Patterns Of Gene Loss Research Articles

Independent Genome Reduction and Phylogenetic Reclassification of the Oceanic SAR11 Clade

The SAR11 clade, here represented by Candidatus Pelagibacter ubique, is the most successful group of bacteria in the upper surface waters of the oceans. In contrast to previous studies that have associated the 1.3 Mb genome of Ca. Pelagibacter ubique with the less than 1.5 Mb genomes of the Rickettsiales, our phylogenetic analysis suggests that Ca. Pelagibacter ubique is most closely related to soil and aquatic Alphaproteobacteria with large genomes. This implies that the SAR11 clade and the Rickettsiales have undergone genome reduction independently. A gene flux analysis of 46 representative alphaproteobacterial genomes indicates the loss of more than 800 genes in each of Ca. Pelagibacter ubique and the Rickettsiales. Consistent with their different phylogenetic affiliations, the pattern of gene loss differs with a higher loss of genes for repair and recombination processes in Ca. Pelagibacter ubique as compared with a more extensive loss of genes for biosynthetic functions in the Rickettsiales. Some of the lost genes in Ca. Pelagibacter ubique, such as mutLS, recFN, and ruvABC, are conserved in all other alphaproteobacterial genomes including the small genomes of the Rickettsiales. The mismatch repair genes mutLS are absent from all currently sequenced SAR11 genomes and also underrepresented in the global ocean metagenome data set. We hypothesize that the unique loss of genes involved in repair and recombination processes in Ca. Pelagibacter ubique has been driven by selection and that this helps explain many of the characteristics of the SAR11 population, such as the streamlined genomes, the long branch lengths, the high recombination frequencies, and the extensive sequence divergence within the population.

Evaluating ortholog prediction algorithms in a yeast model clade.

BackgroundAccurate identification of orthologs is crucial for evolutionary studies and for functional annotation. Several algorithms have been developed for ortholog delineation, but so far, manually curated genome-scale biological databases of orthologous genes for algorithm evaluation have been lacking. We evaluated four popular ortholog prediction algorithms (MultiParanoid; and OrthoMCL; RBH: Reciprocal Best Hit; RSD: Reciprocal Smallest Distance; the last two extended into clustering algorithms cRBH and cRSD, respectively, so that they can predict orthologs across multiple taxa) against a set of 2,723 groups of high-quality curated orthologs from 6 Saccharomycete yeasts in the Yeast Gene Order Browser.ResultsExamination of sensitivity [TP/(TP+FN)], specificity [TN/(TN+FP)], and accuracy [(TP+TN)/(TP+TN+FP+FN)] across a broad parameter range showed that cRBH was the most accurate and specific algorithm, whereas OrthoMCL was the most sensitive. Evaluation of the algorithms across a varying number of species showed that cRBH had the highest accuracy and lowest false discovery rate [FP/(FP+TP)], followed by cRSD. Of the six species in our set, three descended from an ancestor that underwent whole genome duplication. Subsequent differential duplicate loss events in the three descendants resulted in distinct classes of gene loss patterns, including cases where the genes retained in the three descendants are paralogs, constituting ‘traps’ for ortholog prediction algorithms. We found that the false discovery rate of all algorithms dramatically increased in these traps.ConclusionsThese results suggest that simple algorithms, like cRBH, may be better ortholog predictors than more complex ones (e.g., OrthoMCL and MultiParanoid) for evolutionary and functional genomics studies where the objective is the accurate inference of single-copy orthologs (e.g., molecular phylogenetics), but that all algorithms fail to accurately predict orthologs when paralogy is rampant.

Phylogenomic Analysis of the Uracil-DNA Glycosylase Superfamily

The spontaneous deamination of cytosine produces uracil mispaired with guanine in DNA, which will produce a mutation, unless repaired. In all domains of life, uracil-DNA glycosylases (UDGs) are responsible for the elimination of uracil from DNA. Thus, UDGs contribute to the integrity of the genetic information and their loss results in mutator phenotypes. We are interested in understanding the role of UDG genes in the evolutionary variation of the rate and the spectrum of spontaneous mutations. To this end, we determined the presence or absence of the five main UDG families in more than 1,000 completely sequenced genomes and analyzed their patterns of gene loss and gain in eubacterial lineages. We observe nonindependent patterns of gene loss and gain between UDG families in Eubacteria, suggesting extensive functional overlap in an evolutionary timescale. Given that UDGs prevent transitions at G:C sites, we expected the loss of UDG genes to bias the mutational spectrum toward a lower equilibrium G + C content. To test this hypothesis, we used phylogenetically independent contrasts to compare the G + C content at intergenic and 4-fold redundant sites between lineages where UDG genes have been lost and their sister clades. None of the main UDG families present in Eubacteria was associated with a higher G + C content at intergenic or 4-fold redundant sites. We discuss the reasons of this negative result and report several features of the evolution of the UDG superfamily with implications for their functional study. uracil-DNA glycosylase, mutation rate evolution, mutational bias, GC content, DNA repair, mutator gene.

