Nonredundant roles for cytochrome c2 and two high-potential iron-sulfur proteins in the photoferrotroph Rhodopseudomonas palustris TIE-1

J Bacteriol. 2014 Feb;196(4):850-8. doi: 10.1128/JB.00843-13. Epub 2013 Dec 6.

Abstract

The purple bacterium Rhodopseudomonas palustris TIE-1 expresses multiple small high-potential redox proteins during photoautotrophic growth, including two high-potential iron-sulfur proteins (HiPIPs) (PioC and Rpal_4085) and a cytochrome c2. We evaluated the role of these proteins in TIE-1 through genetic, physiological, and biochemical analyses. Deleting the gene encoding cytochrome c2 resulted in a loss of photosynthetic ability by TIE-1, indicating that this protein cannot be replaced by either HiPIP in cyclic electron flow. PioC was previously implicated in photoferrotrophy, an unusual form of photosynthesis in which reducing power is provided through ferrous iron oxidation. Using cyclic voltammetry (CV), electron paramagnetic resonance (EPR) spectroscopy, and flash-induced spectrometry, we show that PioC has a midpoint potential of 450 mV, contains all the typical features of a HiPIP, and can reduce the reaction centers of membrane suspensions in a light-dependent manner at a much lower rate than cytochrome c2. These data support the hypothesis that PioC linearly transfers electrons from iron, while cytochrome c2 is required for cyclic electron flow. Rpal_4085, despite having spectroscopic characteristics and a reduction potential similar to those of PioC, is unable to reduce the reaction center. Rpal_4085 is upregulated by the divalent metals Fe(II), Ni(II), and Co(II), suggesting that it might play a role in sensing or oxidizing metals in the periplasm. Taken together, our results suggest that these three small electron transfer proteins perform different functions in the cell.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Cytochromes c2 / genetics
  • Cytochromes c2 / metabolism*
  • Gene Deletion
  • Iron-Sulfur Proteins / genetics
  • Iron-Sulfur Proteins / metabolism*
  • Light
  • Metals / metabolism
  • Oxidation-Reduction
  • Photosynthesis
  • Photosynthetic Reaction Center Complex Proteins / genetics
  • Photosynthetic Reaction Center Complex Proteins / metabolism*
  • Rhodopseudomonas / enzymology*
  • Rhodopseudomonas / genetics
  • Rhodopseudomonas / metabolism*
  • Spectrum Analysis
  • Static Electricity

Substances

  • Bacterial Proteins
  • Iron-Sulfur Proteins
  • Metals
  • Photosynthetic Reaction Center Complex Proteins
  • high potential iron-sulfur protein
  • Cytochromes c2