PubMed Health⌕ Search

Biomedical subjects

Eric Bapteste

Publications and source records attributed to Eric Bapteste.

17 recordsLinked to original sources

Refuting phylogenetic relationships.

BACKGROUND: Phylogenetic methods are philosophically grounded, and so can be philosophically biased in ways that limit explanatory power. This constitutes an important methodologic dimension not often taken into account. Here we address this dimension in the context of concatenation approaches to phylogeny. RESULTS: We discuss some of the limits of a methodology restricted to verificationism, the philosophy on which gene concatenation practices generally rely. As an alternative, we describe a software which identifies and focuses on impossible or refuted relationships, through a simple analysis of bootstrap bipartitions, followed by multivariate statistical analyses. We show how refuting phylogenetic relationships could in principle facilitate systematics. We also apply our method to the study of two complex phylogenies: the phylogeny of the archaea and the phylogeny of the core of genes shared by all life forms. While many groups are rejected, our results left open a possible proximity of N. equitans and the Methanopyrales, of the Archaea and the Cyanobacteria, and as well the possible grouping of the Methanobacteriales/Methanoccocales and Thermosplasmatales, of the Spirochaetes and the Actinobacteria and of the Proteobacteria and firmicutes. CONCLUSION: It is sometimes easier (and preferable) to decide which species do not group together than which ones do. When possible topologies are limited, identifying local relationships that are rejected may be a useful alternative to classical concatenation approaches aiming to find a globally resolved tree on the basis of weak phylogenetic markers. REVIEWERS: This article was reviewed by Mark Ragan, Eugene V Koonin and J Peter Gogarten.

Journal Article↗

A selective barrier to horizontal gene transfer in the T4-type bacteriophages that has preserved a core genome with the viral replication and structural genes.

Genomic analysis of bacteriophages frequently reveals a mosaic structure made up from modules that come from disparate sources. This fact has led to the general acceptance of the notion that rampant and promiscuous lateral gene transfer (LGT) plays a critical role in phage evolution. However, recent sequencing of a series of the T4-type phages has revealed that these large and complex genomes all share 2 substantial syntenous blocks of genes encoding the replication and virion structural genes. To analyze the pattern of inheritance of this core T4 genome, we compared the complete genome sequences of 16 T4-type phages. We identified a set of 24 genes present in all these T4-type genomes. Somewhat surprisingly, only one of these genes, that encodes for ribonucleotide reductase (NrdA), displayed evidence of LGT with the bacterial host. We test the congruence of the inheritance of the other 23 markers using heat map analyses and comparison of a reference topology with the 23 individual gene phylogenies. The vast majority of these core genes share a common evolutionary history. In contrast, analyses of all the noncore genes present in the same 16 genomes, located in the hyperplastic regions of the genome, show considerable evidence of frequent LGT. The similar evolution of the core replication and virion structural genes in the T4-type phage genomes suggests that, unlike the situation in many other phage groups, such portions of T4-type genome have been inherited as a block, without significant LGT, from a distant common ancestor. The preservation of the synteny of the core T4 genome could result from several factors acting in synergy, such as the constraints imposed by the sophisticated regulation of the transcription. Moreover, numerous and complex protein-protein interactions during virion morphogenesis could also impose a supplementary barrier against LGT. Finally, there may be some real evolutionary advantage to maintaining large regions of conserved sequence. Such segments could be a sort of genetic glue that maintains the genetic cohesion of the T4-type phages via recombination within the most conserved sequences. This could mediate the swapping of nonconserved sequences that they flank.

Bacteriophage T4↗

The two tempos of nuclear pore complex evolution: highly adapting proteins in an ancient frozen structure.

