The symbiotic intestinal ciliates and the evolution of their hosts

Seung Yeo Moon-van der Staay; Georg W. M. van der Staay; Tadeusz Michalowski; Jean-Pierre Jouany; Peter Pristas; Peter Javorsky; Svetlana Kisidayova; Zora Varadyova; Neil R. McEwan; C. Jamie Newbold; Theo van Alen; Rob de Graaf; Markus Schmid; Martijn A. Huynen; Johannes H. P. Hackstein

doi:10.1016/j.ejop.2014.01.004

The symbiotic intestinal ciliates and the evolution of their hosts

Seung Yeo Moon-van der Staay
, Georg W. M. van der Staay
, Tadeusz Michalowski
, Jean-Pierre Jouany
, Peter Pristas
, Peter Javorsky
, Svetlana Kisidayova
, Zora Varadyova
, Neil R. McEwan
, C. Jamie Newbold
, Theo van Alen
, Rob de Graaf
, Markus Schmid
, Martijn A. Huynen
, Johannes H. P. Hackstein

Publications: Contribution to journal › Article › Peer Reviewed

Abstract

The evolution of sophisticated differentiations of the gastro-intestinal tract enabled herbivorous mammals to digest dietary cellulose and hemicellulose with the aid of a complex anaerobic microbiota. Distinctive symbiotic ciliates, which are unique to this habitat, are the largest representatives of this microbial community. Analyses of a total of 484 different 18S rRNA genes show that extremely complex, but related ciliate communities can occur in the rumen of cattle, sheep, goats and red deer (301 sequences). The communities in the hindgut of equids (Equus caballus, Equus quagga), and elephants (Elephas maximus, Loxodonta africanus; 162 sequences), which are clearly distinct from the ruminant ciliate biota, exhibit a much higher diversity than anticipated on the basis of their morphology. All these ciliates from the gastro-intestinal tract constitute a monophyletic group, which consists of two major taxa, i.e. Vestibuliferida and Entodiniomorphida. The ciliates from the evolutionarily older hindgut fermenters exhibit a clustering that is specific for higher taxa of their hosts, as extant species of horse and zebra on the one hand, and Africa and Indian elephant on the other hand, share related ciliates. The evolutionary younger ruminants altogether share the various entodiniomorphs and the vestibuliferids from ruminants.

Original language	English
Pages (from-to)	166-173
Number of pages	8
Journal	European Journal of Protistology
Volume	50
Issue number	2
DOIs	https://doi.org/10.1016/j.ejop.2014.01.004
Publication status	Published - Apr 2014

Funding

We are indebted to Prof. Dr. S Tamminga (Wageningen), Prof. Dr. A.G.M. Tielens (Utrecht), and Dr. J. Koopman (Nijmegen) for providing rumen fluid. The technical assistance by Nadine Thomas, Nancy Nelson, and the contributions by Eli Nsabimana, Didier Macheboeuf, Martina Regensbogenova, Freda M. McIntosh are gratefully acknowledged. The authors would like to thank also the research students and trainees Minh Bao Huynh, Alvin Polenewen, Mark Holewijn and Emily Cadot for their help in isolating DNA, cloning, sequencing and performing phylogenetic analyses. This project was supported by the European Union 5th framework grants ERCULE and CIMES. The Rowett Research Institute is supported by the Scottish Executive Environmental and Rural Affairs Department. Dagmar Thierer, IZW, Berlin, and the people from Burger's Zoo, Arnhem, are gratefully acknowledged for providing faeces from various hindgut fermenters.

Austrian Fields of Science 2012

106022 Microbiology

Keywords

Caecum/colon
Ciliates
Community analysis
Gastro-intestinal tract
Rumen
18S rDNA
18S RDNA SEQUENCES
PHYLOGENETIC ANALYSIS
SHEEP RUMEN
PROTOZOA
CILIOPHORA
ENTODINIOMORPHIDA
ELEPHANTS
DIVERSITY
BACTERIA
ORIGINS

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10.1016/j.ejop.2014.01.004

Cite this

Moon-van der Staay, S. Y., van der Staay, G. W. M., Michalowski, T., Jouany, J.-P., Pristas, P., Javorsky, P., Kisidayova, S., Varadyova, Z., McEwan, N. R., Newbold, C. J., van Alen, T., de Graaf, R., Schmid, M., Huynen, M. A., & Hackstein, J. H. P. (2014). The symbiotic intestinal ciliates and the evolution of their hosts. European Journal of Protistology, 50(2), 166-173. https://doi.org/10.1016/j.ejop.2014.01.004

