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Lateral transfer at the gene and subgenic levels in the evolution of eukaryotic enolase.

ABSTRACT: Enolase genes from land plants and apicomplexa (intracellular parasites, including the malarial parasite, Plasmodium) share two short insertions. This observation has led to the suggestion that the apicomplexan enolase is the product of a lateral transfer event involving the algal endosymbiont from which the apicomplexan plastid is derived. We have examined enolases from a wide variety of algae, as well as ciliates (close relatives of apicomplexa), to determine whether lateral transfer can account for the origin of the apicomplexan enolase. We find that lateral gene transfer, likely occurring intracellularly between endosymbiont and host nucleus, does account for the evolution of cryptomonad and chlorarachniophyte algal enolases but fails to explain the apicomplexan enolase. This failure is because the phylogenetic distribution of the insertions--which we find in apicomplexa, ciliates, land plants, and charophyte green algae--directly conflicts with the phylogeny of the gene itself. Protein insertions have traditionally been treated as reliable markers of evolutionary events; however, these enolase insertions do not seem to reflect accurately the evolutionary history of the molecule. The lack of congruence between insertions and phylogeny could be because of the parallel loss of both insertions in two or more lineages, or what is more likely, because the insertions were transmitted between distantly related genes by lateral transfer and fine-scale recombination, resulting in a mosaic gene. This latter process would be difficult to detect without such insertions to act as markers, and such mosaic genes could blur the "tree of life" beyond the extent to which whole-gene lateral transfer is already known to confound evolutionary reconstruction.

SUBMITTER: Keeling PJ

PROVIDER: S-EPMC58546 | biostudies-literature | 2001 Sep

REPOSITORIES: biostudies-literature

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Lateral transfer at the gene and subgenic levels in the evolution of eukaryotic enolase.

Keeling P J PJ Palmer J D JD

Proceedings of the National Academy of Sciences of the United States of America 20010828 19

Enolase genes from land plants and apicomplexa (intracellular parasites, including the malarial parasite, Plasmodium) share two short insertions. This observation has led to the suggestion that the apicomplexan enolase is the product of a lateral transfer event involving the algal endosymbiont from which the apicomplexan plastid is derived. We have examined enolases from a wide variety of algae, as well as ciliates (close relatives of apicomplexa), to determine whether lateral transfer can accou ...[more]

PMID: 11526220

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Project description:BACKGROUND: Lateral gene transfer is increasingly invoked to explain phylogenetic results that conflict with our understanding of organismal relationships. In eukaryotes, the most common observation interpreted in this way is the appearance of a bacterial gene (one that is not clearly derived from the mitochondrion or plastid) in a eukaryotic nuclear genome. Ideally such an observation would involve a single eukaryote or a small group of related eukaryotes encoding a gene from a specific bacterial lineage. RESULTS: Here we show that several apparently simple cases of lateral transfer are actually more complex than they originally appeared: in these instances we find that two or more distantly related eukaryotic groups share the same bacterial gene, resulting in a punctate distribution. Specifically, we describe phylogenies of three core carbon metabolic enzymes: transketolase, glyceraldehyde-3-phosphate dehydrogenase and ribulose-5-phosphate-3-epimerase. Phylogenetic trees of each of these enzymes includes a strongly-supported clade consisting of several eukaryotes that are distantly related at the organismal level, but whose enzymes are apparently all derived from the same lateral transfer. With less sampling any one of these examples would appear to be a simple case of bacterium-to-eukaryote lateral transfer; taken together, their evolutionary histories cannot be so simple. The distributions of these genes may represent ancient paralogy events or genes that have been transferred from bacteria to an ancient ancestor of the eukaryotes that retain them. They may alternatively have been transferred laterally from a bacterium to a single eukaryotic lineage and subsequently transferred between distantly related eukaryotes. CONCLUSION: Determining how complex the distribution of a transferred gene is depends on the sampling available. These results show that seemingly simple cases may be revealed to be more complex with greater sampling, suggesting many bacterial genes found in eukaryotic genomes may have a punctate distribution.

