Yeasts illustrate the molecular mechanisms of eukaryotic genome evolution

Hemiascomycetous yeasts have the greatest number of sequenced species for a single phylum, and are at the forefront of evolutionary genomics of eukaryotes. Yeast genomes show the dynamic interplay between the formation and loss of genes and help to characterize the mechanisms involved and their functional and evolutionary consequences. These mechanisms have equivalents in the genomes of multicellular organisms. Yeast genomes show extensive loss of introns and a reduced role of transposable elements, and so probably have a more limited potential to form novel genes and functions than multicellular organisms, possibly explaining their conserved biological and morphological properties despite their considerable evolutionary range.     

Two-stepping through time: mammals and viruses

Recent studies have identified ancient virus genomes preserved as fossils within diverse animal genomes. These fossils have led to the revelation that a broad range of mammalian virus families are older and more ubiquitous than previously appreciated. Long-term interactions between viruses and their hosts often develop into genetic arms races where both parties continually jockey for evolutionary dominance. It is difficult to imagine how mammalian hosts have kept pace in the evolutionary race against rapidly evolving viruses over large expanses of time, given their much slower evolutionary rates. However, recent data has begun to reveal the evolutionary strategy of slowly-evolving hosts. We review these data and suggest a modified arms race model where the evolutionary possibilities of viruses are relatively constrained. Such a model could allow more accurate forecasting of virus evolution.     

Evolutionarily conserved orthologous families in phages are relatively rare in their prokaryotic hosts

We have identified conserved orthologs in completely sequenced genomes of double-strand DNA phages and arranged them into evolutionary families (phage orthologous groups [POGs]). Using this resource to analyze the collection of known phage genomes, we find that most orthologs are unique in their genomes (having no diverged duplicates [paralogs]), and while many proteins contain multiple domains, the evolutionary recombination of these domains does not appear to be a major factor in evolution of these orthologous families. The number of POGs has been rapidly increasing over the past decade, the percentage of genes in phage genomes that have orthologs in other phages has also been increasing, and the percentage of unknown "ORFans" is decreasing as more proteins find homologs and establish a family. Other properties of phage genomes have remained relatively stable over time, most notably the high fraction of genes that are never or only rarely observed in their cellular hosts. This suggests that despite the renowned ability of phages to transduce cellular genes, these cellular "hitchhiker" genes do not dominate the phage genomic landscape, and a large fraction of the genes in phage genomes maintain an evolutionary trajectory that is distinct from that of the host genes.     

Hemiascomycetous yeasts at the forefront of comparative genomics

With more than a dozen species fully sequenced, as many as this partially sequenced, and more in development, yeasts are now used to explore the frontlines of comparative genomics of eukaryotes. Innovative procedures have been developed to compare and annotate genomes at various evolutionary distances, to identify short cis-acting regulatory elements, to map duplications, or to align syntenic blocks. Human and plant pathogens, in addition to yeasts that show a variety of interesting physiological properties, are included in this multidimensional comparative survey, which encompasses a very broad evolutionary range. As major steps of the evolutionary history of hemiascomycetous genomes emerge, precise questions on the general mechanisms of their evolution can be addressed, using both experimental and in silico methods.     

Comparative genomics and evolution of the tailed-bacteriophages

The number of completely sequenced tailed-bacteriophage genomes that have been published increased to more than 125 last year. The comparison of these genomes has brought their highly mosaic nature into much sharper focus. Furthermore, reports of the complete sequences of about 150 bacterial genomes have shown that the many prophage and parts thereof that reside in these bacterial genomes must comprise a significant fraction of Earth's phage gene pool. These phage and prophage genomes are fertile ground for attempts to deduce the nature of viral evolutionary processes, and such analyses have made it clear that these phage have enjoyed a significant level of horizontal exchange of genetic information throughout their long histories. The strength of these evolutionary deductions rests largely on the extensive knowledge that has accumulated during intensive study into the molecular nature of the life cycles of a few 'model system' phages over the past half century. Recent molecular studies of phages other than these model system phages have made it clear that much remains to be learnt about the variety of lifestyle strategies utilized by the tailed-phage.     