15-P003 An EST screen from the annelid Pomatoceros lamarckii reveals patterns of gene loss and gain in animals

15-P003 An EST screen from the annelid Pomatoceros lamarckii reveals patterns of gene loss and gain in animals

Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids

Whole-genome duplication (polyploidisation) is a widespread mechanism of speciation in plants. Over time, polyploid genomes tend towards a more diploid-like state, through downsizing and loss of duplicated genes (homoeologues), but relatively little is known about the timing of gene loss during polyploid formation and stabilisation. Several studies have also shown gene transcription to be affected by polyploidisation. Here, we examine patterns of gene loss in 10 sets of homoeologues in five natural populations of the allotetraploid Tragopogon miscellus that arose within the past 80 years following independent whole-genome duplication events. We also examine 44 first-generation synthetic allopolyploids of the same species. No cases of homoeologue loss arose in the first allopolyploid generation, but after 80 years, 1.6% of homoeologues were lost in natural populations. For seven homoeologue sets we also examined transcription, finding that 3.4% of retained homoeologues had been silenced in the natural populations, but none in the synthetic plants. The homoeologue losses and silencing events found were not fixed within natural populations and did not form a predictable pattern among populations. We therefore show haphazard loss and silencing of homoeologues, occurring within decades of polyploid formation in T. miscellus, but not in the initial generation.

An EST screen from the annelid Pomatoceros lamarckii reveals patterns of gene loss and gain in animals

BackgroundSince the drastic reorganisation of the phylogeny of the animal kingdom into three major clades of bilaterians; Ecdysozoa, Lophotrochozoa and Deuterostomia, it became glaringly obvious that the selection of model systems with extensive molecular resources was heavily biased towards only two of these three clades, namely the Ecdysozoa and Deuterostomia. Increasing efforts have been put towards redressing this imbalance in recent years, and one of the principal phyla in the vanguard of this endeavour is the Annelida.ResultsIn the context of this effort we here report our characterisation of an Expressed Sequence Tag (EST) screen in the serpulid annelid, Pomatoceros lamarckii. We have sequenced over 5,000 ESTs which consolidate into over 2,000 sequences (clusters and singletons). These sequences are used to build phylogenetic trees to estimate relative branch lengths amongst different taxa and, by comparison to genomic data from other animals, patterns of gene retention and loss are deduced.ConclusionThe molecular phylogenetic trees including the P. lamarckii sequences extend early observations that polychaetes tend to have relatively short branches in such trees, and hence are useful taxa with which to reconstruct gene family evolution. Also, with the availability of lophotrochozoan data such as that of P. lamarckii, it is now possible to make much more accurate reconstructions of the gene complement of the ancestor of the bilaterians than was previously possible from comparisons of ecdysozoan and deuterostome genomes to non-bilaterian outgroups. It is clear that the traditional molecular model systems for protostomes (e.g. Drosophila melanogaster and Caenorhabditis elegans), which are restricted to the Ecdysozoa, have undergone extensive gene loss during evolution. These ecdysozoan systems, in terms of gene content, are thus more derived from the bilaterian ancestral condition than lophotrochozoan systems like the polychaetes, and thus cannot be used as good, general representatives of protostome genomes. Currently sequenced insect and nematode genomes are less suitable models for deducing bilaterian ancestral states than lophotrochozoan genomes, despite the array of powerful genetic and mechanistic manipulation techniques in these ecdysozoans. A distinct category of genes that includes those present in non-bilaterians and lophotrochozoans, but which are absent from ecdysozoans and deuterostomes, highlights the need for further lophotrochozoan data to gain a more complete understanding of the gene complement of the bilaterian ancestor.

The gene complement of the ancestral bilaterian - was Urbilateria a monster?

Expressed sequence tag analyses of the annelid Pomatoceros lamarckii, recently published in BMC Evolutionary Biology, are consistent with less extensive gene loss in the Lophotrochozoa than in the Ecdysozoa, but it would be premature to generalize about patterns of gene loss on the basis of the limited data available.See research article http://www.biomedcentral.com/1471-2148/9/240.

