Thermosynechoccus elongatus DpsA binds Zn(II) at a unique three histidine‐containing ferroxidase center and utilizes O₂ as iron oxidant with very high efficiency, unlike the typical Dps proteins

Abstract

The cyanobacterium Thermosynechococcus elongatus is one the few bacteria to possess two Dps proteins, DpsA‐Te and Dps‐Te. The present characterization of DpsA‐Te reveals unusual structural and functional features that differentiate it from Dps‐Te and the other known Dps proteins. Notably, two Zn(II) are bound at the ferroxidase center, owing to the unique substitution of a metal ligand at the A‐site (His78 in place of the canonical aspartate) and to the presence of a histidine (His164) in place of a hydrophobic residue at a metal‐coordinating distance in the B‐site. Only the latter Zn(II) is displaced by incoming iron, such that Zn(II)–Fe(III) complexes are formed upon oxidation, as indicated by absorbance and atomic emission spectroscopy data. In contrast to the typical behavior of Dps proteins, where Fe(II) oxidation by H2O2 is about 100‐fold faster than by O2, in DpsA‐Te the ferroxidation efficiency of O2 is very high and resembles that of H2O2. Oxygraphic experiments show that two Fe(II) are required to reduce O2, and that H2O2 is not released into solution at the end of the reaction. On this basis, a reaction mechanism is proposed that also takes into account the formation of Zn(II)–Fe(III) complexes. The physiological significance of the DpsA‐Te behavior is discussed in the framework of a possible localization of the protein at the thylakoid membranes, where photosynthesis takes place, with the consequent increased formation of reactive oxygen species. Structured digital abstract http://mint.bio.uniroma2.it/mint/search/interaction.do?interactionAc=MINT-7312099: DpsA (uniprotkb:http://www.uniprot.org/uniprot/Q8DL82?format=text&ascii) and DpsA (uniprotkb:http://www.uniprot.org/uniprot/Q8DL82?format=text&ascii) bind (http://www.ebi.ac.uk/ontology-lookup/?termId=MI:0407) by x‐ray crystallography (http://www.ebi.ac.uk/ontology-lookup/?termId=MI:0114)

Structural and Thermodynamic Characterization of Metal Ion Binding in Streptococcus suis Dpr

“…12 Recently, the binding of two zinc ions to the FOC of Thermosynechoccus elongatus DpsA was reported and attributed to the preference of the protein for O 2 over H 2 O 2 in the catalytic mechanism. 13 Moreover, a dizinc binding in the ferroxidase site of Streptococcus pyogenes Dpr has also been reported. 14 A number of other zinc binding sites away from the ferroxidase site have been identified.…”

Biomimetic Materials Synthesis from Ferritin-Related, Cage-Shaped Proteins

“…4B). These ferroxidase centre ligands are conserved in all Dps with the only known exception of T. elongatus DpsA, where His78 replaces the canonical aspartate (D58, Listeria numbering) (Alaleona et al, 2010 ). The occupancy of the two metal binding sites with iron varies significantly in the known crystal structures.…”

“…The only known exception is represented by DpsA from T. elongatus. The peculiar set of iron coordination residues of this protein, where the conserved Asp58 (Listeria numbering) is replaced by His78, endows the A site with a strong affinity for Zn(II) (Alaleona et al, 2010). …”

The Dps4 fromNostoc punctiformeATCC 29133 is a member of His-type FOC containing Dps protein class that can be broadly found among cyanobacteria

“…In cyanobacteria the existence of multiple Dps proteins has been found to be rather common [13,14]. But most of the more well-studied Dps proteins originate from pathogens that possess only one or two Dps proteins [2,15–17].…”