Novel Trypanosomatid-Bacterium Association: Evolution of Endosymbiosis in Action

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ABSTRACT

We describe a novel symbiotic association between a kinetoplastid protist, Novymonas esmeraldas gen. nov., sp. nov., and an intracytoplasmic bacterium, “ Candidatus Pandoraea novymonadis” sp. nov., discovered as a result of a broad-scale survey of insect trypanosomatid biodiversity in Ecuador. We characterize this association by describing the morphology of both organisms, as well as their interactions, and by establishing their phylogenetic affinities. Importantly, neither partner is closely related to other known organisms previously implicated in eukaryote-bacterial symbiosis. This symbiotic association seems to be relatively recent, as the host does not exert a stringent control over the number of bacteria harbored in its cytoplasm. We argue that this unique relationship may represent a suitable model for studying the initial stages of establishment of endosymbiosis between a single-cellular eukaryote and a prokaryote. Based on phylogenetic analyses, Novymonas could be considered a proxy for the insect-only ancestor of the dixenous genus Leishmania and shed light on the origin of the two-host life cycle within the subfamily Leishmaniinae.

IMPORTANCE

The parasitic trypanosomatid protist Novymonas esmeraldas gen. nov., sp. nov. entered into endosymbiosis with the bacterium “ Ca. Pandoraea novymonadis” sp. nov. This novel and rather unstable interaction shows several signs of relatively recent establishment, qualifying it as a potentially unique transient stage in the increasingly complex range of eukaryotic-prokaryotic relationships.

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Most cited references 64

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Learning how to live together: genomic insights into prokaryote-animal symbioses.

Andrés Moya, Juli Peretó, Rosario Gil … (2008)

Our understanding of prokaryote-eukaryote symbioses as a source of evolutionary innovation has been rapidly increased by the advent of genomics, which has made possible the biological study of uncultivable endosymbionts. Genomics is allowing the dissection of the evolutionary process that starts with host invasion then progresses from facultative to obligate symbiosis and ends with replacement by, or coexistence with, new symbionts. Moreover, genomics has provided important clues on the mechanisms driving the genome-reduction process, the functions that are retained by the endosymbionts, the role of the host, and the factors that might determine whether the association will become parasitic or mutualistic.

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The number, speed, and impact of plastid endosymbioses in eukaryotic evolution.

Patrick J Keeling (2013)

Plastids (chloroplasts) have long been recognized to have originated by endosymbiosis of a cyanobacterium, but their subsequent evolutionary history has proved complex because they have also moved between eukaryotes during additional rounds of secondary and tertiary endosymbioses. Much of this history has been revealed by genomic analyses, but some debates remain unresolved, in particular those relating to secondary red plastids of the chromalveolates, especially cryptomonads. Here, I examine several fundamental questions and assumptions about endosymbiosis and plastid evolution, including the number of endosymbiotic events needed to explain plastid diversity, whether the genetic contribution of the endosymbionts to the host genome goes far beyond plastid-targeted genes, and whether organelle origins are best viewed as a singular transition involving one symbiont or as a gradual transition involving a long line of transient food/symbionts. I also discuss a possible link between transporters and the evolution of protein targeting in organelle integration.

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Evolutionary and geographical history of the Leishmania donovani complex with a revision of current taxonomy.

Eva Chocholova, Ketty Soteriadou, Jean-Claude Dujardin … (2007)

Leishmaniasis is a geographically widespread severe disease, with an increasing incidence of two million cases per year and 350 million people from 88 countries at risk. The causative agents are species of Leishmania, a protozoan flagellate. Visceral leishmaniasis, the most severe form of the disease, lethal if untreated, is caused by species of the Leishmania donovani complex. These species are morphologically indistinguishable but have been identified by molecular methods, predominantly multilocus enzyme electrophoresis. We have conducted a multifactorial genetic analysis that includes DNA sequences of protein-coding genes as well as noncoding segments, microsatellites, restriction-fragment length polymorphisms, and randomly amplified polymorphic DNAs, for a total of approximately 18,000 characters for each of 25 geographically representative strains. Genotype is strongly correlated with geographical (continental) origin, but not with current taxonomy or clinical outcome. We propose a new taxonomy, in which Leishmania infantum and L. donovani are the only recognized species of the L. donovani complex, and we present an evolutionary hypothesis for the origin and dispersal of the species. The genus Leishmania may have originated in South America, but diversified after migration into Asia. L. donovani and L. infantum diverged approximately 1 Mya, with further divergence of infraspecific genetic groups between 0.4 and 0.8 Mya. The prevailing mode of reproduction is clonal, but there is evidence of genetic exchange between strains, particularly in Africa.

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Author and article information

Journal

Journal ID (nlm-ta): mBio

Journal ID (iso-abbrev): MBio

Journal ID (hwp): mbio

Journal ID (pmc): mbio

Journal ID (publisher-id): mBio

Title: mBio

Publisher: American Society of Microbiology (1752 N St., N.W., Washington, DC )

ISSN (Electronic): 2150-7511

Publication date (Electronic): 15 March 2016

Publication date Collection: Mar-Apr 2016

Volume: 7

Issue: 2

Electronic Location Identifier: e01985-15

Affiliations

[a ]Life Science Research Centre, Faculty of Science, University of Ostrava, Ostrava, Czech Republic

[b ]Biology Centre, Institute of Parasitology, Czech Academy of Sciences, České Budějovice (Budweis), Czech Republic

[c ]Department of Biology, University of California at Riverside, Riverside, California, USA

[d ]Department of Parasitology, Faculty of Science, Charles University, Prague, Czech Republic

[e ]Faculty of Sciences, University of South Bohemia, České Budějovice (Budweis), Czech Republic

[f ]Canadian Institute for Advanced Research, Toronto, Ontario, Canada

[g ]Department of Pathology, Albert Einstein College of Medicine, Bronx, New York, USA

Author notes

Address correspondence to Vyacheslav Yurchenko, vyacheslav.yurchenko@ 123456osu.cz , and Julius Lukeš, jula@ 123456paru.cas.cz .

A.Y.K., E.D. and A.G.-I. contributed equally to this work.

Editor Keith Gull, University of Oxford

This article is a direct contribution from a Fellow of the American Academy of Microbiology.

Article

Publisher ID: mBio01985-15

DOI: 10.1128/mBio.01985-15

PMC ID: 4807368

PubMed ID: 26980834

SO-VID: 8bcf108e-890d-404a-8cf2-113e5f1261fd

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 1 December 2015

Date accepted : 28 January 2016

Page count

supplementary-material: 2, Figures: 6, Tables: 0, Equations: 0, References: 79, Pages: 12, Words: 9797

Funding

This work, including the efforts of Julius Lukeš, was funded by Czech Science Foundation (14-23986S), COST action (CM 1307), and Seventh Framework Programme (FP7) (316304). This work, including the efforts of Vyacheslav Yurchenko and Alexei Y. Kostygov, was funded by Moravskoslezsky Kraj Research Initiative (DT1/RRC/2013-2014). This work, including the efforts of Vyacheslav Yurchenko, was funded by Moravskoslezsky Kraj Research Initiative (00955/RRC/2015). This work, including the efforts of Anastasiia Grybchuk-Ieremenko, was funded by Grant from University of Ostrava (SGS27/PrF/2015). The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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cover-date March/April 2016

ScienceOpen disciplines: Life sciences

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ScienceOpen disciplines: Life sciences

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