The role of duplications in the evolution of genomes highlights the need for evolutionary-based approaches in comparative genomics

Understanding the evolutionary plasticity of the genome requires a global, comparative approach in which genetic events are considered both in a phylogenetic framework and with regard to population genetics and environmental variables. In the mechanisms that generate adaptive and non-adaptive changes in genomes, segmental duplications (duplication of individual genes or genomic regions) and polyploidization (whole genome duplications) are well-known driving forces. The probability of fixation and maintenance of duplicates depends on many variables, including population sizes and selection regimes experienced by the corresponding genes: a combination of stochastic and adaptive mechanisms has shaped all genomes. A survey of experimental work shows that the distinction made between fixation and maintenance of duplicates still needs to be conceptualized and mathematically modeled. Here we review the mechanisms that increase or decrease the probability of fixation or maintenance of duplicated genes, and examine the outcome of these events on the adaptation of the organism

Nme Gene Family Evolutionary History Reveals Pre-Metazoan Origins and High Conservation between Humans and the Sea Anemone, Nematostella vectensis

There was an error in affiliation 1 for authors Thomas Desvignes and Julien Bobe. Affiliation 1 should be: INRA, UR1037 SCRIBE, Campus de Beaulieu, F-35000 Rennes, FranceBackground: The Nme gene family is involved in multiple physiological and pathological processes such as cellular differentiation, development, metastatic dissemination, and cilia functions. Despite the known importance of Nme genes and their use as clinical markers of tumor aggressiveness, the associated cellular mechanisms remain poorly understood. Over the last 20 years, several non-vertebrate model species have been used to investigate Nme functions. However, the evolutionary history of the family remains poorly understood outside the vertebrate lineage. The aim of the study was thus to elucidate the evolutionary history of the Nme gene family in Metazoans. [br/]Methodology/Principal Findings: Using a total of 21 eukaryote species including 14 metazoans, the evolutionary history of Nme genes was reconstructed in the metazoan lineage. We demonstrated that the complexity of the Nme gene family, initially thought to be restricted to chordates, was also shared by the metazoan ancestor. We also provide evidence suggesting that the complexity of the family is mainly a eukaryotic innovation, with the exception of Nme8 that is likely to be a choanoflagellate/metazoan innovation. Highly conserved gene structure, genomic linkage, and protein domains were identified among metazoans, some features being also conserved in eukaryotes. When considering the entire Nme family, the starlet sea anemone is the studied metazoan species exhibiting the most conserved gene and protein sequence features with humans. In addition, we were able to show that most of the proteins known to interact with human NME proteins were also found in starlet sea anemone. [br/]Conclusion/Significance: Together, our observations further support the association of Nme genes with key cellular functions that have been conserved throughout metazoan evolution. Future investigations of evolutionarily conserved Nme gene functions using the starlet sea anemone could shed new light on a wide variety of key developmental and cellular processes

Eleven ancestral gene families lost in mammals and vertebrates while otherwise universally conserved in animals

BACKGROUND: Gene losses played a role which may have been as important as gene and genome duplications and rearrangements, in modelling today species' genomes from a common ancestral set of genes. The set and diversity of protein-coding genes in a species has direct output at the functional level. While gene losses have been reported in all the major lineages of the metazoan tree of life, none have proposed a focus on specific losses in the vertebrates and mammals lineages. In contrast, genes lost in protostomes (i.e. arthropods and nematodes) but still present in vertebrates have been reported and extensively detailed. This probable over-anthropocentric way of comparing genomes does not consider as an important phenomena, gene losses in species that are usually described as "higher". However reporting universally conserved genes throughout evolution that have recently been lost in vertebrates and mammals could reveal interesting features about the evolution of our genome, particularly if these losses can be related to losses of capability. RESULTS: We report 11 gene families conserved throughout eukaryotes from yeasts (such as Saccharomyces cerevisiae) to bilaterian animals (such as Drosophila melanogaster or Caenorhabditis elegans). This evolutionarily wide conservation suggests they were present in the last common ancestors of fungi and metazoan animals. None of these 11 gene families are found in human nor mouse genomes, and their absence generally extends to all vertebrates. A total of 8 out of these 11 gene families have orthologs in plants, suggesting they were present in the Last Eukaryotic Common Ancestor (LECA). We investigated known functional information for these 11 gene families. This allowed us to correlate some of the lost gene families to loss of capabilities. CONCLUSION: Mammalian and vertebrate genomes lost evolutionary conserved ancestral genes that are probably otherwise not dispensable in eukaryotes. Hence, the human genome, which is generally viewed as being the result of increased complexity and gene-content, has also evolved through simplification and gene losses. This acknowledgement confirms, as already suggested, that the genome of our far ancestor was probably more complex than ever considered