@article{f315915998ec46ac9a8c4b6447c6555a,

title = "The symbiotic intestinal ciliates and the evolution of their hosts",

abstract = "The evolution of sophisticated differentiations of the gastro-intestinal tract enabled herbivorous mammals to digest dietary cellulose and hemicellulose with the aid of a complex anaerobic microbiota. Distinctive symbiotic ciliates, which are unique to this habitat, are the largest representatives of this microbial community. Analyses of a total of 484 different 18S rRNA genes show that extremely complex, but related ciliate communities can occur in the rumen of cattle, sheep, goats and red deer (301 sequences). The communities in the hindgut of equids (Equus caballus, Equus quagga), and elephants (Elephas maximus, Loxodonta africanus; 162 sequences), which are clearly distinct from the ruminant ciliate biota, exhibit a much higher diversity than anticipated on the basis of their morphology. All these ciliates from the gastro-intestinal tract constitute a monophyletic group, which consists of two major taxa, i.e. Vestibuliferida and Entodiniomorphida. The ciliates from the evolutionarily older hindgut fermenters exhibit a clustering that is specific for higher taxa of their hosts, as extant species of horse and zebra on the one hand, and Africa and Indian elephant on the other hand, share related ciliates. The evolutionary younger ruminants altogether share the various entodiniomorphs and the vestibuliferids from ruminants.",

keywords = "Caecum/colon, Ciliates, Community analysis, Gastro-intestinal tract, Rumen, 18S rDNA, 18S RDNA SEQUENCES, PHYLOGENETIC ANALYSIS, SHEEP RUMEN, PROTOZOA, CILIOPHORA, ENTODINIOMORPHIDA, ELEPHANTS, DIVERSITY, BACTERIA, ORIGINS",

author = "\{Moon-van der Staay\}, \{Seung Yeo\} and \{van der Staay\}, \{Georg W. M.\} and Tadeusz Michalowski and Jean-Pierre Jouany and Peter Pristas and Peter Javorsky and Svetlana Kisidayova and Zora Varadyova and McEwan, \{Neil R.\} and Newbold, \{C. Jamie\} and \{van Alen\}, Theo and \{de Graaf\}, Rob and Markus Schmid and Huynen, \{Martijn A.\} and Hackstein, \{Johannes H. P.\}",

note = "Funding Information: We are indebted to Prof. Dr. S. Tamminga (Wageningen), Prof. Dr. A.G.M. Tielens (Utrecht), and Dr. J. Koopman (Nijmegen) for providing rumen fluid. The technical assistance by Nadine Thomas, Nancy Nelson, and the contributions by Eli Nsabimana, Didier Macheboeuf, Martina Regensbogenova, Freda M. McIntosh are gratefully acknowledged. The authors would like to thank also the research students and trainees Minh Bao Huynh, Alvin Polenewen, Mark Holewijn and Emily Cadot for their help in isolating DNA, cloning, sequencing and performing phylogenetic analyses. This project was supported by the European Union 5th framework grants ERCULE and CIMES. The Rowett Research Institute is supported by the Scottish Executive Environmental and Rural Affairs Department. Dagmar Thierer, IZW, Berlin, and the people from Burger's Zoo, Arnhem, are gratefully acknowledged for providing faeces from various hindgut fermenters.",

year = "2014",

month = apr,

doi = "10.1016/j.ejop.2014.01.004",

language = "English",

volume = "50",

pages = "166--173",

journal = "European Journal of Protistology",

issn = "0932-4739",

number = "2",

}

Moon-van der Staay, SY, van der Staay, GWM, Michalowski, T, Jouany, J-P, Pristas, P, Javorsky, P, Kisidayova, S, Varadyova, Z, McEwan, NR, Newbold, CJ, van Alen, T, de Graaf, R, Schmid, M, Huynen, MA & Hackstein, JHP 2014, 'The symbiotic intestinal ciliates and the evolution of their hosts', European Journal of Protistology, vol. 50, no. 2, pp. 166-173. https://doi.org/10.1016/j.ejop.2014.01.004

TY - JOUR

T1 - The symbiotic intestinal ciliates and the evolution of their hosts

AU - Moon-van der Staay, Seung Yeo

AU - van der Staay, Georg W. M.

AU - Michalowski, Tadeusz

AU - Jouany, Jean-Pierre

AU - Pristas, Peter

AU - Javorsky, Peter

AU - Kisidayova, Svetlana

AU - Varadyova, Zora

AU - McEwan, Neil R.

