Research article

Horizontal gene transfer from Bacteria to rumen Ciliates indicates adaptation to their anaerobic, carbohydrates-rich environment

Guénola Ricard¹ , Neil R McEwan² , Bas E Dutilh¹ , Jean-Pierre Jouany³ , Didier Macheboeuf³ , Makoto Mitsumori⁴ , Freda M McIntosh⁵ , Tadeusz Michalowski⁶ , Takafumi Nagamine⁷ , Nancy Nelson⁵ , Charles J Newbold⁷ , Eli Nsabimana³ , Akio Takenaka⁴ , Nadine A Thomas⁵ , Kazunari Ushida⁸ , Johannes HP Hackstein⁹ and Martijn A Huynen¹

¹Center for Molecular and Biomolecular Informatics, Nijmegen Center for Molecular Life Sciences, Radboud University Nijmegen Medical Centre, Toernooiveld 1, 6525 ED Nijmegen, The Netherlands

²Institute of Rural Sciences, University of Wales, Aberystwyth, SY23 3AL, UK

³I.N.R.A., Station de Recherches sur la Nutrition des Herbivores, Centre de Recherches de Clermont-Ferrand/Theix, France

⁴National Institute of Livestock and Grassland Science, 2 Ikenodai, Kukizaki, Ibaraki, 305-0901, Japan

⁵Rowett Research Institute, Aberdeen, AB21 9SB, UK

⁶Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, Jablonna, Warsaw, Poland

⁷Rumen Microbiology Research Team, STAFF-Institute, 446-1 Ippaizuka, Kamiyokoba, Tsukuba 305-0854, Japan

⁸Laboratory of Animal Science, Kyoto Prefectural University, Shimogamo, Kyoto 606-8522, Japan

⁹Department of Evolutionary Microbiology, Radboud University Nijmegen, Nijmegen, The Netherlands

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BMC Genomics 2006, 7:22doi:10.1186/1471-2164-7-22

Published:	10 February 2006

Abstract

Background

The horizontal transfer of expressed genes from Bacteria into Ciliates which live in close contact with each other in the rumen (the foregut of ruminants) was studied using ciliate Expressed Sequence Tags (ESTs). More than 4000 ESTs were sequenced from representatives of the two major groups of rumen Cilates: the order Entodiniomorphida (Entodinium simplex, Entodinium caudatum, Eudiplodinium maggii, Metadinium medium, Diploplastron affine, Polyplastron multivesiculatum and Epidinium ecaudatum) and the order Vestibuliferida, previously called Holotricha (Isotricha prostoma, Isotricha intestinalis and Dasytricha ruminantium).

Results

A comparison of the sequences with the completely sequenced genomes of Eukaryotes and Prokaryotes, followed by large-scale construction and analysis of phylogenies, identified 148 ciliate genes that specifically cluster with genes from the Bacteria and Archaea. The phylogenetic clustering with bacterial genes, coupled with the absence of close relatives of these genes in the Ciliate Tetrahymena thermophila, indicates that they have been acquired via Horizontal Gene Transfer (HGT) after the colonization of the gut by the rumen Ciliates.

Conclusion

Among the HGT candidates, we found an over-representation (>75%) of genes involved in metabolism, specifically in the catabolism of complex carbohydrates, a rich food source in the rumen. We propose that the acquisition of these genes has greatly facilitated the Ciliates' colonization of the rumen providing evidence for the role of HGT in the adaptation to new niches.