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

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

Research output: Contribution to journalArticleResearchpeer-review

64 Citations (Scopus)

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.

Original languageEnglish
Pages (from-to)22
JournalBMC Genomics
Volume7
DOIs
Publication statusPrint publication - 10 Feb 2006
Externally publishedYes

Fingerprint

Horizontal Gene Transfer
Rumen
Carbohydrates
Bacteria
Expressed Sequence Tags
Ruminants
Genes
Tetrahymena thermophila
Bacterial Genes
Urodela
Archaea
Phylogeny
Multigene Family
Eukaryota
Cluster Analysis
Genome
Food

Keywords

  • Adaptation, Physiological/genetics
  • Anaerobiosis
  • Animals
  • Bacteria/classification
  • Bacteria, Anaerobic
  • Carbohydrate Metabolism/genetics
  • Ciliophora/classification
  • Expressed Sequence Tags/chemistry
  • Gene Transfer, Horizontal
  • Genes, Bacterial
  • Genes, Protozoan
  • Glycoside Hydrolases/genetics
  • Phylogeny
  • Ruminants/microbiology

Cite this

Ricard, G., McEwan, N. R., Dutilh, B. E., Jouany, J-P., Macheboeuf, D., Mitsumori, M., ... Huynen, M. A. (2006). Horizontal gene transfer from Bacteria to rumen Ciliates indicates adaptation to their anaerobic, carbohydrates-rich environment. BMC Genomics, 7, 22. https://doi.org/10.1186/1471-2164-7-22
Ricard, Guénola ; McEwan, Neil R ; Dutilh, Bas E ; Jouany, Jean-Pierre ; Macheboeuf, Didier ; Mitsumori, Makoto ; McIntosh, Freda M ; Michalowski, Tadeusz ; Nagamine, Takafumi ; Nelson, Nancy ; Newbold, Charles J ; Nsabimana, Eli ; Takenaka, Akio ; Thomas, Nadine A ; Ushida, Kazunari ; Hackstein, Johannes H P ; Huynen, Martijn A. / Horizontal gene transfer from Bacteria to rumen Ciliates indicates adaptation to their anaerobic, carbohydrates-rich environment. In: BMC Genomics. 2006 ; Vol. 7. pp. 22.
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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.",
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author = "Gu{\'e}nola Ricard and McEwan, {Neil R} and Dutilh, {Bas E} and Jean-Pierre Jouany and Didier Macheboeuf and Makoto Mitsumori and McIntosh, {Freda M} and Tadeusz Michalowski and Takafumi Nagamine and Nancy Nelson and Newbold, {Charles J} and Eli Nsabimana and Akio Takenaka and Thomas, {Nadine A} and Kazunari Ushida and Hackstein, {Johannes H P} and Huynen, {Martijn A}",
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Ricard, G, McEwan, NR, Dutilh, BE, Jouany, J-P, Macheboeuf, D, Mitsumori, M, McIntosh, FM, Michalowski, T, Nagamine, T, Nelson, N, Newbold, CJ, Nsabimana, E, Takenaka, A, Thomas, NA, Ushida, K, Hackstein, JHP & Huynen, MA 2006, 'Horizontal gene transfer from Bacteria to rumen Ciliates indicates adaptation to their anaerobic, carbohydrates-rich environment', BMC Genomics, vol. 7, pp. 22. https://doi.org/10.1186/1471-2164-7-22

Horizontal gene transfer from Bacteria to rumen Ciliates indicates adaptation to their anaerobic, carbohydrates-rich environment. / Ricard, Guénola; McEwan, Neil R; Dutilh, Bas E; Jouany, Jean-Pierre; Macheboeuf, Didier; Mitsumori, Makoto; McIntosh, Freda M; Michalowski, Tadeusz; Nagamine, Takafumi; Nelson, Nancy; Newbold, Charles J; Nsabimana, Eli; Takenaka, Akio; Thomas, Nadine A; Ushida, Kazunari; Hackstein, Johannes H P; Huynen, Martijn A.

In: BMC Genomics, Vol. 7, 10.02.2006, p. 22.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Horizontal gene transfer from Bacteria to rumen Ciliates indicates adaptation to their anaerobic, carbohydrates-rich environment

AU - Ricard, Guénola

AU - McEwan, Neil R

AU - Dutilh, Bas E

AU - Jouany, Jean-Pierre

AU - Macheboeuf, Didier

AU - Mitsumori, Makoto

AU - McIntosh, Freda M

AU - Michalowski, Tadeusz

AU - Nagamine, Takafumi

AU - Nelson, Nancy

AU - Newbold, Charles J

AU - Nsabimana, Eli

AU - Takenaka, Akio

AU - Thomas, Nadine A

AU - Ushida, Kazunari

AU - Hackstein, Johannes H P

AU - Huynen, Martijn A

PY - 2006/2/10

Y1 - 2006/2/10

N2 - 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.

AB - 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.

KW - Adaptation, Physiological/genetics

KW - Anaerobiosis

KW - Animals

KW - Bacteria/classification

KW - Bacteria, Anaerobic

KW - Carbohydrate Metabolism/genetics

KW - Ciliophora/classification

KW - Expressed Sequence Tags/chemistry

KW - Gene Transfer, Horizontal

KW - Genes, Bacterial

KW - Genes, Protozoan

KW - Glycoside Hydrolases/genetics

KW - Phylogeny

KW - Ruminants/microbiology

U2 - 10.1186/1471-2164-7-22

DO - 10.1186/1471-2164-7-22

M3 - Article

VL - 7

SP - 22

JO - BMC Genomics

JF - BMC Genomics

SN - 1471-2164

ER -