Cyanobacterial contribution to the genomes of the plastid-lacking protists

Department of Biological Sciences, Graduate School of Science, University of Tokyo, Bunkyo, Tokyo 113-0033, Japan.
BMC Evolutionary Biology (Impact Factor: 3.37). 09/2009; 9(1):197. DOI: 10.1186/1471-2148-9-197
Source: PubMed


Eukaryotic genes with cyanobacterial ancestry in plastid-lacking protists have been regarded as important evolutionary markers implicating the presence of plastids in the early evolution of eukaryotes. Although recent genomic surveys demonstrated the presence of cyanobacterial and algal ancestry genes in the genomes of plastid-lacking protists, comparative analyses on the origin and distribution of those genes are still limited.
We identified 12 gene families with cyanobacterial ancestry in the genomes of a taxonomically wide range of plastid-lacking eukaryotes (Phytophthora [Chromalveolata], Naegleria [Excavata], Dictyostelium [Amoebozoa], Saccharomyces and Monosiga [Opisthokonta]) using a novel phylogenetic pipeline. The eukaryotic gene clades with cyanobacterial ancestry were mostly composed of genes from bikonts (Archaeplastida, Chromalveolata, Rhizaria and Excavata). We failed to find genes with cyanobacterial ancestry in Saccharomyces and Dictyostelium, except for a photorespiratory enzyme conserved among fungi. Meanwhile, we found several Monosiga genes with cyanobacterial ancestry, which were unrelated to other Opisthokonta genes.
Our data demonstrate that a considerable number of genes with cyanobacterial ancestry have contributed to the genome composition of the plastid-lacking protists, especially bikonts. The origins of those genes might be due to lateral gene transfer events, or an ancient primary or secondary endosymbiosis before the diversification of bikonts. Our data also show that all genes identified in this study constitute multi-gene families with punctate distribution among eukaryotes, suggesting that the transferred genes could have survived through rounds of gene family expansion and differential reduction.