BACKGROUND: The origin of the nuclear compartment has been extensively debated, leading to several alternative views on the evolution of the eukaryotic nucleus. Until recently, too little phylogenetic information was available to address this issue by using multiple characters for many lineages. RESULTS: We analyzed 65 proteins integral to or associated with the nuclear pore complex (NPC), including all the identified nucleoporins, the components of their anchoring system and some of their main partners. We used reconstruction of ancestral sequences of these proteins to expand the detection of homologs, and showed that the majority of them, present all over the nuclear pore structure, share homologs in all extant eukaryotic lineages. The anchoring system, by contrast, is analogous between the different eukaryotic lineages and is thus a relatively recent innovation. We also showed the existence of high heterogeneity of evolutionary rates between these proteins, as well as between and within lineages. We show that the ubiquitous genes of the nuclear pore structure are not strongly conserved at the sequence level, and that only their domains are relatively well preserved. CONCLUSION: We propose that an NPC very similar to the extant one was already present in at least the last common ancestor of all extant eukaryotes and it would not have undergone major changes since its early origin. Importantly, we observe that sequences and structures obey two very different tempos of evolution. We suggest that, despite strong constraints that froze the structural evolution of the nuclear pore, the NPC is still highly adaptive, modern, and flexible at the sequence level.

Adaptation, Physiological↗

Evolutionary plasticity of methionine biosynthesis.

Methionine is an essential cellular constituent, the initiator of protein synthesis and a precursor in many metabolic activities, such as methylation and formylation. Here we investigate the genomic distribution of the methionine biosynthetic pathway and analyze its evolutionary history by reconstructing the phylogeny of its enzymatic components. We demonstrate the evolutionary complexity of methionine synthesis and describe the various mechanisms that have shaped this biosynthetic pathway: gene duplication, functional reassignment, lateral acquisition and gene loss. Lateral gene transfer within and between domains and gene recruitment have played an important role in the evolution of this pathway, especially in its first and third enzymatic steps--homoserine activation and homocysteine methylation. These analyses are also the basis of predictions regarding methionine synthesis in Archaea, where the pathway is yet to be characterized. This study illustrates how diverse molecular solutions can fulfill a conserved function in living beings.

Arabidopsis↗

Deduction of probable events of lateral gene transfer through comparison of phylogenetic trees by recursive consolidation and rearrangement.

BACKGROUND: When organismal phylogenies based on sequences of single marker genes are poorly resolved, a logical approach is to add more markers, on the assumption that weak but congruent phylogenetic signal will be reinforced in such multigene trees. Such approaches are valid only when the several markers indeed have identical phylogenies, an issue which many multigene methods (such as the use of concatenated gene sequences or the assembly of supertrees) do not directly address. Indeed, even when the true history is a mixture of vertical descent for some genes and lateral gene transfer (LGT) for others, such methods produce unique topologies. RESULTS: We have developed software that aims to extract evidence for vertical and lateral inheritance from a set of gene trees compared against an arbitrary reference tree. This evidence is then displayed as a synthesis showing support over the tree for vertical inheritance, overlaid with explicit lateral gene transfer (LGT) events inferred to have occurred over the history of the tree. Like splits-tree methods, one can thus identify nodes at which conflict occurs. Additionally one can make reasonable inferences about vertical and lateral signal, assigning putative donors and recipients. CONCLUSION: A tool such as ours can serve to explore the reticulated dimensionality of molecular evolution, by dissecting vertical and lateral inheritance at high resolution. By this, we mean that individual nodes can be examined not only for congruence, but also for coherence in light of LGT. We assert that our tools will facilitate the comparison of phylogenetic trees, and the interpretation of conflicting data.

Animals↗

Does the 'Ring of Life' ring true?

