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

Guénola Ricard,Charles J Newbold,Freda M Mcintosh,Kazunari Ushida,Nancy Nelson,Bas E Dutilh,Nadine A Thomas,Didier Macheboeuf,Martijn A Huynen,Eli Nsabimana,Tadeusz Michalowski,Takafumi Nagamine,Jean-Pierre Jouany,Akio Takenaka,Makoto Mitsumori,Johannes Hp Hackstein,Neil R Mcewan

doi:10.1186/1471-2164-7-22

Abstract

BackgroundThe 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).ResultsA 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.ConclusionAmong 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.

Highlights

The horizontal transfer of expressed genes from Bacteria into Ciliates which live in close contact with each other in the rumen was studied using ciliate Expressed Sequence Tags (ESTs)
Among the Horizontal Gene Transfer (HGT) candidates there is an over representation of genes involved in metabolism: while in the complete EST dataset the functions involved in Cellular process and signalling (47.0%) are prevalent, most of the HGT candidates are involved in Metabolism (75.4%) (See Figure 2).(Note that this number is an underestimate as it does not include 15 of the 30 sequences which do not belong to a KOG/COG – among which are eight xylanases, two cellulases, three pectate lyases, one uridine kinase and one α-glucosidase)
Comparing the numbers of ESTs per cluster we found no indication that horizontally transferred genes are higher expressed than non-transferred ones. 125 sequences out of the 148 HGT candidates encode

Summary

Introduction

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). Horizontal Gene Transfer (HGT) implicates the transfer of genetic material between species. Genes acquired by this process can provide novel functions to the recipient organism, when that organism is naive for functions associated with the newly acquired gene(s). HGT on a large-scale has mainly been described from organelles to the nucleus transfer [2], and between different species of Bacteria and Archaea [3,4], and on a smaller scale from Eukaryotes to Bacteria [5]. The transfer of 16 bacterial genes to Nematodes [8] and of 96 such genes to Entamoeba histolytica [9] are the only examples where HGT from Bacteria to Eukaryotes has been investigated on a large-scale

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