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MBE Advance Access published online on June 30, 2009

Molecular Biology and Evolution, doi:10.1093/molbev/msp123
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© The Author 2009. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Article

Streamlining and large ancestral genomes in Archaea inferred with a phylogenetic birth-and-death model

Miklós Csurös1 and István Miklós2

1 Department of Computer Science and Operations Research, University of Montréal, Canada
2 Rényi Institute of Mathematics, Hungarian Academy of Sciences, Budapest, Hungary

Corresponding author: Miklós Csurös. Département d'informatique et de recherche opérationnelle, Université de Montréal, C.P. 6128, succursale Centre-Ville, Montréal, QC, H3C 3J7, Canada. Tel: +1 514 343–6111 extension 1655. Fax: +1 514 343–6111. E-mail: csuros{at}iro.umontreal.ca.

Received for publication February 19, 2009. Revision received June 2, 2009. Accepted for publication June 9, 2009.

Homologous genes originate from a common ancestor through vertical inheritance, duplication or horizontal gene transfer. Entire homolog families spawned by a single ancestral gene can be identified across multiple genomes based on protein sequence similarity. The sequences, however, do not always reveal conclusively the history of large families. In order to study the evolution of complete gene repertoires, we propose here a mathematical framework that does not rely on resolved gene family histories. We show that so-called phylogenetic profiles, formed by family sizes across multiple genomes, are sufficient to infer principal evolutionary trends. The main novelty in our approach is an efficient algorithm to compute the likelihood of a phylogenetic profile in a model of birth-and-death processes acting on a phylogeny.

We examine known gene families in 28 archaeal genomes using a probabilistic model that involves lineage- and family-specific components of gene acquisition, duplication, and loss. The model enables us to consider all possible histories when inferring statistics about archaeal evolution. According to our reconstruction, most lineages are characterized by a net loss of gene families. Major increases in gene repertoire have occurred only a few times. Our reconstruction underlines the importance of persistent streamlining processes in shaping genome composition in Archaea. It also suggests that early archaeal genomes were as complex as typical modern ones, and even show signs, in the case of the methanogenic ancestor, of an extremely large gene repertoire.

Key Words: gene content evolution • maximum likelihood • Last Archaeal Common Ancestor


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