A redox switch allows binding of Fe(II) and Fe(III) ions in the cyanobacterial iron- binding protein FutA from Prochlorococcus

• 成果类型: Article
• 署名作者: Bolton, Rachel; Machelett, Moritz M.; Stubbs, Jack; Axford, Danny; Caramello, Nicolas; Catapano, Lucrezia; Maly, Martin; Rodrigues, Matthew J.; Cordery, Charlotte; Tizzard, Graham J.; Macmillan, Fraser; Engilberge, Sylvain; von Stetten, David; Tosha, Takehiko; Sugimoto, Hiroshi; Worrall, Jonathan A. R.; Webb, Jeremy S.; Zubkov, Mike; Coles, Simon; Mathieu, Eric; Steiner, Roberto A.; Murshudov, Garib; Schrader, Tobias E.; Orville, Allen M.; Royant, Antoine; Evans, Gwyndaf; Hough, Michael A.; Owen, Robin L.; Tews, Ivo
• 署名单位: University of Southampton; Diamond Light Source; NERC National Oceanography Centre; European Synchrotron Radiation Facility (ESRF); University of Hamburg; University of London; King's College London; UK Research & Innovation (UKRI); Medical Research Council UK (MRC); MRC Laboratory Molecular Biology; Swiss Federal Institutes of Technology Domain; Paul Scherrer Institute; University of Southampton; University of East Anglia; Communaute Universite Grenoble Alpes; Universite Grenoble Alpes (UGA); CEA; Centre National de la Recherche Scientifique (CNRS); European Molecular Biology Laboratory (EMBL); RIKEN; University of Essex; University of Southampton; University of the Highlands & Islands; University of Padua; Helmholtz Association; Research Center Julich; Rosalind Franklin Institute
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-10703
• DOI: 10.1073/pnas.2308478121
• 发表日期: 2024-03-19
• 关键词: photosynthetic electron-transport; serial synchrotron; crystallography; idia; phytoplankton; subunit; clades

摘要

The marine cyanobacterium Prochlorococcus is a main contributor to global photosynthesis, whilst being limited by iron availability. Cyanobacterial genomes generally encode two different types of FutA iron- binding proteins: periplasmic FutA2 ABC transporter subunits bind Fe(III), while cytosolic FutA1 binds Fe(II). Owing to their small size and their economized genome Prochlorococcus ecotypes typically possess a single futA gene. How the encoded FutA protein might bind different Fe oxidation states was previously unknown. Here, we use structural biology techniques at room temperature to probe the dynamic behavior of FutA. Neutron diffraction confirmed four negatively charged tyrosinates, that together with a neutral water molecule coordinate iron in trigonal bipyramidal geometry. Positioning of the positively charged Arg103 side chain in the second coordination shell yields an overall charge- neutral Fe(III) binding state in structures determined by neutron diffraction and serial femtosecond crystallography. Conventional rotation X - ray crystallography using a home source revealed X- ray- induced photoreduction of the iron center with observation of the Fe(II) binding state; here, an additional positioning of the Arg203 side chain in the second coordination shell maintained an overall charge neutral Fe(II) binding site. Dose series using serial synchrotron crystallography and an XFEL X - ray pump-probe approach capture the transition between Fe(III) and Fe(II) states, revealing how Arg203 operates as a switch to accommodate the different iron oxidation states. This switching ability of the Prochlorococcus FutA protein may reflect ecological adaptation by genome streamlining and loss of specialized FutA proteins.