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On the reversibility of parasitism: adaptation to a free-living lifestyle via gene acquisitions in the diplomonad Trepomonas sp PC1
Uppsala University, Science for Life Laboratory, SciLifeLab.
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology. Uppsala University, Science for Life Laboratory, SciLifeLab.
Dalhousie Univ, Dept Biol, Halifax, NS, Canada; Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS, Canada; Univ British Columbia, Dept Bot, Vancouver, BC, Canada.
Dalhousie Univ, Dept Biol, Halifax, NS, Canada; Canadian Inst Adv Res, Integrated Microbial Biodivers Program, Toronto, ON, Canada.
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2016 (English)In: BMC Biology, ISSN 1741-7007, E-ISSN 1741-7007, Vol. 14, 62Article in journal (Refereed) Published
Abstract [en]

Background: It is generally thought that the evolutionary transition to parasitism is irreversible because it is associated with the loss of functions needed for a free-living lifestyle. Nevertheless, free-living taxa are sometimes nested within parasite clades in phylogenetic trees, which could indicate that they are secondarily free-living. Herein, we test this hypothesis by studying the genomic basis for evolutionary transitions between lifestyles in diplomonads, a group of anaerobic eukaryotes. Most described diplomonads are intestinal parasites or commensals of various animals, but there are also free-living diplomonads found in oxygen-poor environments such as marine and freshwater sediments. All these nest well within groups of parasitic diplomonads in phylogenetic trees, suggesting that they could be secondarily free-living. Results: We present a transcriptome study of Trepomonas sp. PC1, a diplomonad isolated from marine sediment. Analysis of the metabolic genes revealed a number of proteins involved in degradation of the bacterial membrane and cell wall, as well as an extended set of enzymes involved in carbohydrate degradation and nucleotide metabolism. Phylogenetic analyses showed that most of the differences in metabolic capacity between free-living Trepomonas and the parasitic diplomonads are due to recent acquisitions of bacterial genes via gene transfer. Interestingly, one of the acquired genes encodes a ribonucleotide reductase, which frees Trepomonas from the need to scavenge deoxyribonucleosides. The transcriptome included a gene encoding squalene-tetrahymanol cyclase. This enzyme synthesizes the sterol substitute tetrahymanol in the absence of oxygen, potentially allowing Trepomonas to thrive under anaerobic conditions as a free-living bacterivore, without depending on sterols from other eukaryotes. Conclusions: Our findings are consistent with the phylogenetic evidence that the last common ancestor of diplomonads was dependent on a host and that Trepomonas has adapted secondarily to a free-living lifestyle. We believe that similar studies of other groups where free-living taxa are nested within parasites could reveal more examples of secondarily free-living eukaryotes.

Place, publisher, year, edition, pages
2016. Vol. 14, 62
Keyword [en]
Free-living; Parasite; Diplomonad; Dollo's law; Reversibility; Trepomonas; Horizontal gene transfer; Ribonucleotide reductase
National Category
Evolutionary Biology
URN: urn:nbn:se:uu:diva-251638DOI: 10.1186/s12915-016-0284-zISI: 000381184600002PubMedID: 27480115OAI: oai:DiVA.org:uu-251638DiVA: diva2:807198
Swedish Research Council Formas, 2010-899Science for Life Laboratory - a national resource center for high-throughput molecular bioscienceSwedish Research Council

Correction in: BMC Biology, vol. 14, article number 77

DOI: 10.1186/s12915-016-0302-1

Available from: 2015-04-23 Created: 2015-04-22 Last updated: 2016-10-07Bibliographically approved
In thesis
1. Comparative Genomics in Diplomonads: Lifestyle Variations Revealed at Genetic Level
Open this publication in new window or tab >>Comparative Genomics in Diplomonads: Lifestyle Variations Revealed at Genetic Level
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

As sequencing technologies advance genome studies are becoming a basic tool for studying an organism, and with more genomes available comparative genomics is maturing into a powerful tool for biological research. This thesis demonstrates the strength of a comparative genomics approach on a group of understudied eukaryotes, the diplomonads.

Diplomonads are a group of single cell eukaryotic flagellates living in oxygen-poor environments. Most diplomonads are intestinal parasites, like the well-studied human parasite Giardia intestinalis. There are seven different G. intestinalis assemblages (genotypes) affecting different hosts, and it’s under debate whether these are one species. A genome-wide study of three G. intestinalis genomes from different assemblages reveals little inter-assemblage sexual recombination, supporting that the different G. intestinalis assemblages are genetically isolated and thus different species.

A genomic comparison between the fish parasite S. salmonicida and G. intestinalis reveals genetic differences reflecting differences in their parasitic lifestyles. There is a tighter transcriptional regulation and a larger metabolic reservoir in S. salmonicida, likely adaptations to the fluctuating environments it encounters during its systemic infection compared to G. intestinalis which is a strict intestinal parasite.

The S. salmonicida genome analysis also discovers genes involved in energy metabolism. Some of these are experimentally shown to localize to mitochondrion-related organelles in S. salmonicida, indicating that they possess energy-producing organelles that should be classified as hydrogenosomes, as opposed to the mitosomes in G. intestinalis.

A transcriptome analysis of the free-living Trepomonas is compared with genomic data from the two parasitic diplomonads. The majority of the genes associated with a free-living lifestyle, like phagocytosis and a larger metabolic capacity, are of prokaryotic origin. This suggests that the ancestor of the free-living diplomonad was likely host-associated and that the free-living lifestyle is a secondary adaptation acquired through horizontal gene transfers. 

In conclusion, this thesis uses different comparative genomics approaches to broaden the knowledge on diplomonad diversity and to provide more insight into how the lifestyle differences are reflected on the genetic level. The bioinformatics pipelines and expertise gained in these studies will be useful in other projects in diplomonads and other organismal groups.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2015. 64 p.
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1261
comparative genomics, Giardia intestinalis, Spironucleus salmonicida, Trepomonas, diplomonad, intestinal parasite, free-living, sexual recombination, hydrogenosome, horizontal gene transfer
National Category
Bioinformatics and Systems Biology Evolutionary Biology Microbiology
Research subject
Biology with specialization in Molecular Evolution
urn:nbn:se:uu:diva-251650 (URN)978-91-554-9262-5 (ISBN)
Public defence
2015-06-12, BMC, B41, Husargatan 3, Uppsala, 13:00 (English)
Available from: 2015-05-22 Created: 2015-04-23 Last updated: 2015-07-07Bibliographically approved

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