The rhizome of life: what about metazoa?

International audienceThe increase in huge number of genomic sequences in recent years has contributed to various genetic events such as horizontal gene transfer (HGT), gene duplication and hybridization of species. Among them HGT has played an important role in the genome evolution and was believed to occur only in Bacterial and Archaeal genomes. As a result, genomes were found to be chimeric and the evolution of life was represented in different forms such as forests, networks and species evolution was described more like a rhizome, rather than a tree. However, in the last few years, HGT has also been evidenced in other group such as metazoa (for example in root-knot nematodes, bdelloid rotifers and mammals). In addition to HGT, other genetic events such as transfer by retrotransposons and hybridization between more closely related lineages are also well established. Therefore, in the light of such genetic events, whether the evolution of metazoa exists in the form of a tree, network or rhizome is highly questionable and needs to be determined. In the current review, we will focus on the role of HGT, retrotransposons and hybridization in the metazoan evolution

Compound Poisson Approximation and Testing for Gene Clusters with Multigene Families

International audienceWe present in this article a compound Poisson approximation for computing probabilities involved in significance tests for conserved genomic regions between different species. We consider the case when the conserved genomic regions are found by the reference region approach. An important aspect of our computations is the fact that we are taking into account the existence of multigene families. We obtain convergence results for the error of our approximation by using the Stein-Chen method for compound Poisson approximation

Nme protein family evolutionary history, a vertebrate perspective

Background: The Nme family, previously known as Nm23 or NDPK, is involved in various molecular processes including tumor metastasis and some members of the family, but not all, exhibit a Nucleoside Diphosphate Kinase (NDPK) activity. Ten genes are known in humans, in which some members have been extensively studied. In non-mammalian species, the Nme protein family has received, in contrast, far less attention. The picture of the vertebrate Nme family remains thus incomplete and orthology relationships with mammalian counterparts were only partially characterized. The present study therefore aimed at characterizing the Nme gene repertoire in vertebrates with special interest for teleosts, and providing a comprehensive overview of the Nme gene family evolutionary history in vertebrates. Results: In the present study, we present the evolutionary history of the Nme family in vertebrates and characterize the gene family repertoire for the first time in several non-mammalian species. Our observations show that vertebrate Nme genes can be separated in two evolutionary distinct groups. Nme1, Nme2, Nme3, and Nme4 belong to Group I while vertebrate Nme5, Nme6, Nme7, Nme8, and Nme9 belong to Group II. The position of Nme10 is in contrast more debatable due to its very specific evolutionary history. The present study clearly indicates that Nme5, Nme6, Nme7, and Nme8 originate from duplication events that occurred before the chordate radiation. In contrast, Nme genes of the Group I have a very different evolutionary history as our results suggest that they all arise from a common gene present in the chordate ancestor. In addition, expression patterns of all zebrafish nme transcripts were studied in a broad range of tissues by quantitative PCR and discussed in the light of the function of their mammalian counterparts. Conclusion: This work offers an evolutionary framework that will pave the way for future studies on vertebrate Nme proteins and provides a unified vertebrate Nme nomenclature that is consistent with the nomenclature in use in mammals. Based on protein structure and expression data, we also provide new insight into molecular functions of Nme proteins among vertebrates and raise intriguing questions on the roles of Nme proteins in gonads

Massive comparative genomic analysis reveals convergent evolution of specialized bacteria