Temporal pattern of loss/persistence of duplicate genes involved in signal transduction and metabolic pathways after teleost-specific genome duplication

BackgroundRecent genomic studies have revealed a teleost-specific third-round whole genome duplication (3R-WGD) event occurred in a common ancestor of teleost fishes. However, it is unclear how the genes duplicated in this event were lost or persisted during the diversification of teleosts, and therefore, how many of the duplicated genes contribute to the genetic differences among teleosts. This subject is also important for understanding the process of vertebrate evolution through WGD events. We applied a comparative evolutionary approach to this question by focusing on the genes involved in long-term potentiation, taste and olfactory transduction, and the tricarboxylic acid cycle, based on the whole genome sequences of four teleosts; zebrafish, medaka, stickleback, and green spotted puffer fish.ResultsWe applied a state-of-the-art method of maximum-likelihood phylogenetic inference and conserved synteny analyses to each of 130 genes involved in the above biological systems of human. These analyses identified 116 orthologous gene groups between teleosts and tetrapods, and 45 pairs of 3R-WGD-derived duplicate genes among them. This suggests that more than half [(45×2)/(116+45)] = 56.5%) of the loci, probably more than ten thousand genes, present in a common ancestor of the four teleosts were still duplicated after the 3R-WGD. The estimated temporal pattern of gene loss suggested that, after the 3R-WGD, many (71/116) of the duplicated genes were rapidly lost during the initial 75 million years (MY), whereas on average more than half (27.3/45) of the duplicated genes remaining in the ancestor of the four teleosts (45/116) have persisted for about 275 MY. The 3R-WGD-derived duplicates that have persisted for a long evolutionary periods of time had significantly larger number of interacting partners and longer length of protein coding sequence, implying that they tend to be more multifunctional than the singletons after the 3R-WGD.ConclusionWe have shown firstly the temporal pattern of gene loss process after 3R-WGD on the basis of teleost phylogeny and divergence time frameworks. The 3R-WGD-derived duplicates have not undergone constant exponential decay, suggesting that selection favoured the long-term persistence of a subset of duplicates that tend to be multi-functional. On the basis of these results obtained from the analysis of 116 orthologous gene groups, we propose that more than ten thousand of 3R-WGD-derived duplicates have experienced lineage-specific evolution, that is, the differential sub-/neo-functionalization or secondary loss between lineages, and contributed to teleost diversity.

The Role of Mutational Dynamics in Genome Shrinkage

Genome shrinkage occurs after whole genome duplications (WGDs) and in the evolution of parasitic or symbiotic species. The dynamics of this process, whether it occurs by single gene deletions or also by larger deletions are however unknown. In yeast, genome shrinkage has occurred after a WGD. Using a computational model of genome evolution, we show that in a random genome single gene deletions cannot explain the observed pattern of gene loss in yeast. The distribution of genes deleted per event can be very well described by a geometric distribution, with a mean of 1.1 genes per event. In terms of deletions of a stretch of base pairs, we find that a geometric distribution with an average of 500-600 base pairs per event describes the data very well. Moreover, in the model, as in the data, gene pairs that have a small intergenic distance are more likely to be both deleted. This proves that simultaneous deletion of multiple genes causes the observed pattern of gene deletions, rather than deletion of functionally clustered genes by selection. Furthermore, we found that in the bacterium Buchnera aphidicola larger deletions than in yeast are necessary to explain the clustering of deleted genes. We show that the excess clustering of deleted genes in B. aphidicola can be explained by the clustering of genes in operons. Therefore, we show that selection has little effect on the clustering of deleted genes after the WGD in yeast, while it has during genome shrinkage in B. aphidicola.

Independent sorting-out of thousands of duplicated gene pairs in two yeast species descended from a whole-genome duplication.

Among yeasts that underwent whole-genome duplication (WGD), Kluyveromyces polysporus represents the lineage most distant from Saccharomyces cerevisiae. By sequencing the K. polysporus genome and comparing it with the S. cerevisiae genome using a likelihood model of gene loss, we show that these species diverged very soon after the WGD, when their common ancestor contained >9,000 genes. The two genomes subsequently converged onto similar current sizes (5,600 protein-coding genes each) and independently retained sets of duplicated genes that are strikingly similar. Almost half of their surviving single-copy genes are not orthologs but paralogs formed by WGD, as would be expected if most gene pairs were resolved independently. In addition, by comparing the pattern of gene loss among K. polysporus, S. cerevisiae, and three other yeasts that diverged after the WGD, we show that the patterns of gene loss changed over time. Initially, both members of a duplicate pair were equally likely to be lost, but loss of the same gene copy in independent lineages was increasingly favored at later time points. This trend parallels an increasing restriction of reciprocal gene loss to more slowly evolving gene pairs over time and suggests that, as duplicate genes diverged, one gene copy became favored over the other. The apparent low initial sequence divergence of the gene pairs leads us to propose that the yeast WGD was probably an autopolyploidization.

