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Phylogenomic test of the hypotheses for the evolutionary origin of eukaryotes.

ABSTRACT: The evolutionary origin of eukaryotes is a question of great interest for which many different hypotheses have been proposed. These hypotheses predict distinct patterns of evolutionary relationships for individual genes of the ancestral eukaryotic genome. The availability of numerous completely sequenced genomes covering the three domains of life makes it possible to contrast these predictions with empirical data. We performed a systematic analysis of the phylogenetic relationships of ancestral eukaryotic genes with archaeal and bacterial genes. In contrast with previous studies, we emphasize the critical importance of methods accounting for statistical support, horizontal gene transfer, and gene loss, and we disentangle the processes underlying the phylogenomic pattern we observe. We first recover a clear signal indicating that a fraction of the bacteria-like eukaryotic genes are of alphaproteobacterial origin. Then, we show that the majority of bacteria-related eukaryotic genes actually do not point to a relationship with a specific bacterial taxonomic group. We also provide evidence that eukaryotes branch close to the last archaeal common ancestor. Our results demonstrate that there is no phylogenetic support for hypotheses involving a fusion with a bacterium other than the ancestor of mitochondria. Overall, they leave only two possible interpretations, respectively, based on the early-mitochondria hypotheses, which suppose an early endosymbiosis of an alphaproteobacterium in an archaeal host and on the slow-drip autogenous hypothesis, in which early eukaryotic ancestors were particularly prone to horizontal gene transfers.

SUBMITTER: Rochette NC

PROVIDER: S-EPMC3969559 | biostudies-literature | 2014 Apr

REPOSITORIES: biostudies-literature

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Phylogenomic test of the hypotheses for the evolutionary origin of eukaryotes.

Rochette Nicolas C NC Brochier-Armanet Céline C Gouy Manolo M

Molecular biology and evolution 20140107 4

The evolutionary origin of eukaryotes is a question of great interest for which many different hypotheses have been proposed. These hypotheses predict distinct patterns of evolutionary relationships for individual genes of the ancestral eukaryotic genome. The availability of numerous completely sequenced genomes covering the three domains of life makes it possible to contrast these predictions with empirical data. We performed a systematic analysis of the phylogenetic relationships of ancestral ...[more]

PMID: 24398320

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Project description:Phosphatidylinositol-3-kinases (PI3Ks) are a family of eukaryotic enzymes modifying phosphoinositides in phosphatidylinositols-3-phosphate. Located upstream of the AKT/mTOR signalling pathway, PI3Ks activate secondary messengers of extracellular signals. They are involved in many critical cellular processes such as cell survival, angiogenesis and autophagy. PI3K family is divided into three classes, including 14 human homologs. While class II enzymes are composed of a single catalytic subunit, class I and III also contain regulatory subunits. Here we present an in-depth phylogenetic analysis of all PI3K proteins.We confirmed that PI3K catalytic subunits form a monophyletic group, whereas regulatory subunits form three distinct groups. The phylogeny of the catalytic subunits indicates that they underwent two major duplications during their evolutionary history: the most ancient arose in the Last Eukaryotic Common Ancestor (LECA) and led to the emergence of class III and class I/II, while the second - that led to the separation between class I and II - occurred later, in the ancestor of Unikonta (i.e., the clade grouping Amoebozoa, Fungi, and Metazoa). These two major events were followed by many lineage specific duplications in particular in vertebrates, but also in various protist lineages. Major loss events were also detected in Vidiriplantae and Fungi. For the regulatory subunits, we identified homologs of class III in all eukaryotic groups indicating that, for this class, both the catalytic and the regulatory subunits were presents in LECA. In contrast, homologs of the regulatory class I have a more recent origin.The phylogenetic analysis of the PI3K shed a new light on the evolutionary history of these enzymes. We found that LECA already contained a PI3K class III composed of a catalytic and a regulatory subunit. Absence of class II regulatory subunits and the recent origin of class I regulatory subunits is puzzling given that the class I/II catalytic subunit was present in LECA and has been conserved in most present-day eukaryotic lineages. We also found surprising major loss and duplication events in various eukaryotic lineages. Given the functional specificity of PI3K proteins, this suggests dynamic adaptation during the diversification of eukaryotes.

Project description:BackgroundThe cystatin superfamily comprises cysteine protease inhibitors that play key regulatory roles in protein degradation processes. Although they have been the subject of many studies, little is known about their genesis, evolution and functional diversification. Our aim has been to obtain a comprehensive insight into their origin, distribution, diversity, evolution and classification in Eukaryota, Bacteria and Archaea.ResultsWe have identified in silico the full complement of the cystatin superfamily in more than 2100 prokaryotic and eukaryotic genomes. The analysis of numerous eukaryotic genomes has provided strong evidence for the emergence of this superfamily in the ancestor of eukaryotes. The progenitor of this superfamily was most probably intracellular and lacked a signal peptide and disulfide bridges, much like the extant Giardia cystatin. A primordial gene duplication produced two ancestral eukaryotic lineages, cystatins and stefins. While stefins remain encoded by a single or a small number of genes throughout the eukaryotes, the cystatins have undergone a more complex and dynamic evolution through numerous gene and domain duplications. In the cystatin superfamily we discovered twenty vertebrate-specific and three angiosperm-specific orthologous families, indicating that functional diversification has occurred only in multicellular eukaryotes. In vertebrate orthologous families, the prevailing trends were loss of the ancestral inhibitory activity and acquisition of novel functions in innate immunity. Bacterial cystatins and stefins may be emergency inhibitors that enable survival of bacteria in the host, defending them from the host's proteolytic activity.ConclusionThis study challenges the current view on the classification, origin and evolution of the cystatin superfamily and provides valuable insights into their functional diversification. The findings of this comprehensive study provide guides for future structural and evolutionary studies of the cystatin superfamily as well as of other protease inhibitors and proteases.

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Phylogenomic test of the hypotheses for the evolutionary origin of eukaryotes.

Publications

Phylogenomic test of the hypotheses for the evolutionary origin of eukaryotes.

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