Project description:BackgroundLarge scale genome arrangement, such as whole gene insertion/deletion, plays an important role in bacterial genome evolution. Various methods have been employed to study the dynamic process of gene insertions and deletions, such as parsimony methods and maximum likelihood methods. Previous maximum likelihood studies have assumed that the rate of gene insertions/deletions is constant over different genes. This assumption is unrealistic. For instance, it has been shown that informational genes are less likely to be laterally transferred than non-informational genes. However, how much of the variation in gene transfer rates is due to the difference between informational genes and non-informational genes is unclear. In this study, a Gamma-distribution was incorporated in the likelihood estimation by considering rate variation for gene insertions/deletions between genes. This makes it possible to address whether a difference between informational genes and non-informational genes is the main contributor to rate variation of lateral gene transfers.ResultsThe results show that models incorporating rate variation fit the data better than do constant rate models in many phylogenetic groups. Even though informational genes are less likely to be laterally transferred than non-informational genes, the degree of rate variation for insertions/deletions did not change dramatically and remained high even when informational genes were excluded from the study. This suggests that the variation in rate of insertions/deletions is not due mainly to the simple difference between informational genes and non-informational genes. Among genes that are not classified as informational and among the informational genes themselves, there are still large differences in the rates that these genes are inserted and deleted.ConclusionWhile the difference in informational gene rates contributes to rate variation, it is only a small fraction of the variation present; instead, a substantial amount of rate variation for insertions/deletions remains among both informational genes and among non-informational genes.

Project description:BackgroundPhylogeographic reconstruction of some bacterial populations is hindered by low diversity coupled with high levels of lateral gene transfer. A comparison of recombination levels and diversity at seven housekeeping genes for eleven bacterial species, most of which are commonly cited as having high levels of lateral gene transfer shows that the relative contributions of homologous recombination versus mutation for Burkholderia pseudomallei is over two times higher than for Streptococcus pneumoniae and is thus the highest value yet reported in bacteria. Despite the potential for homologous recombination to increase diversity, B. pseudomallei exhibits a relative lack of diversity at these loci. In these situations, whole genome genotyping of orthologous shared single nucleotide polymorphism loci, discovered using next generation sequencing technologies, can provide very large data sets capable of estimating core phylogenetic relationships. We compared and searched 43 whole genome sequences of B. pseudomallei and its closest relatives for single nucleotide polymorphisms in orthologous shared regions to use in phylogenetic reconstruction.ResultsBayesian phylogenetic analyses of >14,000 single nucleotide polymorphisms yielded completely resolved trees for these 43 strains with high levels of statistical support. These results enable a better understanding of a separate analysis of population differentiation among >1,700 B. pseudomallei isolates as defined by sequence data from seven housekeeping genes. We analyzed this larger data set for population structure and allele sharing that can be attributed to lateral gene transfer. Our results suggest that despite an almost panmictic population, we can detect two distinct populations of B. pseudomallei that conform to biogeographic patterns found in many plant and animal species. That is, separation along Wallace's Line, a biogeographic boundary between Southeast Asia and Australia.ConclusionWe describe an Australian origin for B. pseudomallei, characterized by a single introduction event into Southeast Asia during a recent glacial period, and variable levels of lateral gene transfer within populations. These patterns provide insights into mechanisms of genetic diversification in B. pseudomallei and its closest relatives, and provide a framework for integrating the traditionally separate fields of population genetics and phylogenetics for other bacterial species with high levels of lateral gene transfer.

Dataset Information

Lateral transfer at the gene and subgenic levels in the evolution of eukaryotic enolase.

Publications

Lateral transfer at the gene and subgenic levels in the evolution of eukaryotic enolase.

Similar Datasets

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