Comparative genomics and the evolution of prokaryotes

Although biologists have long recognized the importance of studying evolution to understand the organization of living organisms, only with the development of genomics have evolutionary studies become part of their routine toolkit. Placing genomes into an evolutionary framework has proved useful for understanding the functioning of organisms. It has also substantially increased understanding of the processes by which genomes evolve and led to a re-evaluation of our representation of the diversity and the history of life. In this review, we present some of the most important recent advances and promising leads in the field of microbial evolutionary genomics.     

A new genomic evolutionary model for rearrangements, duplications, and losses that applies across eukaryotes and prokaryotes

Genomic rearrangements have been studied since the beginnings of modern genetics and models for such rearrangements have been the subject of many papers over the last 10 years. However, none of the extant models can predict the evolution of genomic organization into circular unichromosomal genomes (as in most prokaryotes) and linear multichromosomal genomes (as in most eukaryotes). Very few of these models support gene duplications and losses--yet these events may be more common in evolutionary history than rearrangements and themselves cause apparent rearrangements. We propose a new evolutionary model that integrates gene duplications and losses with genome rearrangements and that leads to genomes with either one (or a very few) circular chromosome or a collection of linear chromosomes. Our model is based on existing rearrangement models and inherits their linear-time algorithms for pairwise distance computation (for rearrangement only). Moreover, our model predictions fit observations about the evolution of gene family sizes and agree with the existing predictions about the growth in the number of chromosomes in eukaryotic genomes.     

Phylogenomics and the reconstruction of the tree of life

As more complete genomes are sequenced, phylogenetic analysis is entering a new era - that of phylogenomics. One branch of this expanding field aims to reconstruct the evolutionary history of organisms on the basis of the analysis of their genomes. Recent studies have demonstrated the power of this approach, which has the potential to provide answers to several fundamental evolutionary questions. However, challenges for the future have also been revealed. The very nature of the evolutionary history of organisms and the limitations of current phylogenetic reconstruction methods mean that part of the tree of life might prove difficult, if not impossible, to resolve with confidence.     

Applying mobile genetic elements for genome analysis and evolution

Transposable elements (TEs) are ubiquitous components of all living organisms, and in the course of their coexistence with their respective host geneomes, these parasitc DNAs have played important roles in the evolution of complex genetic networks. The interaction between mobile DNAs and their host genomes are quite diverse, ranging from modifications of gene structure and regulation to alterations in general genome architecture. Thus during evolutionary time these elements can be regarded as natural molecular tools in shaping the organization, structure, and function of eukaryotic genes and genomes. Based on their intrinsic properties and features, mobile DNAs are widely applied at present as a technical “toolbox”, essential for studying a diverse spectrum of biological questions. In this review, we aim to summarize both the evolutionary impact of TEs on geneome evolution and their valuable and diverse methodological applications as molecular tools.     

DETECTING EVOLUTIONARY TRANSFER OF GENES USING PhIGs1

Organisms have acquired plastids by convoluted paths that have provided multiple opportunities for gene transfer into a host nucleus from intracellular organisms, including the cyanobacterial ancestor of plastids, the proteobacterial ancestor of mitochondria, and both green and red algae whose engulfment has led to secondary acquisition of plastids. These gene movements are most accurately demonstrated by building phylogenetic trees that identify the evolutionary origin of each gene, and one effective tool for this is “PhIGs” (Phylogenetically Inferred Groups; http://PhIGs.org ), a set of databases and computer tools with a Web interface for whole‐genome evolutionary analysis. PhIGs takes as input gene sets of completely sequenced genomes, builds clusters of genes using a novel, graph‐based approach, and reconstructs the evolutionary relationships among all gene families. The user can view and download the sequence alignments, compare intron‐exon structures, and follow links to functional genomic databases. Currently, PhIGs contains 652,756 genes from 45 genomes grouped into 61,059 gene families. Graphical displays show the relative positions of these genes among genomes. PhIGs has been used to detect the evolutionary transfer of hundreds of genes from cyanobacteria and red algae into oömycete nuclear genomes, revealing that even though they have no plastids, their ancestors did, having secondarily acquired them from an intracellular red alga. A great number of genomes are soon to become available that are relevant to our broader understanding of the movement of genes among intracellular compartments after engulfing other organisms, and PhIGs will be an effective tool to interpret these gene movements.     

