Horizontal gene transfer of an entire metabolic pathway between a eukaryotic alga and its DNA virus

  1. Adam Monier1,5,
  2. António Pagarete2,
  3. Colomban de Vargas2,6,
  4. Michael J. Allen3,
  5. Betsy Read4,
  6. Jean-Michel Claverie1 and
  7. Hiroyuki Ogata1,6
  1. 1 Structural and Genomic Information Laboratory, CNRS-UPR2589, Mediterranean Institute of Microbiology (IFR-88), Université de la Méditerranée, Parc Scientifique de Luminy, Marseille FR-13288, France;
  2. 2 Equipe EPPO-Evolution du Plancton et PaléoOcéans, CNRS-UMR7144, Université Pierre et Marie Curie, Roscoff FR-29682, France;
  3. 3 Plymouth Marine Laboratory, Plymouth, PL1 3DH, United Kingdom;
  4. 4 Department of Biological Science, California State University San Marcos, San Marcos, California 92096-0001, USA

    Abstract

    Interactions between viruses and phytoplankton, the main primary producers in the oceans, affect global biogeochemical cycles and climate. Recent studies are increasingly revealing possible cases of gene transfers between cyanobacteria and phages, which might have played significant roles in the evolution of cyanobacteria/phage systems. However, little has been documented about the occurrence of horizontal gene transfer in eukaryotic phytoplankton/virus systems. Here we report phylogenetic evidence for the transfer of seven genes involved in the sphingolipid biosynthesis pathway between the cosmopolitan eukaryotic microalga Emiliania huxleyi and its large DNA virus EhV. PCR assays indicate that these genes are prevalent in E. huxleyi and EhV strains isolated from different geographic locations. Patterns of protein and gene sequence conservation support that these genes are functional in both E. huxleyi and EhV. This is the first clear case of horizontal gene transfer of multiple functionally linked enzymes in a eukaryotic phytoplankton–virus system. We examine arguments for the possible direction of the gene transfer. The virus-to-host direction suggests the existence of ancient viruses that controlled the complex metabolic pathway in order to infect primitive eukaryotic cells. In contrast, the host-to-virus direction suggests that the serial acquisition of genes involved in the same metabolic pathway might have been a strategy for the ancestor of EhVs to stay ahead of their closest relatives in the great evolutionary race for survival.

    Footnotes

    • 5 Present address: Monterey Bay Aquarium Research Institute, Moss Landing, CA 95039, USA.

    • 6 Corresponding authors.

      E-mail Hiroyuki.Ogata{at}igs.cnrs-mrs.fr; fax 33-491-825421.

      E-mail vargas{at}sb-roscoff.fr; 33-298-292324.

    • [Supplemental material is available online at www.genome.org. The sequence data from this study have been submitted to GenBank (http://www.ncbi.nlm.nih.gov/Genbank/) under accession nos. FJ531546–FJ531633.]

    • Article published online before print. Article and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.091686.109.

      • Received January 27, 2009.
      • Accepted April 29, 2009.
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