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

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 of 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 Prochlorococcus marinus, revealed high levels of similarity to cyanobacterial Fds (root mean square deviations of ≤0.5 Å). Additionally, pssm2-Fd exhibited a low midpoint reduction potential (–336 mV versus a standard hydrogen electrode), similar to other photosynthetic Fds, although it had lower thermostability (Tm = 28 °C) than did many other Fds. When expressed in an Escherichia coli strain deficient in sulfite assimilation, pssm2-Fd complemented bacterial growth when coexpressed with a P. marinus sulfite reductase, revealing that pssm2-Fd can transfer electrons to a host protein involved in nutrient assimilation. The high levels of structural similarity with cyanobacterial Fds and reactivity with a host sulfite reductase suggestmore » that phage Fds evolved to transfer electrons to cyanobacterially encoded oxidoreductases.« less

Authors:
ORCiD logo; ORCiD logo; ; ; ORCiD logo; ORCiD logo; ORCiD logo; ORCiD logo; ; ORCiD logo
Publication Date:
Research Org.:
Rice Univ., Houston, TX (United States); Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Aeronautics and Space Administration (NASA); National Science Foundation (NSF); Gordon and Betty Moore Foundation; National Cancer Institutes; National Institutes of General Medical Sciences; National Institutes of Health (NIH)
OSTI Identifier:
1769482
Alternate Identifier(s):
OSTI ID: 1802667
Grant/Contract Number:  
SC0014462; AC02-06CH11357; 7524; 80NSSC18M0093; 1231306; ACB-12002; AGM-12006; S10 OD012289
Resource Type:
Published Article
Journal Name:
Journal of Biological Chemistry
Additional Journal Information:
Journal Name: Journal of Biological Chemistry Journal Volume: 295 Journal Issue: 31; Journal ID: ISSN 0021-9258
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; biochemistry & molecular biology; cyanbacteria; cyanophage; marine; bacteriophage; reductase; hydrogen sulfide; structural biology; electron transfer; ferredoxin; sulfite reductase

Citation Formats

Campbell, Ian J., Olmos, Jr., Jose Luis, Xu, Weijun, Kahanda, Dimithree, Atkinson, Joshua T., Sparks, Othneil Noble, Miller, Mitchell D., Phillips, Jr., George N., Bennett, George N., and Silberg, Jonathan J. Prochlorococcus phage ferredoxin: structural characterization and electron transfer to cyanobacterial sulfite reductases. United States: N. p., 2020. Web. doi:10.1074/jbc.RA120.013501.
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Campbell, Ian J., Olmos, Jr., Jose Luis, Xu, Weijun, Kahanda, Dimithree, Atkinson, Joshua T., Sparks, Othneil Noble, Miller, Mitchell D., Phillips, Jr., George N., Bennett, George N., & Silberg, Jonathan J. Prochlorococcus phage ferredoxin: structural characterization and electron transfer to cyanobacterial sulfite reductases. United States. https://doi.org/10.1074/jbc.RA120.013501
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Campbell, Ian J., Olmos, Jr., Jose Luis, Xu, Weijun, Kahanda, Dimithree, Atkinson, Joshua T., Sparks, Othneil Noble, Miller, Mitchell D., Phillips, Jr., George N., Bennett, George N., and Silberg, Jonathan J. Wed . "Prochlorococcus phage ferredoxin: structural characterization and electron transfer to cyanobacterial sulfite reductases". United States. https://doi.org/10.1074/jbc.RA120.013501.
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@article{osti_1769482,
title = {Prochlorococcus phage ferredoxin: structural characterization and electron transfer to cyanobacterial sulfite reductases},
author = {Campbell, Ian J. and Olmos, Jr., Jose Luis and Xu, Weijun and Kahanda, Dimithree and Atkinson, Joshua T. and Sparks, Othneil Noble and Miller, Mitchell D. and Phillips, Jr., George N. and Bennett, George N. and Silberg, Jonathan J.},
abstractNote = {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 of 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 Prochlorococcus marinus, revealed high levels of similarity to cyanobacterial Fds (root mean square deviations of ≤0.5 Å). Additionally, pssm2-Fd exhibited a low midpoint reduction potential (–336 mV versus a standard hydrogen electrode), similar to other photosynthetic Fds, although it had lower thermostability (Tm = 28 °C) than did many other Fds. When expressed in an Escherichia coli strain deficient in sulfite assimilation, pssm2-Fd complemented bacterial growth when coexpressed with a P. marinus sulfite reductase, revealing that pssm2-Fd can transfer electrons to a host protein involved in nutrient assimilation. The high levels of structural similarity with cyanobacterial Fds and reactivity with a host sulfite reductase suggest that phage Fds evolved to transfer electrons to cyanobacterially encoded oxidoreductases.},
doi = {10.1074/jbc.RA120.013501},
journal = {Journal of Biological Chemistry},
number = 31,
volume = 295,
place = {United States},
year = {Wed Jul 01 00:00:00 EDT 2020},
month = {Wed Jul 01 00:00:00 EDT 2020}
}
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