Evolution of Red Algal Plastid Genomes: Ancient Architectures,Introns, Horizontal Gene Transfer,and Taxonomic Utility of Plastid Markers

Red algae have the most gene-rich plastid genomes known, but despite their evolutionary importance these genomes remain poorly sampled. Here we characterize three complete and one partial plastid genome from a diverse range of florideophytes. By unifying annotations across all available red algal plastid genomes we show they all share a highly compact and slowly-evolving architecture and uniquely rich gene complements. Both chromosome structure and gene content have changed very little during red algal diversification, and suggest that plastid-to nucleus gene transfers have been rare. Despite their ancient character, however, the red algal plastids also contain several unprecedented features, including a group II intron in a tRNA-Met gene that encodes the first example of red algal plastid intron maturase – a feature uniquely shared among florideophytes. We also identify a rare case of a horizontally-acquired proteobacterial operon, and propose this operon may have been recruited for plastid function and potentially replaced a nucleus-encoded plastid-targeted paralogue. Plastid genome phylogenies yield a fully resolved tree and suggest that plastid DNA is a useful tool for resolving red algal relationships. Lastly, we estimate the evolutionary rates among more than 200 plastid genes, and assess their usefulness for species and subspecies taxonomy by comparison to well-established barcoding markers such as cox1 and rbcL. Overall, these data demonstrates that red algal plastid genomes are easily obtainable using high-throughput sequencing of total genomic DNA, interesting from evolutionary perspectives, and promising in resolving red algal relationships at evolutionarily-deep and species/subspecies levels.     

On the need for integrative phylogenomics,and some steps toward its creation

Recently improved understanding of evolutionary processes suggests that tree-based phylogenetic analyses of evolutionary change cannot adequately explain the divergent evolutionary histories of a great many genes and gene complexes. In particular, genetic diversity in the genomes of prokaryotes, phages, and plasmids cannot be fit into classic tree-like models of evolution. These findings entail the need for fundamental reform of our understanding of molecular evolution and the need to devise alternative apparatus for integrated analysis of these genomes. We advocate the development of integrative phylogenomics for analyzing these genomes and their histories, with tools suited to analyzing the importance of lateral gene transfer (LGT) and of DNA evolution in extra-cellular mobile genetic elements (e.g., viruses, plasmids). These phenomena greatly increase the complexity of relationships among interacting genetic partners, as they exchange functional genetic units. We examine the ontology of functional genetic units, interacting genetic partners, and emergent genetic associations, argue that these three categories of entities are required for a successful integrated phylogenomics. We conclude with arguments to suggest that the proposed new perspective and associated tools are suitable, and perhaps required, as a replacement for the bifurcating trees that have dominated evolutionary thinking for the last 150 years.     

Fitting the niche by genomic adaptation

Studying microbial genomics has shown that the genomes of bacteria are extremely dynamic in evolutionary terms. Many research groups have linked the adaptation of an organism to a niche to large changes in genome size and content. A number of recent papers have underlined the degree to which the genomes of different organisms are a reflection of the opportunities and constraints imposed by their chosen niche.     

