Prochlorococcus phage ferredoxin: Structural characterization and electron transfer to cyanobacterial sulfite reductases

By Ian J. Campbell, Jose Luis Olmos, Weijun Xu, Dimithree Kahanda, Joshua T. Atkinson, Othneil Noble Sparks, Mitchell Miller1, George Phillips1, George N. Bennett, Jonathan J. Silberg

1. Rice University

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Type

journal-article

Author

Ian J. Campbell and Jose Luis Olmos and Weijun Xu and Dimithree Kahanda and Joshua T Atkinson and Othneil Noble Sparks and Mitchell D. Miller and George N Phillips and George N. Bennett and Jonathan J. Silberg

Citation

Campbell, I.J. et al., 2020. Prochlorococcus phage ferredoxin: Structural characterization and electron transfer to cyanobacterial sulfite reductases. Journal of Biological Chemistry, p.jbc.RA120.013501. Available at: http://dx.doi.org/10.1074/jbc.ra120.013501.

Abstract

Marine cyanobacteria are infected by phages whose genomes encode ferredoxin (Fd) electron carriers. These Fds are thought to redirect the energy harvested from light to phage-encoded oxidoreductases that enhance viral fitness, but it is  unclear how the biophysical properties and partner specificities of phage Fds relate to those in photosynthetic organisms. Here, results of a bioinformatics analysis using a sequence similarity network revealed that phage Fds are most closely related to cyanobacterial Fds that transfer electrons from photosystems to oxidoreductases involved in nutrient assimilation. Structural analysis of myovirus P-SSM2 Fd (pssm2-Fd), which infects the cyanobacterium Prochlorococcusmarinus, revealed a high  similarity to cyanobacterial Fds (≤ 0.5 Å root-mean-square deviation). Additionally, pssm2-Fd exhibited a low midpoint reduction potential (–336 mV versus standard hydrogen electrode) similar to other photosynthetic Fds, albeit had lower thermostability (Tm = 28°C) than many other Fds. When expressed in an Escherichia coli strain deficient in sulfite assimilation, pssm2-Fd complemented bacterial growth when co-expressed with a P. marinus sulfite reductase, revealing that pssm2-Fd can transfer electrons to a host protein involved in nutrient assimilation. The high structural similarity with cyanobacterial Fds and reactivity with a host sulfite reductase suggest that phage Fds evolved to transfer electrons to cyanobacterial-encoded oxidoreductases.

DOI

Funding

NSF-STC Biology with X-ray Lasers (NSF-1231306)