Endosymbiont Capture, a Repeated Process of Endosymbiont Transfer with Replacement in Trypanosomatids <i>Angomonas</i> spp.

Trypanosomatids of the subfamily Strigomonadinae bear permanent intracellular bacterial symbionts acquired by the common ancestor of these flagellates. However, the cospeciation pattern inherent to such relationships was revealed to be broken upon the description of <i>Angomonas ambiguus</i...

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Main Authors: Tomáš Skalický, João M. P. Alves, Anderson C. Morais, Jana Režnarová, Anzhelika Butenko, Julius Lukeš, Myrna G. Serrano, Gregory A. Buck, Marta M. G. Teixeira, Erney P. Camargo, Mandy Sanders, James A. Cotton, Vyacheslav Yurchenko, Alexei Y. Kostygov
Format: Article
Language:English
Published: MDPI AG 2021-06-01
Series:Pathogens
Subjects:
Online Access:https://www.mdpi.com/2076-0817/10/6/702
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spelling doaj-e6318c683f224d4ba0b9d17778a1414e2021-06-30T23:21:16ZengMDPI AGPathogens2076-08172021-06-011070270210.3390/pathogens10060702Endosymbiont Capture, a Repeated Process of Endosymbiont Transfer with Replacement in Trypanosomatids <i>Angomonas</i> spp.Tomáš Skalický0João M. P. Alves1Anderson C. Morais2Jana Režnarová3Anzhelika Butenko4Julius Lukeš5Myrna G. Serrano6Gregory A. Buck7Marta M. G. Teixeira8Erney P. Camargo9Mandy Sanders10James A. Cotton11Vyacheslav Yurchenko12Alexei Y. Kostygov13Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice (Budweis), Czech RepublicDepartment of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo 05508-000, BrazilDepartment of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo 05508-000, BrazilLife Science Research Centre, Faculty of Science, University of Ostrava, 710 00 Ostrava, Czech RepublicInstitute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice (Budweis), Czech RepublicInstitute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice (Budweis), Czech RepublicDepartment of Microbiology and Immunology, Virginia Commonwealth University, Richmond, VA 23298-0678, USADepartment of Microbiology and Immunology, Virginia Commonwealth University, Richmond, VA 23298-0678, USADepartment of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo 05508-000, BrazilDepartment of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo 05508-000, BrazilWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UKWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UKLife Science Research Centre, Faculty of Science, University of Ostrava, 710 00 Ostrava, Czech RepublicLife Science Research Centre, Faculty of Science, University of Ostrava, 710 00 Ostrava, Czech RepublicTrypanosomatids of the subfamily Strigomonadinae bear permanent intracellular bacterial symbionts acquired by the common ancestor of these flagellates. However, the cospeciation pattern inherent to such relationships was revealed to be broken upon the description of <i>Angomonas ambiguus</i>, which is sister to <i>A. desouzai</i>, but bears an endosymbiont genetically close to that of <i>A. deanei</i>. Based on phylogenetic inferences, it was proposed that the bacterium from <i>A. deanei</i> had been horizontally transferred to <i>A. ambiguus</i>. Here, we sequenced the bacterial genomes from two <i>A. ambiguus</i> isolates, including a new one from Papua New Guinea, and compared them with the published genome of the <i>A. deanei</i> endosymbiont, revealing differences below the interspecific level. Our phylogenetic analyses confirmed that the endosymbionts of <i>A. ambiguus</i> were obtained from <i>A. deanei</i> and, in addition, demonstrated that this occurred more than once. We propose that coinfection of the same blowfly host and the phylogenetic relatedness of the trypanosomatids facilitate such transitions, whereas the drastic difference in the occurrence of the two trypanosomatid species determines the observed direction of this process. This phenomenon is analogous to organelle (mitochondrion/plastid) capture described in multicellular organisms and, thereafter, we name it endosymbiont capture.https://www.mdpi.com/2076-0817/10/6/702genomebacterial endosymbiontsTrypanosomatidae<i>Angomonas</i>
collection DOAJ
language English
format Article
sources DOAJ
author Tomáš Skalický
João M. P. Alves
Anderson C. Morais
Jana Režnarová
Anzhelika Butenko
Julius Lukeš
Myrna G. Serrano
Gregory A. Buck
Marta M. G. Teixeira
Erney P. Camargo
Mandy Sanders
James A. Cotton
Vyacheslav Yurchenko
Alexei Y. Kostygov
spellingShingle Tomáš Skalický
João M. P. Alves
Anderson C. Morais
Jana Režnarová
Anzhelika Butenko
Julius Lukeš
Myrna G. Serrano
Gregory A. Buck
Marta M. G. Teixeira
Erney P. Camargo
Mandy Sanders
James A. Cotton
Vyacheslav Yurchenko
Alexei Y. Kostygov
Endosymbiont Capture, a Repeated Process of Endosymbiont Transfer with Replacement in Trypanosomatids <i>Angomonas</i> spp.
