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

Abstract

International audienceInteractions 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

The Chlorella variabilis NC64A Genome Reveals Adaptation to Photosymbiosis, Coevolution with Viruses, and Cryptic Sex

“…A similar evolutionary scenario was also evoked for the eukaryotic microalga Emiliania huxleyi that exchanged seven genes of the sphingolipid biosynthesis pathway with its large DNA virus, EhV (Monier et al, 2009), though the direction of gene transfer is unknown. Thus, the large DNA viruses predominantly associated with microalgae and marine protists might have played a much larger role in the evolution of their hosts than previously recognized.…”

Identification of an l -Rhamnose Synthetic Pathway in Two Nucleocytoplasmic Large DNA Viruses

“…Indeed, all other members of the ATCV-1 clade are green algae. This alga-virus HGT event is not surprising or unique, since there is evidence that algae and their viruses have shared some other genes via HGT (32). It is worth noticing that two other green algal viruses, Ostreococcus tauri virus 1 and Ostreococcus virus OsV5, encode putative UGDs; however, they are closer to the one found in metazoa.…”

Host-derived viral transporter protein for nitrogen uptake in infected marine phytoplankton

“…However, the influence of viruses on oceanic ecosystems extends beyond top-down host mortality. Genomic and metagenomic analyses show that marine viruseseither phages or eukaryotic viruses-harbor host-derived genes encoding a diverse range of putative functions (19)(20)(21), including whole biochemical pathways (22). These "auxiliary metabolic genes" (AMGs) may allow the virus to manipulate the host via metabolic reprogramming during infection and have been experimentally shown to alter the central carbon metabolism and pigment biosynthesis of cyanobacteria (23,24) and to "reprogram"…”