Unstable Relationship Between Braarudosphaera bigelowii (= Chrysochromulina parkeae) and Its Nitrogen-Fixing Endosymbiont

Marine phytoplankton are major primary producers, and their growth is primarily limited by nitrogen in the oligotrophic ocean environment. The haptophyte Braarudosphaera bigelowii possesses a cyanobacterial endosymbiont (UCYN-A), which plays a major role in nitrogen fixation in the ocean. However, h...

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Autores principales: Shigekatsu Suzuki, Masanobu Kawachi, Chinatsu Tsukakoshi, Atsushi Nakamura, Kyoko Hagino, Isao Inouye, Ken-ichiro Ishida
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Publicado: Frontiers Media S.A. 2021
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spelling oai:doaj.org-article:fe720bc96ff44226b30fe494fb5718da2021-12-03T14:43:54ZUnstable Relationship Between Braarudosphaera bigelowii (= Chrysochromulina parkeae) and Its Nitrogen-Fixing Endosymbiont1664-462X10.3389/fpls.2021.749895https://doaj.org/article/fe720bc96ff44226b30fe494fb5718da2021-12-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fpls.2021.749895/fullhttps://doaj.org/toc/1664-462XMarine phytoplankton are major primary producers, and their growth is primarily limited by nitrogen in the oligotrophic ocean environment. The haptophyte Braarudosphaera bigelowii possesses a cyanobacterial endosymbiont (UCYN-A), which plays a major role in nitrogen fixation in the ocean. However, host-symbiont interactions are poorly understood because B. bigelowii was unculturable. In this study, we sequenced the complete genome of the B. bigelowii endosymbiont and showed that it was highly reductive and closely related to UCYN-A2 (an ecotype of UCYN-A). We succeeded in establishing B. bigelowii strains and performed microscopic observations. The detailed observations showed that the cyanobacterial endosymbiont was surrounded by a single host derived membrane and divided synchronously with the host cell division. The transcriptome of B. bigelowii revealed that B. bigelowii lacked the expression of many essential genes associated with the uptake of most nitrogen compounds, except ammonia. During cultivation, some of the strains completely lost the endosymbiont. Moreover, we did not find any evidence of endosymbiotic gene transfer from the endosymbiont to the host. These findings illustrate an unstable morphological, metabolic, and genetic relationship between B. bigelowii and its endosymbiont.Shigekatsu SuzukiMasanobu KawachiChinatsu TsukakoshiAtsushi NakamuraKyoko HaginoIsao InouyeKen-ichiro IshidaFrontiers Media S.A.articlenitrogen fixationendosymbiosishaptophyteUCYN-Areductive evolutionPlant cultureSB1-1110ENFrontiers in Plant Science, Vol 12 (2021)
institution DOAJ
collection DOAJ
language EN
topic nitrogen fixation
endosymbiosis
haptophyte
UCYN-A
reductive evolution
Plant culture
SB1-1110
spellingShingle nitrogen fixation
endosymbiosis
haptophyte
UCYN-A
reductive evolution
Plant culture
SB1-1110
Shigekatsu Suzuki
Masanobu Kawachi
Chinatsu Tsukakoshi
Atsushi Nakamura
Kyoko Hagino
Isao Inouye
Ken-ichiro Ishida
Unstable Relationship Between Braarudosphaera bigelowii (= Chrysochromulina parkeae) and Its Nitrogen-Fixing Endosymbiont
description Marine phytoplankton are major primary producers, and their growth is primarily limited by nitrogen in the oligotrophic ocean environment. The haptophyte Braarudosphaera bigelowii possesses a cyanobacterial endosymbiont (UCYN-A), which plays a major role in nitrogen fixation in the ocean. However, host-symbiont interactions are poorly understood because B. bigelowii was unculturable. In this study, we sequenced the complete genome of the B. bigelowii endosymbiont and showed that it was highly reductive and closely related to UCYN-A2 (an ecotype of UCYN-A). We succeeded in establishing B. bigelowii strains and performed microscopic observations. The detailed observations showed that the cyanobacterial endosymbiont was surrounded by a single host derived membrane and divided synchronously with the host cell division. The transcriptome of B. bigelowii revealed that B. bigelowii lacked the expression of many essential genes associated with the uptake of most nitrogen compounds, except ammonia. During cultivation, some of the strains completely lost the endosymbiont. Moreover, we did not find any evidence of endosymbiotic gene transfer from the endosymbiont to the host. These findings illustrate an unstable morphological, metabolic, and genetic relationship between B. bigelowii and its endosymbiont.
format article
author Shigekatsu Suzuki
Masanobu Kawachi
Chinatsu Tsukakoshi
Atsushi Nakamura
Kyoko Hagino
Isao Inouye
Ken-ichiro Ishida
author_facet Shigekatsu Suzuki
Masanobu Kawachi
Chinatsu Tsukakoshi
Atsushi Nakamura
Kyoko Hagino
Isao Inouye
Ken-ichiro Ishida
author_sort Shigekatsu Suzuki
title Unstable Relationship Between Braarudosphaera bigelowii (= Chrysochromulina parkeae) and Its Nitrogen-Fixing Endosymbiont
title_short Unstable Relationship Between Braarudosphaera bigelowii (= Chrysochromulina parkeae) and Its Nitrogen-Fixing Endosymbiont
title_full Unstable Relationship Between Braarudosphaera bigelowii (= Chrysochromulina parkeae) and Its Nitrogen-Fixing Endosymbiont
title_fullStr Unstable Relationship Between Braarudosphaera bigelowii (= Chrysochromulina parkeae) and Its Nitrogen-Fixing Endosymbiont
title_full_unstemmed Unstable Relationship Between Braarudosphaera bigelowii (= Chrysochromulina parkeae) and Its Nitrogen-Fixing Endosymbiont
title_sort unstable relationship between braarudosphaera bigelowii (= chrysochromulina parkeae) and its nitrogen-fixing endosymbiont
publisher Frontiers Media S.A.
publishDate 2021
url https://doaj.org/article/fe720bc96ff44226b30fe494fb5718da
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