In a recent stimulating paper, Rivera and Lake applied a new phylogenetic method to study the evolution of genomes, which challenges the classical representation of the Tree of Life. Acknowledging the evolutionary importance of lateral gene transfer, they used the conditioned genome approach to reconstruct the Tree of Life, and in the end proposed a Ring of Life. They explained that the Ring of Life structure is a result of a single fusion event between two prokaryotic genomes at the base of the eukaryotic tree, probably between the ancestors of a photosynthetic bacterium and an archaeon. Because this constitutes an important conclusion with regards to the evolutionary process and origin of the eukaryotic cell, their work deserves further attention before these conclusions can be accepted. Here we question the reconstruction and the meaning of the Ring of Life. In addition to general problems associated with gene-content-based phylogenetic analyses, we discuss some implicit premises and potential weaknesses of the conditioned genome method and conclude that, although Rivera and Lake's conclusions might be right, they have not been established by their current approach.

Eukaryotic Cells↗

Higher-level classification of the Archaea: evolution of methanogenesis and methanogens.

We used a phylogenetic approach to analyze the evolution of methanogenesis and methanogens. We show that 23 vertically transmitted ribosomal proteins do not support the monophyly of methanogens, and propose instead that there are two distantly related groups of extant archaea that produce methane, which we have named Class I and Class II. Based on this finding, we subsequently investigated the uniqueness of the origin of methanogenesis by studying both the enzymes of methanogenesis and the proteins that synthesize its specific coenzymes. We conclude that hydrogenotrophic methanogenesis appeared only once during evolution. Genes involved in the seven central steps of the methanogenic reduction of carbon dioxide (CO(2)) are ubiquitous in methanogens and share a common history. This suggests that, although extant methanogens produce methane from various substrates (CO(2), formate, acetate, methylated C-1 compounds), these archaea have a core of conserved enzymes that have undergone little evolutionary change. Furthermore, this core of methanogenesis enzymes seems to originate (as a whole) from the last ancestor of all methanogens and does not appear to have been horizontally transmitted to other organisms or between members of Class I and Class II. The observation of a unique and ancestral form of methanogenesis suggests that it was preserved in two independent lineages, with some instances of specialization or added metabolic flexibility. It was likely lost in the Halobacteriales, Thermoplasmatales and Archaeoglobales. Given that fossil evidence for methanogenesis dates back 2.8 billion years, a unique origin of this process makes the methanogenic archaea a very ancient taxon.

Archaea↗

The timing of eukaryotic evolution: does a relaxed molecular clock reconcile proteins and fossils?

The use of nucleotide and amino acid sequences allows improved understanding of the timing of evolutionary events of life on earth. Molecular estimates of divergence times are, however, controversial and are generally much more ancient than suggested by the fossil record. The limited number of genes and species explored and pervasive variations in evolutionary rates are the most likely sources of such discrepancies. Here we compared concatenated amino acid sequences of 129 proteins from 36 eukaryotes to determine the divergence times of several major clades, including animals, fungi, plants, and various protists. Due to significant variations in their evolutionary rates, and to handle the uncertainty of the fossil record, we used a Bayesian relaxed molecular clock simultaneously calibrated by six paleontological constraints. We show that, according to 95% credibility intervals, the eukaryotic kingdoms diversified 950-1,259 million years ago (Mya), animals diverged from choanoflagellates 761-957 Mya, and the debated age of the split between protostomes and deuterostomes occurred 642-761 Mya. The divergence times appeared to be robust with respect to prior assumptions and paleontological calibrations. Interestingly, these relaxed clock time estimates are much more recent than those obtained under the assumption of a global molecular clock, yet bilaterian diversification appears to be approximately 100 million years more ancient than the Cambrian boundary.

Animals↗

Evolution of the RNA polymerase B' subunit gene (rpoB') in Halobacteriales: a complementary molecular marker to the SSU rRNA gene.

