Life Cycle, Ultrastructure, and Phylogeny of New Diplonemids and Their Endosymbiotic Bacteria

ABSTRACT Diplonemids represent a hyperdiverse and abundant yet poorly studied group of marine protists. Here we describe two new members of the genus Diplonema (Diplonemea, Euglenozoa), Diplonema japonicum sp. nov. and Diplonema aggregatum sp. nov., based on life cycle, morphology, and 18S rRNA gene...

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Autores principales: Daria Tashyreva, Galina Prokopchuk, Jan Votýpka, Akinori Yabuki, Aleš Horák, Julius Lukeš
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:d306f612122942a995008744ef3095272021-11-15T15:53:26ZLife Cycle, Ultrastructure, and Phylogeny of New Diplonemids and Their Endosymbiotic Bacteria10.1128/mBio.02447-172150-7511https://doaj.org/article/d306f612122942a995008744ef3095272018-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02447-17https://doaj.org/toc/2150-7511ABSTRACT Diplonemids represent a hyperdiverse and abundant yet poorly studied group of marine protists. Here we describe two new members of the genus Diplonema (Diplonemea, Euglenozoa), Diplonema japonicum sp. nov. and Diplonema aggregatum sp. nov., based on life cycle, morphology, and 18S rRNA gene sequences. Along with euglenozoan apomorphies, they contain several unique features. Their life cycle is complex, consisting of a trophic stage that is, following the depletion of nutrients, transformed into a sessile stage and subsequently into a swimming stage. The latter two stages are characterized by the presence of tubular extrusomes and the emergence of a paraflagellar rod, the supportive structure of the flagellum, which is prominently lacking in the trophic stage. These two stages also differ dramatically in motility and flagellar size. Both diplonemid species host endosymbiotic bacteria that are closely related to each other and constitute a novel branch within Holosporales, for which a new genus, “Candidatus Cytomitobacter” gen. nov., has been established. Remarkably, the number of endosymbionts in the cytoplasm varies significantly, as does their localization within the cell, where they seem to penetrate the mitochondrion, a rare occurrence. IMPORTANCE We describe the morphology, behavior, and life cycle of two new Diplonema species that established a relationship with two Holospora-like bacteria in the first report of an endosymbiosis in diplonemids. Both endosymbionts reside in the cytoplasm and the mitochondrion, which establishes an extremely rare case. Within their life cycle, the diplonemids undergo transformation from a trophic to a sessile and eventually a highly motile swimming stage. These stages differ in several features, such as the presence or absence of tubular extrusomes and a paraflagellar rod, along with the length of the flagella. These morphological and behavioral interstage differences possibly reflect distinct functions in dispersion and invasion of the host and/or prey and may provide novel insight into the virtually unknown function of diplonemids in the oceanic ecosystem.Daria TashyrevaGalina ProkopchukJan VotýpkaAkinori YabukiAleš HorákJulius LukešAmerican Society for MicrobiologyarticleHolosporalesdiplonemidendosymbiontslife cycleultrastructureMicrobiologyQR1-502ENmBio, Vol 9, Iss 2 (2018)
institution DOAJ
collection DOAJ
language EN
topic Holosporales
diplonemid
endosymbionts
life cycle
ultrastructure
Microbiology
QR1-502
spellingShingle Holosporales
diplonemid
endosymbionts
life cycle
ultrastructure
Microbiology
QR1-502
Daria Tashyreva
Galina Prokopchuk
Jan Votýpka
Akinori Yabuki
Aleš Horák
Julius Lukeš
Life Cycle, Ultrastructure, and Phylogeny of New Diplonemids and Their Endosymbiotic Bacteria
description ABSTRACT Diplonemids represent a hyperdiverse and abundant yet poorly studied group of marine protists. Here we describe two new members of the genus Diplonema (Diplonemea, Euglenozoa), Diplonema japonicum sp. nov. and Diplonema aggregatum sp. nov., based on life cycle, morphology, and 18S rRNA gene sequences. Along with euglenozoan apomorphies, they contain several unique features. Their life cycle is complex, consisting of a trophic stage that is, following the depletion of nutrients, transformed into a sessile stage and subsequently into a swimming stage. The latter two stages are characterized by the presence of tubular extrusomes and the emergence of a paraflagellar rod, the supportive structure of the flagellum, which is prominently lacking in the trophic stage. These two stages also differ dramatically in motility and flagellar size. Both diplonemid species host endosymbiotic bacteria that are closely related to each other and constitute a novel branch within Holosporales, for which a new genus, “Candidatus Cytomitobacter” gen. nov., has been established. Remarkably, the number of endosymbionts in the cytoplasm varies significantly, as does their localization within the cell, where they seem to penetrate the mitochondrion, a rare occurrence. IMPORTANCE We describe the morphology, behavior, and life cycle of two new Diplonema species that established a relationship with two Holospora-like bacteria in the first report of an endosymbiosis in diplonemids. Both endosymbionts reside in the cytoplasm and the mitochondrion, which establishes an extremely rare case. Within their life cycle, the diplonemids undergo transformation from a trophic to a sessile and eventually a highly motile swimming stage. These stages differ in several features, such as the presence or absence of tubular extrusomes and a paraflagellar rod, along with the length of the flagella. These morphological and behavioral interstage differences possibly reflect distinct functions in dispersion and invasion of the host and/or prey and may provide novel insight into the virtually unknown function of diplonemids in the oceanic ecosystem.
format article
author Daria Tashyreva
Galina Prokopchuk
Jan Votýpka
Akinori Yabuki
Aleš Horák
Julius Lukeš
author_facet Daria Tashyreva
Galina Prokopchuk
Jan Votýpka
Akinori Yabuki
Aleš Horák
Julius Lukeš
author_sort Daria Tashyreva
title Life Cycle, Ultrastructure, and Phylogeny of New Diplonemids and Their Endosymbiotic Bacteria
title_short Life Cycle, Ultrastructure, and Phylogeny of New Diplonemids and Their Endosymbiotic Bacteria
title_full Life Cycle, Ultrastructure, and Phylogeny of New Diplonemids and Their Endosymbiotic Bacteria
title_fullStr Life Cycle, Ultrastructure, and Phylogeny of New Diplonemids and Their Endosymbiotic Bacteria
title_full_unstemmed Life Cycle, Ultrastructure, and Phylogeny of New Diplonemids and Their Endosymbiotic Bacteria
title_sort life cycle, ultrastructure, and phylogeny of new diplonemids and their endosymbiotic bacteria
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/d306f612122942a995008744ef309527
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