Protein Interactions in Rhodopseudomonas palustris TIE-1 Reveal the Molecular Basis for Resilient Photoferrotrophic Iron Oxidation

Inês B. Trindade, Maria O. Firmino, Sander J. Noordam, Alexandra S. Alves, Bruno M. Fonseca, Mario Piccioli, Ricardo O. Louro

Research output: Contribution to journalArticlepeer-review

2 Citations (Scopus)
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Abstract

Rhodopseudomonas palustris is an alphaproteobacterium with impressive metabolic versatility, capable of oxidizing ferrous iron to fix carbon dioxide using light energy. Photoferrotrophic iron oxidation is one of the most ancient metabolisms, sustained by the pio operon coding for three proteins: PioB and PioA, which form an outer-membrane porin–cytochrome complex that oxidizes iron outside of the cell and transfers the electrons to the periplasmic high potential iron–sulfur protein (HIPIP) PioC, which delivers them to the light-harvesting reaction center (LH-RC). Previous studies have shown that PioA deletion is the most detrimental for iron oxidation, while, the deletion of PioC resulted in only a partial loss. The expression of another periplasmic HiPIP, designated Rpal_4085, is strongly upregulated in photoferrotrophic conditions, making it a strong candidate for a PioC substitute. However, it is unable to reduce the LH-RC. In this work we used NMR spectroscopy to map the interactions between PioC, PioA, and the LH-RC, identifying the key amino acid residues involved. We also observed that PioA directly reduces the LH-RC, and this is the most likely substitute upon PioC deletion. By contrast, Rpal_4085 demontrated significant electronic and structural differences from PioC. These differences likely explain its inability to reduce the LH-RC and highlight its distinct functional role. Overall, this work reveals the functional resilience of the pio operon pathway and further highlights the use of paramagnetic NMR for understanding key biological processes.

Original languageEnglish
Article number4733
JournalMolecules
Volume28
Issue number12
DOIs
Publication statusPublished - Jun 2023

Keywords

  • biological electron transfer
  • cytochrome c
  • HIPIP
  • paramagnetic NMR
  • photoferrotrophism
  • protein interactions
  • Rhodopseudomonas

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