Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts
Date
2006-08
Authors
Sullivan, Matthew B.
Lindell, Debbie
Lee, Jessica A.
Thompson, Luke R.
Bielawski, Joseph P.
Chisholm, Sallie W.
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Abstract
Cyanophages ( cyanobacterial viruses) are important agents of horizontal gene transfer among
marine cyanobacteria, the numerically dominant photosynthetic organisms in the oceans. Some
cyanophage genomes carry and express host-like photosynthesis genes, presumably to augment the host
photosynthetic machinery during infection. To study the prevalence and evolutionary dynamics of this
phenomenon, 33 cultured cyanophages of known family and host range and viral DNA from field samples
were screened for the presence of two core photosystem reaction center genes, psbA and psbD.
Combining this expanded dataset with published data for nine other cyanophages, we found that 88% of
the phage genomes contain psbA, and 50% contain both psbA and psbD. The psbA gene was found in all
myoviruses and Prochlorococcus podoviruses, but could not be amplified from Prochlorococcus
siphoviruses or Synechococcus podoviruses. Nearly all of the phages that encoded both psbA and psbD
had broad host ranges. We speculate that the presence or absence of psbA in a phage genome may be
determined by the length of the latent period of infection. Whether it also carries psbD may reflect
constraints on coupling of viral- and host-encoded PsbA-PsbD in the photosynthetic reaction center
across divergent hosts. Phylogenetic clustering patterns of these genes from cultured phages suggest
that whole genes have been transferred from host to phage in a discrete number of events over the
course of evolution ( four for psbA, and two for psbD), followed by horizontal and vertical transfer
between cyanophages. Clustering patterns of psbA and psbD from Synechococcus cells were inconsistent
with other molecular phylogenetic markers, suggesting genetic exchanges involving Synechococcus
lineages. Signatures of intragenic recombination, detected within the cyanophage gene pool as well
as between hosts and phages in both directions, support this hypothesis. The analysis of cyanophage
psbA and psbD genes from field populations revealed significant sequence diversity, much of which is
represented in our cultured isolates. Collectively, these findings show that photosynthesis genes
are common in cyanophages and that significant genetic exchanges occur from host to phage, phage to
host, and within the phage gene pool. This generates genetic diversity among the phage, which serves
as a reservoir for their hosts, and in turn influences photosystem evolution.
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Citation
Sullivan, Matthew B., Debbie Lindell, Jessica A. Lee, Luke R. Thompson, et al. 2006. "Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their
hosts." Plos Biology 4(8): 1344-1357.