Many prokaryotes have multiple ribosomal RNA operons. Generally, sequence differences between small subunit (SSU) rRNA genes are minor (<1%) and cause little concern for phylogenetic inference or environmental diversity studies. For Halobacteriales, an order of extremely halophilic, aerobic Archaea, within-genome SSU rRNA sequence divergence can exceed 5%, rendering phylogenetic assignment problematic. The RNA polymerase B' subunit gene (rpoB') is a single-copy conserved gene that may be an appropriate alternative phylogenetic marker for Halobacteriales. We sequenced a fragment of the rpoB' gene from 21 species, encompassing 15 genera of Halobacteriales. To examine the utility of rpoB' as a phylogenetic marker in Halobacteriales, we investigated three properties of rpoB' trees: the variation in resolution between trees inferred from the rpoB' DNA and RpoB' protein alignment, the degree of mutational saturation between taxa, and congruence with the SSU rRNA tree. The rpoB' DNA and protein trees were for the most part congruent and consistently recovered two well-supported monophyletic groups, the clade I and clade II haloarchaea, within a collection of less well resolved Halobacteriales lineages. A comparison of observed versus inferred numbers of substitution revealed mutational saturation in the rpoB' DNA data set, particularly between more distant species. Thus, the RpoB' protein sequence may be more reliable than the rpoB' DNA sequence for inferring Halobacteriales phylogeny. AU tests of tree selection indicated the trees inferred from rpoB' DNA and protein alignments were significantly incongruent with the SSU rRNA tree. We discuss possible explanations for this incongruence, including tree reconstruction artifact, differential paralog sampling, and lateral gene transfer. This is the first study of Halobacteriales evolution based on a marker other than the SSU rRNA gene. In addition, we present a valuable phylogenetic framework encompassing a broad diversity of Halobacteriales, in which novel sequences can be inserted for evolutionary, ecological, or taxonomic investigations.

Base Sequence↗

Phylogenomics of eukaryotes: impact of missing data on large alignments.

Resolving the relationships between Metazoa and other eukaryotic groups as well as between metazoan phyla is central to the understanding of the origin and evolution of animals. The current view is based on limited data sets, either a single gene with many species (e.g., ribosomal RNA) or many genes but with only a few species. Because a reliable phylogenetic inference simultaneously requires numerous genes and numerous species, we assembled a very large data set containing 129 orthologous proteins ( approximately 30,000 aligned amino acid positions) for 36 eukaryotic species. Included in the alignments are data from the choanoflagellate Monosiga ovata, obtained through the sequencing of about 1,000 cDNAs. We provide conclusive support for choanoflagellates as the closest relative of animals and for fungi as the second closest. The monophyly of Plantae and chromalveolates was recovered but without strong statistical support. Within animals, in contrast to the monophyly of Coelomata observed in several recent large-scale analyses, we recovered a paraphyletic Coelamata, with nematodes and platyhelminths nested within. To include a diverse sample of organisms, data from EST projects were used for several species, resulting in a large amount of missing data in our alignment (about 25%). By using different approaches, we verify that the inferred phylogeny is not sensitive to these missing data. Therefore, this large data set provides a reliable phylogenetic framework for studying eukaryotic and animal evolution and will be easily extendable when large amounts of sequence information become available from a broader taxonomic range.

Animals↗

The genes encoding cAMP-dependent protein kinase catalytic subunit homologues of the microsporidia Encephalitozoon intestinalis and E. cuniculi: molecular characterisation and phylogenetic analysis.

A gene encoding a protein kinase was identified by homology-based PCR amplification in Encephalitozoon intestinalis, a microsporidian parasite pathogenic to humans, and its orthologue has been identified by database mining in the genome of the related species E. cuniculi, whose sequence has been recently published. Phylogenetic analysis revealed that the proteins encoded by these genes are homologues of the cAMP-dependent protein kinase catalytic subunits (PKAc). Southern blot analysis indicated that the EiPKAc gene is present in two copies in the E. intestinalis genome, whereas the E. cuniculi orthologue (EcPKAc) is a single copy gene. RT-PCR data showed that the EiPKAc gene is expressed in at least one of the intracellular stages during infection of the mammalian host cell by E. intestinalis.

Amino Acid Sequence↗

Phylogenetic reconstruction and lateral gene transfer.

