Whole-genome analysis reveals molecular innovations and evolutionary transitions in chromalveolate species

Abstract

The chromalveolates form a highly diverse and fascinating assemblage of organisms, ranging from obligatory parasites such as Plasmodium to free-living ciliates and algae such as kelps, diatoms, and dinoflagellates. Many of the species in this monophyletic grouping are of major medical, ecological, and economical importance. Nevertheless, their genome evolution is much less well studied than that of higher plants, animals, or fungi. In the current study, we have analyzed and compared 12 chromalveolate species for which wholesequence information is available and provide a detailed picture on gene loss and gene gain in the different lineages. As expected, many gene loss and gain events can be directly correlated with the lifestyle and specific adaptations of the organisms studied. For instance, in the obligate intracellular Apicomplexa we observed massive loss of genes that play a role in general basic processes such as amino acid, carbohydrate, and lipid metabolism, reflecting the transition of a free-living to an obligate intracellular lifestyle. In contrast, many gene families show species-specific expansions, such as those in the plant pathogen oomycete Phytophthora that are involved in degrading the plant cell wall polysaccharides to facilitate the pathogen invasion process. In general, chromalveolates show a tremendous difference in genome structure and evolution and in the number of genes they have lost or gained either through duplication or horizontal gene transfer.gene gain ͉ gene loss

The origins of apicomplexan sequence innovation

“…This supports the notion that the Apicomplexa as a group do not share many ancient common adaptations (Martens et al 2008). Six hundred of the 9134 families were shared across deeper taxonomic groupings, of which 173 protein families were identified as potentially being present in the ancestral apicomplexan ( Fig.…”

“…With many more sequences available for these and additional species, we can update this proportion to 7% of proteins. A more recent study, which included the six fully sequenced apicomplexan genomes, focused more on differences between the basal chromalveolate groups (Oomycetes, Diatoms, Apicomplexa, and Ciliates) (Martens et al 2008). We concentrate specifically on the Apicomplexa and focus on extracting the biological implications of our findings.…”

“…Studies of these data sets have provided insights into adaptations that relate to their parasitic ecology, such as the identification of expanded families of proteases in Plasmodium (Wu et al 2003). More systematic sequence comparisons have started to uncover genes restricted to specific Apicomplexa orders (Li et al 2003a;Martens et al 2008), or even individual species (Brayton et al 2007).…”

A Domain-Centric Analysis of Oomycete Plant Pathogen Genomes Reveals Unique Protein Organization

“…The FYVEtype zinc finger is not identified in prokaryotic species; hence, we suggest two independent events, namely a horizontal gene transfer of the GAF domain from bacteria to oomycetes and subsequently a fusion to the zinc finger domain. Horizontal gene transfer seems to play an important role in the evolution of eukaryotes (Keeling and Palmer, 2008), and recent evidence indicates that these events also have a significant contribution to the genome content of protists and oomycetes, as they received genetic material from different sources (Richards and Talbot, 2007;Martens et al, 2008;Morris et al, 2009). Because GAF domains are known to be involved in many different cellular processes, we can only speculate about the biological function of proteins harboring the GAF-FYVE bigram.…”

“…The genomes of oomycetes sequenced so far are variable in size and content, ranging from 65 Mb in Phytophthora ramorum to 240 Mb in P. infestans (Haas et al, 2009), and only include plant pathogenic species. Analysis of these genomes revealed that several gene families facilitating the infection process are expanded (Martens et al, 2008). Extreme examples are gene families encoding cytoplasmic effector proteins such as RXLR effectors, which share the host cell-targeting motif RXLR and suppress defense responses in the host, and the necrosis-inducing proteins classified as Crinklers (Crn; Haas et al, 2009).…”