Pathogens
genome
bacterial endosymbionts
Trypanosomatidae
<i>Angomonas</i>
author_facet Tomáš Skalický
João M. P. Alves
Anderson C. Morais
Jana Režnarová
Anzhelika Butenko
Julius Lukeš
Myrna G. Serrano
Gregory A. Buck
Marta M. G. Teixeira
Erney P. Camargo
Mandy Sanders
James A. Cotton
Vyacheslav Yurchenko
Alexei Y. Kostygov
author_sort Tomáš Skalický
title Endosymbiont Capture, a Repeated Process of Endosymbiont Transfer with Replacement in Trypanosomatids <i>Angomonas</i> spp.
title_short Endosymbiont Capture, a Repeated Process of Endosymbiont Transfer with Replacement in Trypanosomatids <i>Angomonas</i> spp.
title_full Endosymbiont Capture, a Repeated Process of Endosymbiont Transfer with Replacement in Trypanosomatids <i>Angomonas</i> spp.
title_fullStr Endosymbiont Capture, a Repeated Process of Endosymbiont Transfer with Replacement in Trypanosomatids <i>Angomonas</i> spp.
title_full_unstemmed Endosymbiont Capture, a Repeated Process of Endosymbiont Transfer with Replacement in Trypanosomatids <i>Angomonas</i> spp.
title_sort endosymbiont capture, a repeated process of endosymbiont transfer with replacement in trypanosomatids <i>angomonas</i> spp.
publisher MDPI AG
series Pathogens
issn 2076-0817
publishDate 2021-06-01
description Trypanosomatids of the subfamily Strigomonadinae bear permanent intracellular bacterial symbionts acquired by the common ancestor of these flagellates. However, the cospeciation pattern inherent to such relationships was revealed to be broken upon the description of <i>Angomonas ambiguus</i>, which is sister to <i>A. desouzai</i>, but bears an endosymbiont genetically close to that of <i>A. deanei</i>. Based on phylogenetic inferences, it was proposed that the bacterium from <i>A. deanei</i> had been horizontally transferred to <i>A. ambiguus</i>. Here, we sequenced the bacterial genomes from two <i>A. ambiguus</i> isolates, including a new one from Papua New Guinea, and compared them with the published genome of the <i>A. deanei</i> endosymbiont, revealing differences below the interspecific level. Our phylogenetic analyses confirmed that the endosymbionts of <i>A. ambiguus</i> were obtained from <i>A. deanei</i> and, in addition, demonstrated that this occurred more than once. We propose that coinfection of the same blowfly host and the phylogenetic relatedness of the trypanosomatids facilitate such transitions, whereas the drastic difference in the occurrence of the two trypanosomatid species determines the observed direction of this process. This phenomenon is analogous to organelle (mitochondrion/plastid) capture described in multicellular organisms and, thereafter, we name it endosymbiont capture.
topic genome
bacterial endosymbionts
Trypanosomatidae
<i>Angomonas</i>
url https://www.mdpi.com/2076-0817/10/6/702
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