Open Access Highly Accessed Research article

A genomic survey of the fish parasite Spironucleus salmonicida indicates genomic plasticity among diplomonads and significant lateral gene transfer in eukaryote genome evolution

Jan O Andersson1*, Åsa M Sjögren26, David S Horner37, Colleen A Murphy4, Patricia L Dyal3, Staffan G Svärd1, John M Logsdon5, Mark A Ragan48, Robert P Hirt39 and Andrew J Roger2

Author Affiliations

1 Institute of Cell and Molecular Biology, Uppsala University, Biomedical Center, Uppsala, Sweden

2 The Canadian Institute for Advanced Research, Program in Evolutionary Biology, Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Nova Scotia, Canada

3 Department of Zoology, The Natural History Museum, London, UK

4 Institute for Marine Biosciences, National Research Council of Canada, Halifax, Nova Scotia, Canada

5 Roy J. Carver Center for Comparative Genomics, Department of Biological Sciences, University of Iowa, Iowa City, USA

6 Department of Microbiology, Swedish University of Agricultural Sciences, Uppsala, Sweden

7 Dipartimento di Scienze Biomolecolare e Biotecnologie, University of Milan, Milan, Italy

8 ARC Centre in Bioinformatics, and Institute for Molecular Bioscience, The University of Queensland, Brisbane, Australia

9 School of Biology, The Devonshire building, The University of Newcastle upon Tyne, UK

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BMC Genomics 2007, 8:51  doi:10.1186/1471-2164-8-51

Published: 14 February 2007

Abstract

Background

Comparative genomic studies of the mitochondrion-lacking protist group Diplomonadida (diplomonads) has been lacking, although Giardia lamblia has been intensively studied. We have performed a sequence survey project resulting in 2341 expressed sequence tags (EST) corresponding to 853 unique clones, 5275 genome survey sequences (GSS), and eleven finished contigs from the diplomonad fish parasite Spironucleus salmonicida (previously described as S. barkhanus).

Results

The analyses revealed a compact genome with few, if any, introns and very short 3' untranslated regions. Strikingly different patterns of codon usage were observed in genes corresponding to frequently sampled ESTs versus genes poorly sampled, indicating that translational selection is influencing the codon usage of highly expressed genes. Rigorous phylogenomic analyses identified 84 genes – mostly encoding metabolic proteins – that have been acquired by diplomonads or their relatively close ancestors via lateral gene transfer (LGT). Although most acquisitions were from prokaryotes, more than a dozen represent likely transfers of genes between eukaryotic lineages. Many genes that provide novel insights into the genetic basis of the biology and pathogenicity of this parasitic protist were identified including 149 that putatively encode variant-surface cysteine-rich proteins which are candidate virulence factors. A number of genomic properties that distinguish S. salmonicida from its human parasitic relative G. lamblia were identified such as nineteen putative lineage-specific gene acquisitions, distinct mutational biases and codon usage and distinct polyadenylation signals.

Conclusion

Our results highlight the power of comparative genomic studies to yield insights into the biology of parasitic protists and the evolution of their genomes, and suggest that genetic exchange between distantly-related protist lineages may be occurring at an appreciable rate in eukaryote genome evolution.