Horizontal gene transfer of microbial cellulases into nematode genomes is associated with functional assimilation and gene turnover

<p>Abstract</p> <p>Background</p> <p>Natural acquisition of novel genes from other organisms by horizontal or lateral gene transfer is well established for microorganisms. There is now growing evidence that horizontal gene transfer also plays important roles in the evol...

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Main Authors: Dieterich Christoph, Bartelmes Gabi, Schuster Lisa N, Mayer Werner E, Sommer Ralf J
Format: Article
Language:English
Published: BMC 2011-01-01
Series:BMC Evolutionary Biology
Online Access:http://www.biomedcentral.com/1471-2148/11/13
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spelling doaj-5dd24286ba584c198c0ae1f3817a50a82021-09-02T09:05:34ZengBMCBMC Evolutionary Biology1471-21482011-01-011111310.1186/1471-2148-11-13Horizontal gene transfer of microbial cellulases into nematode genomes is associated with functional assimilation and gene turnoverDieterich ChristophBartelmes GabiSchuster Lisa NMayer Werner ESommer Ralf J<p>Abstract</p> <p>Background</p> <p>Natural acquisition of novel genes from other organisms by horizontal or lateral gene transfer is well established for microorganisms. There is now growing evidence that horizontal gene transfer also plays important roles in the evolution of eukaryotes. Genome-sequencing and EST projects of plant and animal associated nematodes such as <it>Brugia</it>, <it>Meloidogyne</it>, <it>Bursaphelenchus </it>and <it>Pristionchus </it>indicate horizontal gene transfer as a key adaptation towards parasitism and pathogenicity. However, little is known about the functional activity and evolutionary longevity of genes acquired by horizontal gene transfer and the mechanisms favoring such processes.</p> <p>Results</p> <p>We examine the transfer of cellulase genes to the free-living and beetle-associated nematode <it>Pristionchus pacificus</it>, for which detailed phylogenetic knowledge is available, to address predictions by evolutionary theory for successful gene transfer. We used transcriptomics in seven <it>Pristionchus </it>species and three other related diplogastrid nematodes with a well-defined phylogenetic framework to study the evolution of ancestral cellulase genes acquired by horizontal gene transfer. We performed intra-species, inter-species and inter-genic analysis by comparing the transcriptomes of these ten species and tested for cellulase activity in each species. Species with cellulase genes in their transcriptome always exhibited cellulase activity indicating functional integration into the host's genome and biology. The phylogenetic profile of cellulase genes was congruent with the species phylogeny demonstrating gene longevity. Cellulase genes show notable turnover with elevated birth and death rates. Comparison by sequencing of three selected cellulase genes in 24 natural isolates of <it>Pristionchus pacificus </it>suggests these high evolutionary dynamics to be associated with copy number variations and positive selection.</p> <p>Conclusion</p> <p>We could demonstrate functional integration of acquired cellulase genes into the nematode's biology as predicted by theory. Thus, functional assimilation, remarkable gene turnover and selection might represent key features of horizontal gene transfer events in nematodes.</p> http://www.biomedcentral.com/1471-2148/11/13
collection DOAJ
language English
format Article
sources DOAJ
author Dieterich Christoph
Bartelmes Gabi
Schuster Lisa N
Mayer Werner E
Sommer Ralf J
spellingShingle Dieterich Christoph
Bartelmes Gabi
Schuster Lisa N
Mayer Werner E
Sommer Ralf J
Horizontal gene transfer of microbial cellulases into nematode genomes is associated with functional assimilation and gene turnover
BMC Evolutionary Biology
author_facet Dieterich Christoph
Bartelmes Gabi
Schuster Lisa N
Mayer Werner E
Sommer Ralf J
author_sort Dieterich Christoph
title Horizontal gene transfer of microbial cellulases into nematode genomes is associated with functional assimilation and gene turnover
title_short Horizontal gene transfer of microbial cellulases into nematode genomes is associated with functional assimilation and gene turnover
title_full Horizontal gene transfer of microbial cellulases into nematode genomes is associated with functional assimilation and gene turnover
title_fullStr Horizontal gene transfer of microbial cellulases into nematode genomes is associated with functional assimilation and gene turnover
title_full_unstemmed Horizontal gene transfer of microbial cellulases into nematode genomes is associated with functional assimilation and gene turnover
title_sort horizontal gene transfer of microbial cellulases into nematode genomes is associated with functional assimilation and gene turnover
publisher BMC
series BMC Evolutionary Biology
issn 1471-2148
publishDate 2011-01-01
description <p>Abstract</p> <p>Background</p> <p>Natural acquisition of novel genes from other organisms by horizontal or lateral gene transfer is well established for microorganisms. There is now growing evidence that horizontal gene transfer also plays important roles in the evolution of eukaryotes. Genome-sequencing and EST projects of plant and animal associated nematodes such as <it>Brugia</it>, <it>Meloidogyne</it>, <it>Bursaphelenchus </it>and <it>Pristionchus </it>indicate horizontal gene transfer as a key adaptation towards parasitism and pathogenicity. However, little is known about the functional activity and evolutionary longevity of genes acquired by horizontal gene transfer and the mechanisms favoring such processes.</p> <p>Results</p> <p>We examine the transfer of cellulase genes to the free-living and beetle-associated nematode <it>Pristionchus pacificus</it>, for which detailed phylogenetic knowledge is available, to address predictions by evolutionary theory for successful gene transfer. We used transcriptomics in seven <it>Pristionchus </it>species and three other related diplogastrid nematodes with a well-defined phylogenetic framework to study the evolution of ancestral cellulase genes acquired by horizontal gene transfer. We performed intra-species, inter-species and inter-genic analysis by comparing the transcriptomes of these ten species and tested for cellulase activity in each species. Species with cellulase genes in their transcriptome always exhibited cellulase activity indicating functional integration into the host's genome and biology. The phylogenetic profile of cellulase genes was congruent with the species phylogeny demonstrating gene longevity. Cellulase genes show notable turnover with elevated birth and death rates. Comparison by sequencing of three selected cellulase genes in 24 natural isolates of <it>Pristionchus pacificus </it>suggests these high evolutionary dynamics to be associated with copy number variations and positive selection.</p> <p>Conclusion</p> <p>We could demonstrate functional integration of acquired cellulase genes into the nematode's biology as predicted by theory. Thus, functional assimilation, remarkable gene turnover and selection might represent key features of horizontal gene transfer events in nematodes.</p>
url http://www.biomedcentral.com/1471-2148/11/13
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