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    • "Regarding the route(s) followed by IS607 to transfer between domains of life, it is noteworthy that several of the taxa in which we found IS607-like sequences have already been involved in various gene HT events. For example, a large number of genes with cyanobacterial ancestry have been uncovered in P. sojae and P. ramorum that are believed to result either from the secondary endosymbiosis through which the ancestor of Stramenopiles acquired its plastid (Tyler et al. 2006; Maruyama et al. 2009; Morris et al. 2009; Keeling 2010) or from later gene HTs specific to oomycetes (Archibald 2009). Several hundred gene HT events have also been reported between bacteria and fungi (Uo et al. 2001; Gojkovicét al. 2004; Hall et al. 2005; Wenzl et al. 2005; Hall and Dietrich 2007; Fitzpatrick et al. 2008; Marcet-Houben and Gabaldon 2010). "
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    ABSTRACT: Horizontal transfer (HT) of transposable elements (TEs) plays a key role in prokaryotic evolution and mounting evidence suggests that it has also had an important impact on eukaryotic evolution. While many prokaryote-to-prokaryote and eukaryote-to-eukaryote HTs of TEs have been characterized, only few cases have been reported between prokaryotes and eukaryotes. Here we carried out a comprehensive search for all major groups of prokaryotic insertion sequences (IS) in 430 eukaryote genomes. We uncovered a total of 80 sequences, all deriving from the IS607 family, integrated in the genomes of 14 eukaryote species belonging to four distinct phyla (Amoebozoa, Ascomycetes, Basidiomycetes and Stramenopiles). Given that eukaryote IS607-like sequences are most closely related to cyanobacterial IS607 and that their phylogeny is incongruent with that of their hosts, we conclude that the presence of IS607-like sequences in eukaryotic genomes is the result of several HT events. Selection analyses further suggest that our ability to detect these prokaryote TEs today in eukaryotes is because HT of these sequences occurred recently and/or some IS607 elements were domesticated after HT, giving rise to new eukaryote genes. Supporting the recent age of some of these HTs, we uncovered intact full-length, potentially active IS607copies in the amoeba Acanthamoeba castellani. Overall, our study shows that prokaryote to eukaryote HT of TEs occurred at relatively low frequency during recent eukaryote evolution and it sets IS607 as the most widespread TE (being present in prokaryotes, eukaryotes, and viruses).
    Full-text · Article · Apr 2013 · Genome Biology and Evolution
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    • "An intriguing case in this respect is the distribution of algal/cyanobacterial genes in eukaryotes. Because eukaryotic photosynthesis is derived from a primary endosymbiosis with a cyanobacterium as well as secondary and tertiary endosymbioses with miscellaneous algae [9-12], these genes are frequently interpreted as relicts of earlier cyanobacterial/algal endosymbionts and, therefore, evidence of plastid losses in some aplastidic eukaryotes [13-15]. As eukaryotic photosynthesis spans multiple major lineages whose relationships critically rely on the plastid existence in them [16-18], an accurate understanding of the distribution and origin of algal genes in eukaryotes is essential. "
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    ABSTRACT: Background Horizontal gene transfer (HGT) is traditionally considered to be rare in multicellular eukaryotes such as animals. Recently, many genes of miscellaneous algal origins were discovered in choanoflagellates. Considering that choanoflagellates are the existing closest relatives of animals, we speculated that ancient HGT might have occurred in the unicellular ancestor of animals and affected the long-term evolution of animals. Results Through genome screening, phylogenetic and domain analyses, we identified 14 gene families, including 92 genes, in the tunicate Ciona intestinalis that are likely derived from miscellaneous photosynthetic eukaryotes. Almost all of these gene families are distributed in diverse animals, suggesting that they were mostly acquired by the common ancestor of animals. Their miscellaneous origins also suggest that these genes are not derived from a particular algal endosymbiont. In addition, most genes identified in our analyses are functionally related to molecule transport, cellular regulation and methylation signaling, suggesting that the acquisition of these genes might have facilitated the intercellular communication in the ancestral animal. Conclusions Our findings provide additional evidence that algal genes in aplastidic eukaryotes are not exclusively derived from historical plastids and thus important for interpreting the evolution of eukaryotic photosynthesis. Most importantly, our data represent the first evidence that more anciently acquired genes might exist in animals and that ancient HGT events have played an important role in animal evolution.
    Full-text · Article · Jun 2012 · BMC Evolutionary Biology
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    • "Similarly, 88 and 14 oomycete-specific OGs have their best blast hits in green and red algae genomes, respectively (supplementary additional file 13, Supplementary Material online). These results, together with studies by others (Andersson and Roger 2002; Tyler et al. 2006; Maruyama et al. 2009), seem to slightly favor the early acquisition of the plastid before the speciation of Stramenochromes and oomycetes. However, recent molecular data support a more complex scenario and later acquisition of the plastid thereby rejecting the Chromalveolate hypothesis (Stiller et al. 2009; Baurain et al. 2010; Felsner et al. 2011; Woehle et al. 2011). "
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    ABSTRACT: The taxonomic class of oomycetes contains numerous pathogens of plants and animals but is related to nonpathogenic diatoms and brown algae. Oomycetes have flexible genomes comprising large gene families that play roles in pathogenicity. The evolutionary processes that shaped the gene content have not yet been studied by applying systematic tree reconciliation of the phylome of these species. We analyzed evolutionary dynamics of ten Stramenopiles. Gene gains, duplications, and losses were inferred by tree reconciliation of 18,459 gene trees constituting the phylome with a highly supported species phylogeny. We reconstructed a strikingly large last common ancestor of the Stramenopiles that contained ~10,000 genes. Throughout evolution, the genomes of pathogenic oomycetes have constantly gained and lost genes, though gene gains through duplications outnumber the losses. The branch leading to the plant pathogenic Phytophthora genus was identified as a major transition point characterized by increased frequency of duplication events that has likely driven the speciation within this genus. Large gene families encoding different classes of enzymes associated with pathogenicity such as glycoside hydrolases are formed by complex and distinct patterns of duplications and losses leading to their expansion in extant oomycetes. This study unveils the large-scale evolutionary dynamics that shaped the genomes of pathogenic oomycetes. By the application of phylogenetic based analyses methods, it provides additional insights that shed light on the complex history of oomycete genome evolution and the emergence of large gene families characteristic for this important class of pathogens.
    Full-text · Article · Jan 2012 · Genome Biology and Evolution
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