Efficient phage-mediated pigment biosynthesis in oceanic cyanobacteria

Area of Science:

• Marine microbial ecology
• Virology
• Biochemistry

Background:

• Oceanic cyanobacteria like Prochlorococcus use chlorophyll for light harvesting, unlike typical cyanobacteria with phycobilisomes.
• Some Prochlorococcus strains and their infecting cyanophages retain or acquire phycobilisome pigment biosynthesis genes.
• Phycobilisome pigment genes in cyanophages suggest potential roles in host-pathogen interactions and nutrient cycling.

Purpose of the Study:

• To investigate the function and prevalence of phycobilisome pigment biosynthesis gene homologs in Prochlorococcus cyanophages.
• To characterize a novel phage enzyme, PebS, involved in phycoerythrobilin synthesis.
• To determine the transcriptional activity of these phage genes during infection and their distribution in marine environments.

Main Methods:

• Enzyme assays were performed on cyanophage homologs of heme oxygenase (ho1), 15,16-dihydrobiliverdin:ferredoxin oxidoreductase (pebA), ferredoxin (petF), and phycocyanobilin:ferredoxin oxidoreductase (pcyA).
• The catalytic activity of the phage PebA homolog was compared to the host's two-enzyme system (PebA and PebB).
• Metagenomic data from global oceans were analyzed to assess the distribution of these genes in both phages and cyanobacteria.

Main Results:

• Phage homologs of ho1, petF, and pcyA mimicked their respective host enzyme activities.
• The phage PebA homolog, renamed phycoerythrobilin synthase (PebS), uniquely catalyzed a two-step reaction in a single step.
• Phage genes (PebS, petF, ho1) were transcribed during infection, and PebS was found exclusively in phages, while Ho1 and PcyA were in both phages and cyanobacteria.

Conclusions:

• Cyanophages encode functional pigment biosynthesis genes that are expressed during infection, potentially enhancing phage fitness.
• The novel phage enzyme PebS represents a streamlined biochemical pathway for pigment synthesis, exclusive to viruses.
• The presence of these genes in both phages and their hosts highlights complex evolutionary interactions and potential roles in marine biogeochemical cycles.