Xanthomonas encodes for a novel dodecameric ferritin-like protein with unique structural features

Iron is considered an essential component of all life forms, but is maintained optimally by fine-tuning of iron homeostasis mechanisms. Iron storage proteins (ISPs), which are ferritin superfamily proteins, play a pivotal role in maintaining iron homeostasis by storing excess cellular iron, often serving as ROS scavengers for protecting cells from oxidative stress. Xanthomonas represents a large and ubiquitous group of phytopathogenic bacteria that causes severe crop loss worldwide. Xanthomonas survives host-imposed iron stress by governing iron uptake, transport, and metabolism in utmost coordination within host environment, accomplishing optimal pathogenesis. However, the structural and functional characterization of ISPs encoded by Xanthomonas remains poorly understood to date. The present study computationally explored Xanthomonas encoding four ISPs belonging to multiple ferritin types, including bacterioferritin, bacterial ferritin, and Dps, which are conserved across the species. Additionally, a novel type of ISP, named XccFtnα, has been reported to exhibit a unique 4 + 1 helical organization with an N-terminally positioned short αA helix. It exhibits an unusual dodecameric cage structure and channel characteristics like Dps. In contrast, it has ferroxidase centers resembling those of 24-meric bacterial ferritins, with conserved iron-binding amino acid residues. Further structural investigation indicates XccFtnα exhibits stronger interfacial interactions and cage formation efficiency, compared to other 12-meric XccDps. However, phylogenetic analysis suggests XccFtnα belongs to a closely related evolutionary lineage with homo-24-meric prokaryotic ferritins. Finally, we conclude XccFtnα as a non-heme-containing ferritin-like protein with a compact, stable 12-meric organization, that might be emerged from divergent but independently acquired characteristics from multiple ferritin types.