Efficient Phage-Mediated Pigment Biosynthesis in Oceanic Cyanobacteria

Thorben Dammeyer, Sarah C. Bagby, Matthew Sullivan, Sallie W. Chisholm, Nicole Frankenberg-Dinkel

Research output: Contribution to journalArticle

96 Citations (Scopus)

Abstract

Although the oceanic cyanobacterium Prochlorococcus harvests light with a chlorophyll antenna [1-3] rather than with the phycobilisomes that are typical of cyanobacteria, some strains express genes that are remnants of the ancestral Synechococcus phycobilisomes [4]. Similarly, some Prochlorococcus cyanophages, which often harbor photosynthesis-related genes [5], also carry homologs of phycobilisome pigment biosynthesis genes [6, 7]. Here, we investigate four such genes in two cyanophages that both infect abundant Prochlorococcus strains [8]: homologs of heme oxygenase (ho1), 15,16-dihydrobiliverdin:ferredoxin oxidoreductase (pebA), ferredoxin (petF) in the myovirus P-SSM2, and a phycocyanobilin:ferredoxin oxidoreductase (pcyA) homolog in the myovirus P-SSM4. We demonstrate that the phage homologs mimic the respective host activities, with the exception of the divergent phage PebA homolog. In this case, the phage PebA single-handedly catalyzes a reaction for which uninfected host cells require two consecutive enzymes, PebA and PebB. We thus renamed the phage enzyme phycoerythrobilin synthase (PebS). This gene, and other pigment biosynthesis genes encoded by P-SSM2 (petF and ho1), are transcribed during infection, suggesting that they can improve phage fitness. Analyses of global ocean metagenomes show that PcyA and Ho1 occur in both cyanobacteria and their phages, whereas the novel PebS-encoding gene is exclusive to phages.

Original languageEnglish (US)
Pages (from-to)442-448
Number of pages7
JournalCurrent Biology
Volume18
Issue number6
DOIs
StatePublished - Mar 25 2008
Externally publishedYes

Fingerprint

Bacteriophages
Biosynthesis
Cyanobacteria
Pigments
bacteriophages
pigments
biosynthesis
Prochlorococcus
Phycobilisomes
Genes
phycobilisome
Ferredoxins
ferredoxins
genes
oxidoreductases
Oxidoreductases
Metagenome
Synechococcus
Heme Oxygenase (Decyclizing)
Gene encoding

Keywords

  • EVO_ECOL

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)

Cite this

Dammeyer, T., Bagby, S. C., Sullivan, M., Chisholm, S. W., & Frankenberg-Dinkel, N. (2008). Efficient Phage-Mediated Pigment Biosynthesis in Oceanic Cyanobacteria. Current Biology, 18(6), 442-448. https://doi.org/10.1016/j.cub.2008.02.067

Efficient Phage-Mediated Pigment Biosynthesis in Oceanic Cyanobacteria. / Dammeyer, Thorben; Bagby, Sarah C.; Sullivan, Matthew; Chisholm, Sallie W.; Frankenberg-Dinkel, Nicole.

In: Current Biology, Vol. 18, No. 6, 25.03.2008, p. 442-448.

Research output: Contribution to journalArticle

Dammeyer, T, Bagby, SC, Sullivan, M, Chisholm, SW & Frankenberg-Dinkel, N 2008, 'Efficient Phage-Mediated Pigment Biosynthesis in Oceanic Cyanobacteria', Current Biology, vol. 18, no. 6, pp. 442-448. https://doi.org/10.1016/j.cub.2008.02.067
Dammeyer, Thorben ; Bagby, Sarah C. ; Sullivan, Matthew ; Chisholm, Sallie W. ; Frankenberg-Dinkel, Nicole. / Efficient Phage-Mediated Pigment Biosynthesis in Oceanic Cyanobacteria. In: Current Biology. 2008 ; Vol. 18, No. 6. pp. 442-448.
@article{dfbf0126929b485090309bae0afddf82,
title = "Efficient Phage-Mediated Pigment Biosynthesis in Oceanic Cyanobacteria",
abstract = "Although the oceanic cyanobacterium Prochlorococcus harvests light with a chlorophyll antenna [1-3] rather than with the phycobilisomes that are typical of cyanobacteria, some strains express genes that are remnants of the ancestral Synechococcus phycobilisomes [4]. Similarly, some Prochlorococcus cyanophages, which often harbor photosynthesis-related genes [5], also carry homologs of phycobilisome pigment biosynthesis genes [6, 7]. Here, we investigate four such genes in two cyanophages that both infect abundant Prochlorococcus strains [8]: homologs of heme oxygenase (ho1), 15,16-dihydrobiliverdin:ferredoxin oxidoreductase (pebA), ferredoxin (petF) in the myovirus P-SSM2, and a phycocyanobilin:ferredoxin oxidoreductase (pcyA) homolog in the myovirus P-SSM4. We demonstrate that the phage homologs mimic the respective host activities, with the exception of the divergent phage PebA homolog. In this case, the phage PebA single-handedly catalyzes a reaction for which uninfected host cells require two consecutive enzymes, PebA and PebB. We thus renamed the phage enzyme phycoerythrobilin synthase (PebS). This gene, and other pigment biosynthesis genes encoded by P-SSM2 (petF and ho1), are transcribed during infection, suggesting that they can improve phage fitness. Analyses of global ocean metagenomes show that PcyA and Ho1 occur in both cyanobacteria and their phages, whereas the novel PebS-encoding gene is exclusive to phages.",
keywords = "EVO_ECOL",
author = "Thorben Dammeyer and Bagby, {Sarah C.} and Matthew Sullivan and Chisholm, {Sallie W.} and Nicole Frankenberg-Dinkel",
year = "2008",
month = "3",
day = "25",
doi = "10.1016/j.cub.2008.02.067",
language = "English (US)",
volume = "18",
pages = "442--448",
journal = "Current Biology",
issn = "0960-9822",
publisher = "Cell Press",
number = "6",