Origins of amino acid transporter loci in trypanosomatid parasites

BackgroundLarge amino acid transporter gene families were identified from the genome sequences of three parasitic protists, Trypanosoma brucei, Trypanosoma cruzi and Leishmania major. These genes encode molecular sensors of the external host environment for trypanosomatid cells and are crucial to modulation of gene expression as the parasite passes through different life stages. This study provides a comprehensive phylogenetic account of the origins of these genes, redefining each locus according to a positional criterion, through the integration of phyletic identity with comparative gene order information.ResultsEach locus was individually specified by its surrounding gene order and associated with homologs showing the same position ('homoeologs') in other species, where available. Bayesian and maximum likelihood phylogenies were in general agreement on systematic relationships and confirmed several 'orthology sets' of genes retained since divergence from the common ancestor. Reconciliation analysis quantified the scale of duplication and gene loss, as well as identifying further apparent orthology sets, which lacked conservation of genomic position. These instances suggested substantial genomic restructuring or transposition. Other analyses identified clear instances of evolutionary rate changes post-duplication, the effects of concerted evolution within tandem gene arrays and gene conversion events between syntenic loci.ConclusionDespite their importance to cell function and parasite development, the repertoires of AAT loci in trypanosomatid parasites are relatively fluid in both complement and gene dosage. Some loci are ubiquitous and, after an ancient origin through transposition, originated through descent from the ancestral trypanosomatid. However, reconciliation analysis demonstrated that unilateral expansions of gene number through tandem gene duplication, transposition of gene duplicates to otherwise well conserved genomic positions, and differential patterns of gene loss have produced largely customised and idiosyncratic AAT repertoires in all three species. Not least in T. brucei, which seems to have retained fewer ancestral loci and has acquired novel loci through a complex mix of tandem and transpositive duplication.

Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia

The duplication of entire genomes has long been recognized as having great potential for evolutionary novelties, but the mechanisms underlying their resolution through gene loss are poorly understood. Here we show that in the unicellular eukaryote Paramecium tetraurelia, a ciliate, most of the nearly 40,000 genes arose through at least three successive whole-genome duplications. Phylogenetic analysis indicates that the most recent duplication coincides with an explosion of speciation events that gave rise to the P. aurelia complex of 15 sibling species. We observed that gene loss occurs over a long timescale, not as an initial massive event. Genes from the same metabolic pathway or protein complex have common patterns of gene loss, and highly expressed genes are over-retained after all duplications. The conclusion of this analysis is that many genes are maintained after whole-genome duplication not because of functional innovation but because of gene dosage constraints.

Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts

A whole-genome duplication occurred in a shared ancestor of the yeast species Saccharomyces cerevisiae, Saccharomyces castellii and Candida glabrata. Here we trace the subsequent losses of duplicated genes, and show that the pattern of loss differs among the three species at 20% of all loci. For example, several transcription factor genes, including STE12, TEC1, TUP1 and MCM1, are single-copy in S. cerevisiae but are retained in duplicate in S. castellii and C. glabrata. At many loci, different species have lost different members of a duplicated gene pair, so that 4-7% of single-copy genes compared between any two species are not orthologues. This pattern of gene loss provides strong evidence for speciation through a version of the Bateson-Dobzhansky-Muller mechanism, in which the loss of alternative copies of duplicated genes leads to reproductive isolation. We show that the lineages leading to the three species diverged shortly after the whole-genome duplication, during a period of precipitous gene loss. The set of loci at which single-copy paralogues are retained is biased towards genes involved in ribosome biogenesis and genes that evolve slowly, consistent with the hypothesis that reciprocal gene loss is more likely to occur between duplicated genes that are functionally indistinguishable. We propose a simple, unified model in which a single mechanism--passive gene loss-enabled whole--genome duplication and led to the rapid emergence of new yeast species.

