Phylogenetic analysis of the triterpene cyclase protein family in prokaryotes and eukaryotes suggests bidirectional lateral gene transfer

Authors

  • Tancred Frickey,

    1. Max Planck Institut fuer Entwicklungsbiologie, Spemannstrasse 35, 72076 Tübingen, Germany.
    2. Research School for Biological Sciences, Australian National University, 2602, Acton Canberra, Australia.
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  • Elmar Kannenberg

    Corresponding author
    1. Universität Tübingen, Mikrobiologie, Auf der Morgenstelle 28, 72076 Tübingen, Germany.
    2. Complex Carbohydrate Research Center, University of Georgia, 315 Riverbend Road, Athens, GA 30602, USA.
      *E-mail elmark@ccrc.uga.edu; Tel. (+1) 706 542 2949; Fax (+1) 706 542 4412.
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  • This paper is dedicated to the late Guy Ourisson. He will be remembered for his tireless interest in the understanding of isoprenoid evolution and function.

*E-mail elmark@ccrc.uga.edu; Tel. (+1) 706 542 2949; Fax (+1) 706 542 4412.

Summary

Functional constraints to modifications in triterpene cyclase amino acid sequences make them good candidates for evolutionary studies on the phylogenetic relatedness of these enzymes in prokaryotes as well as in eukaryotes. In this study, we used a set of identified triterpene cyclases, a group of mainly bacterial squalene cyclases and a group of predominantly eukaryotic oxidosqualene cyclases, as seed sequences to identify 5288 putative triterpene cyclase homologues in publicly available databases. The Cluster Analysis of Sequences software was used to detect groups of sequences with increased pairwise sequence similarity. The sequences fall into two main clusters, a bacterial and a eukaryotic. The conserved, informative regions of a multiple sequence alignment of the family were used to construct a neighbour-joining phylogenetic tree using the AsaturA and maximum likelihood phylogenetic tree using the PhyML software. Both analyses showed that most of the triterpene cyclase sequences were similarly grouped to the accepted taxonomic relationships of the organism the sequences originated from, supporting the idea of vertical transfer of cyclase genes from parent to offspring as the main evolutionary driving force in this protein family. However, a small group of sequences from three bacterial species (Stigmatella, Gemmata and Methylococcus) grouped with an otherwise purely eukaryotic cluster of oxidosqualene cyclases, while a small group of sequences from seven fungal species and a sequence from the fern Adiantum grouped consistently with a cluster of otherwise purely bacterial squalene cyclases. This suggests that lateral gene transfer may have taken place, entailing a transfer of oxidosqualene cyclases from eukaryotes to bacteria and a transfer of squalene cyclase from bacteria to an ancestor of the group of Pezizomycotina fungi.

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