}

TY - JOUR

T1 - Efficient Phage-Mediated Pigment Biosynthesis in Oceanic Cyanobacteria

AU - Dammeyer, Thorben

AU - Bagby, Sarah C.

AU - Sullivan, Matthew

AU - Chisholm, Sallie W.

AU - Frankenberg-Dinkel, Nicole

PY - 2008/3/25

Y1 - 2008/3/25

N2 - Although the oceanic cyanobacterium Prochlorococcus harvests light with a chlorophyll antenna [1-3] rather than with the phycobilisomes that are typical of cyanobacteria, some strains express genes that are remnants of the ancestral Synechococcus phycobilisomes [4]. Similarly, some Prochlorococcus cyanophages, which often harbor photosynthesis-related genes [5], also carry homologs of phycobilisome pigment biosynthesis genes [6, 7]. Here, we investigate four such genes in two cyanophages that both infect abundant Prochlorococcus strains [8]: homologs of heme oxygenase (ho1), 15,16-dihydrobiliverdin:ferredoxin oxidoreductase (pebA), ferredoxin (petF) in the myovirus P-SSM2, and a phycocyanobilin:ferredoxin oxidoreductase (pcyA) homolog in the myovirus P-SSM4. We demonstrate that the phage homologs mimic the respective host activities, with the exception of the divergent phage PebA homolog. In this case, the phage PebA single-handedly catalyzes a reaction for which uninfected host cells require two consecutive enzymes, PebA and PebB. We thus renamed the phage enzyme phycoerythrobilin synthase (PebS). This gene, and other pigment biosynthesis genes encoded by P-SSM2 (petF and ho1), are transcribed during infection, suggesting that they can improve phage fitness. Analyses of global ocean metagenomes show that PcyA and Ho1 occur in both cyanobacteria and their phages, whereas the novel PebS-encoding gene is exclusive to phages.

AB - Although the oceanic cyanobacterium Prochlorococcus harvests light with a chlorophyll antenna [1-3] rather than with the phycobilisomes that are typical of cyanobacteria, some strains express genes that are remnants of the ancestral Synechococcus phycobilisomes [4]. Similarly, some Prochlorococcus cyanophages, which often harbor photosynthesis-related genes [5], also carry homologs of phycobilisome pigment biosynthesis genes [6, 7]. Here, we investigate four such genes in two cyanophages that both infect abundant Prochlorococcus strains [8]: homologs of heme oxygenase (ho1), 15,16-dihydrobiliverdin:ferredoxin oxidoreductase (pebA), ferredoxin (petF) in the myovirus P-SSM2, and a phycocyanobilin:ferredoxin oxidoreductase (pcyA) homolog in the myovirus P-SSM4. We demonstrate that the phage homologs mimic the respective host activities, with the exception of the divergent phage PebA homolog. In this case, the phage PebA single-handedly catalyzes a reaction for which uninfected host cells require two consecutive enzymes, PebA and PebB. We thus renamed the phage enzyme phycoerythrobilin synthase (PebS). This gene, and other pigment biosynthesis genes encoded by P-SSM2 (petF and ho1), are transcribed during infection, suggesting that they can improve phage fitness. Analyses of global ocean metagenomes show that PcyA and Ho1 occur in both cyanobacteria and their phages, whereas the novel PebS-encoding gene is exclusive to phages.

KW - EVO_ECOL

UR - http://www.scopus.com/inward/record.url?scp=42049110060&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=42049110060&partnerID=8YFLogxK

U2 - 10.1016/j.cub.2008.02.067

DO - 10.1016/j.cub.2008.02.067

M3 - Article

C2 - 18356052

AN - SCOPUS:42049110060

VL - 18

SP - 442

EP - 448

JO - Current Biology

JF - Current Biology

SN - 0960-9822

IS - 6

ER -