The Complete Genome Sequence and Comparative Genome Analysis of the High Pathogenicity Yersinia enterocolitica Strain 8081

The human enteropathogen, Yersinia enterocolitica, is a significant link in the range of Yersinia pathologies extending from mild gastroenteritis to bubonic plague. Comparison at the genomic level is a key step in our understanding of the genetic basis for this pathogenicity spectrum. Here we report the genome of Y. enterocolitica strain 8081 (serotype 0:8; biotype 1B) and extensive microarray data relating to the genetic diversity of the Y. enterocolitica species. Our analysis reveals that the genome of Y. enterocolitica strain 8081 is a patchwork of horizontally acquired genetic loci, including a plasticity zone of 199 kb containing an extraordinarily high density of virulence genes. Microarray analysis has provided insights into species-specific Y. enterocolitica gene functions and the intraspecies differences between the high, low, and nonpathogenic Y. enterocolitica biotypes. Through comparative genome sequence analysis we provide new information on the evolution of the Yersinia. We identify numerous loci that represent ancestral clusters of genes potentially important in enteric survival and pathogenesis, which have been lost or are in the process of being lost, in the other sequenced Yersinia lineages. Our analysis also highlights large metabolic operons in Y. enterocolitica that are absent in the related enteropathogen, Yersinia pseudotuberculosis, indicating major differences in niche and nutrients used within the mammalian gut. These include clusters directing, the production of hydrogenases, tetrathionate respiration, cobalamin synthesis, and propanediol utilisation. Along with ancestral gene clusters, the genome of Y. enterocolitica has revealed species-specific and enteropathogen-specific loci. This has provided important insights into the pathology of this bacterium and, more broadly, into the evolution of the genus. Moreover, wider investigations looking at the patterns of gene loss and gain in the Yersinia have highlighted common themes in the genome evolution of other human enteropathogens.

GeneContent: software for whole-genome phylogenetic analysis

GeneContent is a software system to infer the genome phylogeny based on an additive genome distance that can be estimated from the extended gene content data, which contains the genome-wide information (absence of a gene family, presence as single copy or presence as duplicates) across multiple species. GeneContent can also be used to explore the genome-wide evolutionary pattern of gene loss and proliferation. Distribution packages of GeneContent for both Microsoft Windows and Linux operating systems are available at http://xgu.zool.iastate.edu xgu@iastate.edu.

The Case for a Single‐Plastid Origin Revisited: Convergent Evolution in Organellar Gene Content

AbstractThree eukaryotic lineages generally are believed to have plastids that are primary in origin; that is, descended directly from a cyanobacterial endosymbiont. The recovery of these plastids as a monophyletic group in most molecular phylogenetic analyses, along with similarities in genome content and protein targeting mechanisms, have been cited as strong evidence in support of the hypothesis of a single endosymbiotic origin of all plastids. Although these data indeed are consistent with a single plastid origin, they also are consistent with the proposition of multiple endosymbiotic origins. Each hypothesis requires certain evolutionary assumptions in order to be reconciled with all existing data; at present, it is unclear which of these assumptions most likely reflect the historical process that gave rise to plastid diversity. Here we examine similarities in gene content among representatives of the three primary plastid lineages, using as a control the genome of a mitochondrion that almost certainly originated as an independent endosymbiotic association. To minimize metabolic constraints on gene retention we focus on two datasets, ribosomal protein and transfer RNA genes, neither of which is tied directly to specific organellar functions. Analyses of all possible pair‐wise comparisons among the three plastids and mitochondrion indicate that genomic similarities are most consistent with convergent evolution due to constraints on gene loss, rather than with hypothesized shared evolutionary histories. We find no evidence of phylogenetic signal in the pattern of gene loss overlying this convergence. In light of these results, we address other lines of evidence and arguments that have been raised in support of a single plastid origin.

Comparable rates of gene loss and functional divergence after genome duplications early in vertebrate evolution.

Duplicated genes are an important source of new protein functions and novel developmental and physiological pathways. Whereas most models for fate of duplicated genes show that they tend to be rapidly lost, models for pathway evolution suggest that many duplicated genes rapidly acquire novel functions. Little empirical evidence is available, however, for the relative rates of gene loss vs. divergence to help resolve these contradictory expectations. Gene families resulting from genome duplications provide an opportunity to address this apparent contradiction. With genome duplication, the number of duplicated genes in a gene family is at most 2n, where n is the number of duplications. The size of each gene family, e.g., 1, 2, 3, ..., 2n, reflects the patterns of gene loss vs. functional divergence after duplication. We focused on gene families in humans and mice that arose from genome duplications in early vertebrate evolution and we analyzed the frequency distribution of gene family size, i.e., the number of families with two, three or four members. All the models that we evaluated showed that duplicated genes are almost as likely to acquire a new and essential function as to be lost through acquisition of mutations that compromise protein function. An explanation for the unexpectedly high rate of functional divergence is that duplication allows genes to accumulate more neutral than disadvantageous mutations, thereby providing more opportunities to acquire diversified functions and pathways.