<p>Abstract</p> <p>Background</p> <p>Genome size and gene content in bacteria are associated with their lifestyles. Obligate intracellular bacteria (i.e., mutualists and parasites) have small genomes that derived from larger free-living bacterial ancestors; however, the different steps of bacterial specialization from free-living to intracellular lifestyle have not been studied comprehensively. The growing number of available sequenced genomes makes it possible to perform a statistical comparative analysis of 317 genomes from bacteria with different lifestyles.</p> <p>Results</p> <p>Compared to free-living bacteria, host-dependent bacteria exhibit fewer rRNA genes, more split rRNA operons and fewer transcriptional regulators, linked to slower growth rates. We found a function-dependent and non-random loss of the same 100 orthologous genes in all obligate intracellular bacteria. Thus, we showed that obligate intracellular bacteria from different phyla are converging according to their lifestyle. Their specialization is an irreversible phenomenon characterized by translation modification and massive gene loss, including the loss of transcriptional regulators. Although both mutualists and parasites converge by genome reduction, these obligate intracellular bacteria have lost distinct sets of genes in the context of their specific host associations: mutualists have significantly more genes that enable nutrient provisioning whereas parasites have genes that encode Types II, IV, and VI secretion pathways.</p> <p>Conclusion</p> <p>Our findings suggest that gene loss, rather than acquisition of virulence factors, has been a driving force in the adaptation of parasites to eukaryotic cells. This comparative genomic analysis helps to explore the strategies by which obligate intracellular genomes specialize to particular host-associations and contributes to advance our knowledge about the mechanisms of bacterial evolution.</p> <p>Reviewers</p> <p>This article was reviewed by Eugene V. Koonin, Nicolas Galtier, and Jeremy Selengut.</p

Strategies for Reliable Exploitation of Evolutionary Concepts in High Throughput Biology

The recent availability of the complete genome sequences of a large number of model organisms, together with the immense amount of data being produced by the new high-throughput technologies, means that we can now begin comparative analyses to understand the mechanisms involved in the evolution of the genome and their consequences in the study of biological systems. Phylogenetic approaches provide a unique conceptual framework for performing comparative analyses of all this data, for propagating information between different systems and for predicting or inferring new knowledge. As a result, phylogeny-based inference systems are now playing an increasingly important role in most areas of high throughput genomics, including studies of promoters (phylogenetic footprinting), interactomes (based on the presence and degree of conservation of interacting proteins), and in comparisons of transcriptomes or proteomes (phylogenetic proximity and co-regulation/co-expression). Here we review the recent developments aimed at making automatic, reliable phylogeny-based inference feasible in large-scale projects. We also discuss how evolutionary concepts and phylogeny-based inference strategies are now being exploited in order to understand the evolution and function of biological systems. Such advances will be fundamental for the success of the emerging disciplines of systems biology and synthetic biology, and will have wide-reaching effects in applied fields such as biotechnology, medicine and pharmacology

The genealogic tree of mycobacteria reveals a long-standing sympatric life into free-living protozoa.

International audienceFree-living protozoa allow horizontal gene transfer with and between the microorganisms that they host. They host mycobacteria for which the sources of transferred genes remain unknown. Using BLASTp, we searched within the genomes of 15 mycobacteria for homologous genes with 34 amoeba-resistant bacteria and the free-living protozoa Dictyostelium discoideum. Subsequent phylogenetic analysis of these sequences revealed that eight mycobacterial open-reading frames (ORFs) were probably acquired via horizontal transfer from beta- and gamma-Proteobacteria and from Firmicutes, but the transfer histories could not be reliably established in details. One further ORF encoding a pyridine nucleotide disulfide oxidoreductase (pyr-redox) placed non-tuberculous mycobacteria in a clade with Legionella spp., Francisella spp., Coxiella burnetii, the ciliate Tetrahymena thermophila and D. discoideum with a high reliability. Co-culturing Mycobacterium avium and Legionella pneumophila with the amoeba Acanthamoeba polyphaga demonstrated that these two bacteria could live together in amoebae for five days, indicating the biological relevance of intra-amoebal transfer of the pyr-redox gene. In conclusion, the results of this study support the hypothesis that protists can serve as a source and a place for gene transfer in mycobacteria