Giant viruses in the oceans: the 4th Algal Virus Workshop

Giant double-stranded DNA viruses (such as record breaking Acanthamoeba polyphaga Mimivirus), with particle sizes of 0.2 to 0.6 μm, genomes of 300 kbp to 1.200 kbp, and commensurate complex gene contents, constitute an evolutionary mystery. They challenge the common vision of viruses, traditionally seen as highly streamlined genomes optimally fitted to the smallest possible -filterable- package. Such giant viruses are now discovered in increasing numbers through the systematic sampling of ocean waters as well as freshwater aquatic environments, where they play a significant role in controlling phyto- and bacterio- plankton populations. The 4^th algal virus workshop showed that the study of these ecologically important viruses is now massively entering the genomic era, promising a better understanding of their diversity and, hopefully, some insights on their origin and the evolutionary forces that shaped their genomes.     

Mitochondrial genomes of two luminous beetles, Rhagophthalmus lufengensis and R. ohbai (Arthropoda, Insecta, Coleoptera)

We determined the mitochondrial DNA (mtDNA) sequences of two luminous beetles (Arthropoda, Insecta, Coleoptera), Rhagophthalmus lufengensis from Yunnan, China and Rhagophthalmus ohbai from Yaeyama Island, Japan. We identified all the 37 mtDNA genes of R. lufengensis (15,982 bp) and the 34 genes of R. ohbai (15,704 bp). R. lufengensis and R. ohbai genomes have higher A + T contents than other coleopteran genomes although the gene arrangements are similar. Interestingly, in a study of the evolutionary relationship among R. lufengensis, R. ohbai and the firefly Pyrocoelia rufa, the phylogenetic tree inferred from lrRNA genes from mitochondrial genomes indicates a biogeographic relationship among the bioluminescent insects in East Asia and the phylogenetic tree inferred from luciferase-related genes from nuclear genomes shows an appropriate relationship among coleopterans, reflecting the evolutionary origin of bioluminescence. Thus, the mtDNAs of luminescent beetles can provide an insight into their evolutionary origin and biogeography.     

Estimation of the true evolutionary distance under the fragile breakage model

Background

The ability to estimate the evolutionary distance between extant genomes plays a crucial role in many phylogenomic studies. Often such estimation is based on the parsimony assumption, implying that the distance between two genomes can be estimated as the rearrangement distance equal the minimal number of genome rearrangements required to transform one genome into the other. However, in reality the parsimony assumption may not always hold, emphasizing the need for estimation that does not rely on the rearrangement distance. The distance that accounts for the actual (rather than minimal) number of rearrangements between two genomes is often referred to as the true evolutionary distance. While there exists a method for the true evolutionary distance estimation, it however assumes that genomes can be broken by rearrangements equally likely at any position in the course of evolution. This assumption, known as the random breakage model, has recently been refuted in favor of the more rigorous fragile breakage model postulating that only certain “fragile” genomic regions are prone to rearrangements.

Results

We propose a new method for estimating the true evolutionary distance between two genomes under the fragile breakage model. We evaluate the proposed method on simulated genomes, which show its high accuracy. We further apply the proposed method for estimation of evolutionary distances within a set of five yeast genomes and a set of two fish genomes.

Conclusions

The true evolutionary distances between the five yeast genomes estimated with the proposed method reveals that some pairs of yeast genomes violate the parsimony assumption. The proposed method further demonstrates that the rearrangement distance between the two fish genomes underestimates their evolutionary distance by about 20%. These results demonstrate how drastically the two distances can differ and justify the use of true evolutionary distance in phylogenomic studies.

     

Accelerated pseudogenization of trace amine‐associated receptor genes in primates

Trace amines (TAs) in the mammalian brain have been investigated for four decades. Trace amine‐associated receptors (TAARs) were discovered during the search for receptors activated by TAs. TAARs are considered a second class of vertebrate olfactory receptors and successfully proliferated in conjunction with adaptation to living on the ground to detect carnivore odors. Thus, therian mammals have a high number of TAAR genes due to rapid species‐specific gene duplications. In primate lineages, however, their genomes have significantly smaller numbers of TAAR genes than do other mammals. To elucidate the evolutionary force driving these patterns, exhaustive data mining of TAAR genes was performed for 13 primate genomes (covering all four infraorders) and two nonprimate euarchontan genomes. This study identified a large number of pseudogenes in many of these primate genomes and thus investigated the pseudogenization event process for the TAAR repertoires. The degeneration of TAARs is likely associated with arboreal inhabitants reducing their exposure to carnivores, and this was accelerated by the change in the nose shape of haplorhines after their divergence from strepsirrhines. Arboreal life may have decreased the reliance on the chemosensing of predators, suggestive of leading to the depauperation of TAAR subfamilies. The evolutionary deterioration of TAARs in primates has been reestablished in recently derived primates due to high selection pressure and probably functional diversity.     

