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      Models of gene gain and gene loss for probabilistic reconstruction of gene content in the last universal common ancestor of life

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      1 , 2 , 2 , 2 , 2 , 3 , 4 ,
      Biology Direct
      BioMed Central

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          Abstract

          Background

          The problem of probabilistic inference of gene content in the last common ancestor of several extant species with completely sequenced genomes is: for each gene that is conserved in all or some of the genomes, assign the probability that its ancestral gene was present in the genome of their last common ancestor.

          Results

          We have developed a family of models of gene gain and gene loss in evolution, and applied the maximum-likelihood approach that uses phylogenetic tree of prokaryotes and the record of orthologous relationships between their genes to infer the gene content of LUCA, the Last Universal Common Ancestor of all currently living cellular organisms. The crucial parameter, the ratio of gene losses and gene gains, was estimated from the data and was higher in models that take account of the number of in-paralogs in genomes than in models that treat gene presences and absences as a binary trait.

          Conclusion

          While the numbers of genes that are placed confidently into LUCA are similar in the ML methods and in previously published methods that use various parsimony-based approaches, the identities of genes themselves are different. Most of the models of either kind treat the genes found in many existing genomes in a similar way, assigning to them high probabilities of being ancestral (“high ancestrality”). The ML models are more likely than others to assign high ancestrality to the genes that are relatively rare in the present-day genomes.

          Reviewers

          This article was reviewed by Martijn A Huynen, Toni Gabaldón and Fyodor Kondrashov.

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          Most cited references32

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          Horizontal gene transfer in prokaryotes: quantification and classification.

          Comparative analysis of bacterial, archaeal, and eukaryotic genomes indicates that a significant fraction of the genes in the prokaryotic genomes have been subject to horizontal transfer. In some cases, the amount and source of horizontal gene transfer can be linked to an organism's lifestyle. For example, bacterial hyperthermophiles seem to have exchanged genes with archaea to a greater extent than other bacteria, whereas transfer of certain classes of eukaryotic genes is most common in parasitic and symbiotic bacteria. Horizontal transfer events can be classified into distinct categories of acquisition of new genes, acquisition of paralogs of existing genes, and xenologous gene displacement whereby a gene is displaced by a horizontally transferred ortholog from another lineage (xenolog). Each of these types of horizontal gene transfer is common among prokaryotes, but their relative contributions differ in different lineages. The fixation and long-term persistence of horizontally transferred genes suggests that they confer a selective advantage on the recipient organism. In most cases, the nature of this advantage remains unclear, but detailed examination of several cases of acquisition of eukaryotic genes by bacteria seems to reveal the evolutionary forces involved. Examples include isoleucyl-tRNA synthetases whose acquisition from eukaryotes by several bacteria is linked to antibiotic resistance, ATP/ADP translocases acquired by intracellular parasitic bacteria, Chlamydia and Rickettsia, apparently from plants, and proteases that may be implicated in chlamydial pathogenesis.
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            Prokaryotic evolution in light of gene transfer.

            Accumulating prokaryotic gene and genome sequences reveal that the exchange of genetic information through both homology-dependent recombination and horizontal (lateral) gene transfer (HGT) is far more important, in quantity and quality, than hitherto imagined. The traditional view, that prokaryotic evolution can be understood primarily in terms of clonal divergence and periodic selection, must be augmented to embrace gene exchange as a creative force, itself responsible for much of the pattern of similarities and differences we see between prokaryotic microbes. Rather than replacing periodic selection on genetic diversity, gene loss, and other chromosomal alterations as important players in adaptive evolution, gene exchange acts in concert with these processes to provide a rich explanatory paradigm-some of whose implications we explore here. In particular, we discuss (1) the role of recombination and HGT in giving phenotypic "coherence" to prokaryotic taxa at all levels of inclusiveness, (2) the implications of these processes for the reconstruction and meaning of "phylogeny," and (3) new views of prokaryotic adaptation and diversification based on gene acquisition and exchange.
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              The Maximum Likelihood Approach to Reconstructing Ancestral Character States of Discrete Characters on Phylogenies

              Mark Page (1999)
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                Author and article information

                Journal
                Biol Direct
                Biol. Direct
                Biology Direct
                BioMed Central
                1745-6150
                2013
                19 December 2013
                : 8
                : 32
                Affiliations
                [1 ]Department of Invertebrate Zoology, American Museum of Natural History, New York, NY 10024, USA
                [2 ]Stowers Institute for Medical Research, Kansas City, Missouri 64110, USA
                [3 ]Department of Microbiology, Immunology and Molecular Genetics, University of Kansas Medical Center, Kansas City, Kansas 66160, USA
                [4 ]Present address: Division of Molecular and Cellular Biosciences, National Science Foundation, Arlington, VA 22230, USA
                Article
                1745-6150-8-32
                10.1186/1745-6150-8-32
                3892064
                24354654
                17f608fc-0ef6-4574-8d81-771c497f76dc
                Copyright © 2013 Kannan et al.; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 19 July 2013
                : 4 December 2013
                Categories
                Research

                Life sciences
                Life sciences

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