AU - Newbold, C. Jamie

AU - van Alen, Theo

AU - de Graaf, Rob

AU - Schmid, Markus

AU - Huynen, Martijn A.

AU - Hackstein, Johannes H. P.

N1 - Funding Information: We are indebted to Prof. Dr. S. Tamminga (Wageningen), Prof. Dr. A.G.M. Tielens (Utrecht), and Dr. J. Koopman (Nijmegen) for providing rumen fluid. The technical assistance by Nadine Thomas, Nancy Nelson, and the contributions by Eli Nsabimana, Didier Macheboeuf, Martina Regensbogenova, Freda M. McIntosh are gratefully acknowledged. The authors would like to thank also the research students and trainees Minh Bao Huynh, Alvin Polenewen, Mark Holewijn and Emily Cadot for their help in isolating DNA, cloning, sequencing and performing phylogenetic analyses. This project was supported by the European Union 5th framework grants ERCULE and CIMES. The Rowett Research Institute is supported by the Scottish Executive Environmental and Rural Affairs Department. Dagmar Thierer, IZW, Berlin, and the people from Burger's Zoo, Arnhem, are gratefully acknowledged for providing faeces from various hindgut fermenters.

PY - 2014/4

Y1 - 2014/4

N2 - The evolution of sophisticated differentiations of the gastro-intestinal tract enabled herbivorous mammals to digest dietary cellulose and hemicellulose with the aid of a complex anaerobic microbiota. Distinctive symbiotic ciliates, which are unique to this habitat, are the largest representatives of this microbial community. Analyses of a total of 484 different 18S rRNA genes show that extremely complex, but related ciliate communities can occur in the rumen of cattle, sheep, goats and red deer (301 sequences). The communities in the hindgut of equids (Equus caballus, Equus quagga), and elephants (Elephas maximus, Loxodonta africanus; 162 sequences), which are clearly distinct from the ruminant ciliate biota, exhibit a much higher diversity than anticipated on the basis of their morphology. All these ciliates from the gastro-intestinal tract constitute a monophyletic group, which consists of two major taxa, i.e. Vestibuliferida and Entodiniomorphida. The ciliates from the evolutionarily older hindgut fermenters exhibit a clustering that is specific for higher taxa of their hosts, as extant species of horse and zebra on the one hand, and Africa and Indian elephant on the other hand, share related ciliates. The evolutionary younger ruminants altogether share the various entodiniomorphs and the vestibuliferids from ruminants.

AB - The evolution of sophisticated differentiations of the gastro-intestinal tract enabled herbivorous mammals to digest dietary cellulose and hemicellulose with the aid of a complex anaerobic microbiota. Distinctive symbiotic ciliates, which are unique to this habitat, are the largest representatives of this microbial community. Analyses of a total of 484 different 18S rRNA genes show that extremely complex, but related ciliate communities can occur in the rumen of cattle, sheep, goats and red deer (301 sequences). The communities in the hindgut of equids (Equus caballus, Equus quagga), and elephants (Elephas maximus, Loxodonta africanus; 162 sequences), which are clearly distinct from the ruminant ciliate biota, exhibit a much higher diversity than anticipated on the basis of their morphology. All these ciliates from the gastro-intestinal tract constitute a monophyletic group, which consists of two major taxa, i.e. Vestibuliferida and Entodiniomorphida. The ciliates from the evolutionarily older hindgut fermenters exhibit a clustering that is specific for higher taxa of their hosts, as extant species of horse and zebra on the one hand, and Africa and Indian elephant on the other hand, share related ciliates. The evolutionary younger ruminants altogether share the various entodiniomorphs and the vestibuliferids from ruminants.

KW - Caecum/colon

KW - Ciliates

KW - Community analysis

KW - Gastro-intestinal tract

KW - Rumen

KW - 18S rDNA

KW - 18S RDNA SEQUENCES

KW - PHYLOGENETIC ANALYSIS

KW - SHEEP RUMEN

KW - PROTOZOA

KW - CILIOPHORA

KW - ENTODINIOMORPHIDA

KW - ELEPHANTS

KW - DIVERSITY

KW - BACTERIA

KW - ORIGINS

UR - https://www.scopus.com/pages/publications/84896075409

U2 - 10.1016/j.ejop.2014.01.004

DO - 10.1016/j.ejop.2014.01.004

M3 - Article

SN - 0932-4739

VL - 50

SP - 166

EP - 173

JO - European Journal of Protistology

JF - European Journal of Protistology

IS - 2

ER -

The symbiotic intestinal ciliates and the evolution of their hosts

Abstract

Funding

Austrian Fields of Science 2012

Keywords

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