A redox switch allows binding of Fe(II) and Fe(III) ions in the cyanobacterial iron-binding protein FutA from Prochlorococcus
Rachel Bolton
(1, 2)
,
Moritz Machelett
(1, 3)
,
Jack Stubbs
(1, 2)
,
Danny Axford
(2)
,
Nicolas Caramello
(4)
,
Lucrezia Catapano
(5, 6)
,
Martin Malý
(1)
,
Matthew Rodrigues
(1, 2)
,
Charlotte Cordery
(1, 2)
,
Graham Tizzard
(1)
,
Fraser Macmillan
(7)
,
Sylvain Engilberge
(8)
,
David von Stetten
(8)
,
Takehiko Tosha
(9)
,
Hiroshi Sugimoto
(9)
,
Jonathan Worrall
(10)
,
Jeremy Webb
(1, 2)
,
Mike Zubkov
(11)
,
Simon Coles
(12, 1)
,
Eric Mathieu
(13)
,
Roberto Steiner
(5)
,
Garib Murshudov
(14)
,
Tobias Schrader
(15)
,
Allen Orville
(16)
,
Antoine Royant
(13)
,
Gwyndaf Evans
(17)
,
Michael Hough
(17)
,
Robin Owen
(17)
,
Ivo Tews
(2)
1
University of Southampton
2 DIAMOND Light source
3 NOC - National Oceanography Centre
4 IPMC - Institut de pharmacologie moléculaire et cellulaire
5 King‘s College London
6 LMB - MRC Laboratory of Molecular Biology [Cambridge, UK]
7 UEA - University of East Anglia [Norwich]
8 ESRF - European Synchrotron Radiation Facility [Grenoble]
9 RIKEN RSC - RIKEN SPring-8 Center [Hyogo]
10 University of Essex
11 NOC - National Oceanography Centre [Southampton]
12 UCAD - Université Cheikh Anta Diop de Dakar [Sénégal]
13 IBS - UMR 5075 - Institut de biologie structurale
14 MRCLMB - Medical Research Council Laboratory of Molecular Biology
15 JCNS - Jülich Centre for Neutron Science
16 Research Complex at Harwell
17 Harwell Science and Innovation Campus [Didcot, UK]
2 DIAMOND Light source
3 NOC - National Oceanography Centre
4 IPMC - Institut de pharmacologie moléculaire et cellulaire
5 King‘s College London
6 LMB - MRC Laboratory of Molecular Biology [Cambridge, UK]
7 UEA - University of East Anglia [Norwich]
8 ESRF - European Synchrotron Radiation Facility [Grenoble]
9 RIKEN RSC - RIKEN SPring-8 Center [Hyogo]
10 University of Essex
11 NOC - National Oceanography Centre [Southampton]
12 UCAD - Université Cheikh Anta Diop de Dakar [Sénégal]
13 IBS - UMR 5075 - Institut de biologie structurale
14 MRCLMB - Medical Research Council Laboratory of Molecular Biology
15 JCNS - Jülich Centre for Neutron Science
16 Research Complex at Harwell
17 Harwell Science and Innovation Campus [Didcot, UK]
Rachel Bolton
- Fonction : Auteur
- PersonId : 1396926
- ORCID : 0000-0002-0409-8354
Moritz Machelett
- Fonction : Auteur
- PersonId : 1396927
- ORCID : 0009-0008-2328-6271
Jack Stubbs
- Fonction : Auteur
- PersonId : 1316260
- ORCID : 0000-0002-3788-1687
Nicolas Caramello
- Fonction : Auteur
- PersonId : 1172280
- IdHAL : nicolas-caramello
- ORCID : 0000-0003-0025-0213
Lucrezia Catapano
- Fonction : Auteur
- PersonId : 1316261
- ORCID : 0000-0002-5641-0098
Matthew Rodrigues
- Fonction : Auteur
- PersonId : 813125
- ORCID : 0000-0003-1243-903X
Charlotte Cordery
- Fonction : Auteur
- PersonId : 1316262
- ORCID : 0000-0003-2321-8144
Fraser Macmillan
- Fonction : Auteur
- PersonId : 1316264
- ORCID : 0000-0002-2410-4790
Sylvain Engilberge
- Fonction : Auteur
- PersonId : 1168021
- ORCID : 0000-0001-8680-6790
- IdRef : 22783884X
David von Stetten
- Fonction : Auteur
- PersonId : 1178190
- ORCID : 0000-0001-7906-9788
Takehiko Tosha
- Fonction : Auteur
- PersonId : 1316265
- ORCID : 0000-0002-8971-0759
Hiroshi Sugimoto
- Fonction : Auteur
- PersonId : 1316266
- ORCID : 0000-0002-3140-8362
Jonathan Worrall
- Fonction : Auteur
- PersonId : 1316267
- ORCID : 0000-0002-1863-834X
Eric Mathieu
- Fonction : Auteur
- PersonId : 1316270
- ORCID : 0000-0001-8032-4790
Roberto Steiner
- Fonction : Auteur
- PersonId : 1316271
- ORCID : 0000-0001-7084-9745
Tobias Schrader
- Fonction : Auteur
- PersonId : 1316273
- ORCID : 0000-0001-5159-0846
Allen Orville
- Fonction : Auteur
- PersonId : 1316274
- ORCID : 0000-0002-7803-1777
Antoine Royant
- Fonction : Auteur
- PersonId : 1640
- IdHAL : antoine-royant
- ORCID : 0000-0002-1919-8649
- IdRef : 16610020X
Michael Hough
- Fonction : Auteur
- PersonId : 1316276
- ORCID : 0000-0001-7377-6713
Robin Owen
- Fonction : Auteur
- PersonId : 1316277
- ORCID : 0000-0002-2104-7057
Résumé
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.