Integrons: mobilizable platforms that promote genetic diversity in bacteria

Integrons facilitate the capture of potentially adaptive exogenous genetic material by their host genomes. It is now clear that integrons are not limited to the clinical contexts in which they were originally discovered because approximately 10% of bacterial genomes that have been partially or completely sequenced harbour this genetic element. This wealth of sequence information has revealed that integrons are not only much more phylogenetically diverse than previously thought but also more mobilizable, with many integrons having been subjected to frequent lateral gene transfer throughout their evolutionary history. This indicates that the genetic characteristics that make integrons such efficient vectors for the spread of antibiotic resistance genes have been associated with these elements since their earliest origins. Here, we give an overview of the structural and phylogenetic diversity of integrons and describe evolutionary events that have contributed to the success of these genetic elements.     

Comprehensive analysis of endogenous bornavirus-like elements in eukaryote genomes

Bornaviruses are the only animal RNA viruses that establish a persistent infection in their host cell nucleus. Studies of bornaviruses have provided unique information about viral replication strategies and virus–host interactions. Although bornaviruses do not integrate into the host genome during their replication cycle, we and others have recently reported that there are DNA sequences derived from the mRNAs of ancient bornaviruses in the genomes of vertebrates, including humans, and these have been designated endogenous borna-like (EBL) elements. Therefore, bornaviruses have been interacting with their hosts as driving forces in the evolution of host genomes in a previously unexpected way. Studies of EBL elements have provided new models for virology, evolutionary biology and general cell biology. In this review, we summarize the data on EBL elements including what we have newly identified in eukaryotes genomes, and discuss the biological significance of EBL elements, with a focus on EBL nucleoprotein elements in mammalian genomes. Surprisingly, EBL elements were detected in the genomes of invertebrates, suggesting that the host range of bornaviruses may be much wider than previously thought. We also review our new data on non-retroviral integration of Borna disease virus.     

Intense transpositional activity of insertion sequences in an ancient obligate endosymbiont

The streamlined genomes of ancient obligate endosymbionts generally lack transposable elements, such as insertion sequences (IS). Yet, the genome of Wolbachia, one of the most abundant bacterial endosymbionts on Earth, is littered with IS. Such a paradox raises the question as to why there are so many ISs in the genome of this ancient endosymbiont. To address this question, we investigated IS transpositional activity in the unculturable Wolbachia by tracking the evolutionary dynamics and history of ISWpi1 elements. We show that 1) ISWpi1 is widespread in Wolbachia, being present in at least 55% of the 40 sampled strains, 2) ISWpi1 copies exhibit virtually identical nucleotide sequences both within and among Wolbachia genomes and possess an intact transposase gene, 3) individual ISWpi1 copies are differentially inserted among Wolbachia genomes, and 4) ISWpi1 occurs at variable copy numbers among Wolbachia genomes. Collectively, our results provide compelling evidence for intense ISWpi1 transpositional activity and frequent ISWpi1 horizontal transmission among strains during recent Wolbachia evolution. Thus, the genomes of ancient obligate endosymbionts can carry high loads of functional and transpositionally active transposable elements. Our results also indicate that Wolbachia genomes have experienced multiple and temporally distinct ISWpi1 invasions during their evolutionary history. Such recurrent exposition to new IS invasions may explain, at least partly, the unusually high density of transposable elements found in the genomes of Wolbachia endosymbionts.