Quick, Matthias, Hendrickson, Wayne A., and Mancia, Filippo. Structure-based analysis of CysZ-mediated cellular uptake of sulfate. United States: N. p., Web. doi:10.7554/eLife.27829.
Assur Sanghai, Zahra, Liu, Qun, Clarke, Oliver B., Belcher-Dufrisne, Meagan, Wiriyasermkul, Pattama, Giese, M. Hunter, Leal-Pinto, Edgar, Kloss, Brian, Tabuso, Shantelle, Love, James, Punta, Marco, Banerjee, Surajit, Rajashankar, Kanagalaghatta R., Rost, Burkhard, Logothetis, Diomedes, Quick, Matthias, Hendrickson, Wayne A., & Mancia, Filippo. Structure-based analysis of CysZ-mediated cellular uptake of sulfate. United States. doi:10.7554/eLife.27829.
Assur Sanghai, Zahra, Liu, Qun, Clarke, Oliver B., Belcher-Dufrisne, Meagan, Wiriyasermkul, Pattama, Giese, M. Hunter, Leal-Pinto, Edgar, Kloss, Brian, Tabuso, Shantelle, Love, James, Punta, Marco, Banerjee, Surajit, Rajashankar, Kanagalaghatta R., Rost, Burkhard, Logothetis, Diomedes, Quick, Matthias, Hendrickson, Wayne A., and Mancia, Filippo. 2018. "Structure-based analysis of CysZ-mediated cellular uptake of sulfate". United States. doi:10.7554/eLife.27829.
@article{osti_1454809,
title = {Structure-based analysis of CysZ-mediated cellular uptake of sulfate},
author = {Assur Sanghai, Zahra and Liu, Qun and Clarke, Oliver B. and Belcher-Dufrisne, Meagan and Wiriyasermkul, Pattama and Giese, M. Hunter and Leal-Pinto, Edgar and Kloss, Brian and Tabuso, Shantelle and Love, James and Punta, Marco and Banerjee, Surajit and Rajashankar, Kanagalaghatta R. and Rost, Burkhard and Logothetis, Diomedes and Quick, Matthias and Hendrickson, Wayne A. and Mancia, Filippo},
abstractNote = {Sulfur, most abundantly found in the environment as sulfate (SO42-), is an essential element in metabolites required by all living cells, including amino acids, co-factors and vitamins. However, current understanding of the cellular delivery of SO42- at the molecular level is limited. CysZ has been described as a SO42- permease, but its sequence family is without known structural precedent. Based on crystallographic structure information, SO42- binding and flux experiments, we provide insight into the molecular mechanism of CysZ-mediated translocation of SO42- across membranes. CysZ structures from three different bacterial species display a hitherto unknown fold and have subunits organized with inverted transmembrane topology. CysZ from Pseudomonas denitrificans assembles as a trimer of antiparallel dimers and the CysZ structures from two other species recapitulate dimers from this assembly. In conclusion, mutational studies highlight the functional relevance of conserved CysZ residues.},
doi = {10.7554/eLife.27829},
journal = {eLife},
number = ,
volume = 7,
place = {United States},
year = {2018},
month = {5}
}

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