Lateral gene transfer (LGT) is often seen as a form of noise, obscuring the phylogenetic signal with which we might hope to reconstruct the evolution of a group of organisms, or indeed the history of all life (the Tree of Life). Such reconstruction might still be possible if the subset of genes conserved among all genomes in a group (or common to all genomes) comprise a core that is relatively refractory to LGT. Several papers designed to test this notion have recently appeared, and here we re-analyze one, which claims that the core of single-copy orthologs shared by all sequenced genomes of the gammaproteobacteria is essentially free of LGT. This conclusion is unfortunately premature, and it is very hard to determine what fraction of this core has been affected by LGT. We discuss other difficulties with the core concept and suggest that, although the core idea must remain part of our understanding of phylogenetic relationships, it should not be the sole basis for defining such relationships, because these are not exclusively tree-like. We suggest instead a more complex but more natural framework for classification, which we call the Synthesis of Life.

Biological Evolution↗

Rampant horizontal gene transfer and phospho-donor change in the evolution of the phosphofructokinase.

Previous work on the evolution of the phosphofructokinase (PFK) has shown that this key regulatory enzyme of glycolysis has undergone an intricate evolutionary history. Here, we have used a comprehensive data set to address the taxonomic distribution of the different types of PFK (ATP-dependent and PPi-dependent ones) and to estimate the frequency of horizontal gene transfer (HGT) events. Numerous HGT events appear to have occurred. In addition, we focused on the analysis of sites 104 and 124 (usually Gly(104)+Gly(124) or Asp(104)+Lys(124)), known to be involved in catalysis (J. Biol. Chem. 275 (2000) 35677). It revealed the existence of numerous sequences from distantly related species carrying atypical combinations of amino acids. Several adaptive changes of phospho-donors, probably requiring a single mutation at position 104, have likely occurred independently in many lineages. The analysis of this gene suggests the existence of a high rate of both HGT and substitution in its active sites. These rampant HGT events and flexibility in phospho-donor use illustrate the importance of tinkering in molecular evolution.

Animals↗

The analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium, Entamoeba, and Mastigamoeba.

The phylogenetic relationships of amoebae are poorly resolved. To address this difficult question, we have sequenced 1,280 expressed sequence tags from Mastigamoeba balamuthi and assembled a large data set containing 123 genes for representatives of three phenotypically highly divergent major amoeboid lineages: Pelobionta, Entamoebidae, and Mycetozoa. Phylogenetic reconstruction was performed on approximately 25,000 aa positions for 30 species by using maximum-likelihood approaches. All well-established eukaryotic groups were recovered with high statistical support, validating our approach. Interestingly, the three amoeboid lineages strongly clustered together in agreement with the Conosa hypothesis [as defined by T. Cavalier-Smith (1998) Biol. Rev. Cambridge Philos. Soc. 73, 203-266]. Two amitochondriate amoebae, the free-living Mastigamoeba and the human parasite Entamoeba, formed a significant sister group to the exclusion of the mycetozoan Dictyostelium. This result suggested that a part of the reductive process in the evolution of Entamoeba (e.g., loss of typical mitochondria) occurred in its free-living ancestors. Applying this inexpensive expressed sequence tag approach to many other lineages will surely improve our understanding of eukaryotic evolution.

Amoeba↗

Eubacterial phylogeny based on translational apparatus proteins.

Lateral gene transfers are frequent among prokaryotes, although their detection remains difficult. If all genes are equally affected, this questions the very existence of an organismal phylogeny. The complexity hypothesis postulates the existence of a core of genes (those involved in numerous interactions) that are unaffected by transfers. To test the hypothesis, we studied all the proteins involved in translation from 45 eubacterial taxa, and developed a new phylogenetic method to detect transfers. Few of the genes studied show evidence for transfer. The phylogeny based on the genes devoid of transfer is very consistent with the ribosomal RNA tree, suggesting that an eubacterial phylogeny does exist.

Bacteria↗