The Rubisco small subunits in the green algal genus Chloromonas provide insights into evolutionary loss of the eukaryotic carbon-concentrating organelle, the pyrenoid
Abstract Background Pyrenoids are protein microcompartments composed mainly of Rubisco that are localized in the chloroplasts of many photosynthetic organisms. Pyrenoids contribute to the CO2-concentrating mechanism. This organelle has been lost many times during algal/plant evolution, including wit...
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doaj-e25176ef30ad4137a0e28fcb6e02a9182021-08-29T11:05:22ZengBMCBMC Ecology and Evolution2730-71822021-01-0121111410.1186/s12862-020-01733-1The Rubisco small subunits in the green algal genus Chloromonas provide insights into evolutionary loss of the eukaryotic carbon-concentrating organelle, the pyrenoidRyo Matsuzaki0Shigekatsu Suzuki1Haruyo Yamaguchi2Masanobu Kawachi3Yu Kanesaki4Hirofumi Yoshikawa5Toshiyuki Mori6Hisayoshi Nozaki7Center for Environmental Biology and Ecosystem Studies, National Institute for Environmental StudiesCenter for Environmental Biology and Ecosystem Studies, National Institute for Environmental StudiesCenter for Environmental Biology and Ecosystem Studies, National Institute for Environmental StudiesCenter for Environmental Biology and Ecosystem Studies, National Institute for Environmental StudiesResearch Institute of Green Science and Technology, Shizuoka UniversityDepartment of Bioscience, Tokyo University of AgricultureDepartment of Tropical Medicine and Parasitology, Juntendo UniversityDepartment of Biological Sciences, Graduate School of Science, The University of TokyoAbstract Background Pyrenoids are protein microcompartments composed mainly of Rubisco that are localized in the chloroplasts of many photosynthetic organisms. Pyrenoids contribute to the CO2-concentrating mechanism. This organelle has been lost many times during algal/plant evolution, including with the origin of land plants. The molecular basis of the evolutionary loss of pyrenoids is a major topic in evolutionary biology. Recently, it was hypothesized that pyrenoid formation is controlled by the hydrophobicity of the two helices on the surface of the Rubisco small subunit (RBCS), but the relationship between hydrophobicity and pyrenoid loss during the evolution of closely related algal/plant lineages has not been examined. Here, we focused on, the Reticulata group of the unicellular green algal genus Chloromonas, within which pyrenoids are present in some species, although they are absent in the closely related species. Results Based on de novo transcriptome analysis and Sanger sequencing of cloned reverse transcription-polymerase chain reaction products, rbcS sequences were determined from 11 strains of two pyrenoid-lacking and three pyrenoid-containing species of the Reticulata group. We found that the hydrophobicity of the RBCS helices was roughly correlated with the presence or absence of pyrenoids within the Reticulata group and that a decrease in the hydrophobicity of the RBCS helices may have primarily caused pyrenoid loss during the evolution of this group. Conclusions Although we suggest that the observed correlation may only exist for the Reticulata group, this is still an interesting study that provides novel insight into a potential mechanism determining initial evolutionary steps of gain and loss of the pyrenoid.https://doi.org/10.1186/s12862-020-01733-1ChloromonasEvolutionGreen algaeHydrophobicity of RBCS helicesPyrenoidPyrenoid loss |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Ryo Matsuzaki Shigekatsu Suzuki Haruyo Yamaguchi Masanobu Kawachi Yu Kanesaki Hirofumi Yoshikawa Toshiyuki Mori Hisayoshi Nozaki |
spellingShingle |
Ryo Matsuzaki Shigekatsu Suzuki Haruyo Yamaguchi Masanobu Kawachi Yu Kanesaki Hirofumi Yoshikawa Toshiyuki Mori Hisayoshi Nozaki The Rubisco small subunits in the green algal genus Chloromonas provide insights into evolutionary loss of the eukaryotic carbon-concentrating organelle, the pyrenoid BMC Ecology and Evolution Chloromonas Evolution Green algae Hydrophobicity of RBCS helices Pyrenoid Pyrenoid loss |
author_facet |
Ryo Matsuzaki Shigekatsu Suzuki Haruyo Yamaguchi Masanobu Kawachi Yu Kanesaki Hirofumi Yoshikawa Toshiyuki Mori Hisayoshi Nozaki |
author_sort |
Ryo Matsuzaki |
title |
The Rubisco small subunits in the green algal genus Chloromonas provide insights into evolutionary loss of the eukaryotic carbon-concentrating organelle, the pyrenoid |
title_short |
The Rubisco small subunits in the green algal genus Chloromonas provide insights into evolutionary loss of the eukaryotic carbon-concentrating organelle, the pyrenoid |
title_full |
The Rubisco small subunits in the green algal genus Chloromonas provide insights into evolutionary loss of the eukaryotic carbon-concentrating organelle, the pyrenoid |
title_fullStr |
The Rubisco small subunits in the green algal genus Chloromonas provide insights into evolutionary loss of the eukaryotic carbon-concentrating organelle, the pyrenoid |
title_full_unstemmed |
The Rubisco small subunits in the green algal genus Chloromonas provide insights into evolutionary loss of the eukaryotic carbon-concentrating organelle, the pyrenoid |
title_sort |
rubisco small subunits in the green algal genus chloromonas provide insights into evolutionary loss of the eukaryotic carbon-concentrating organelle, the pyrenoid |
publisher |
BMC |
series |
BMC Ecology and Evolution |
issn |
2730-7182 |
publishDate |
2021-01-01 |
description |
Abstract Background Pyrenoids are protein microcompartments composed mainly of Rubisco that are localized in the chloroplasts of many photosynthetic organisms. Pyrenoids contribute to the CO2-concentrating mechanism. This organelle has been lost many times during algal/plant evolution, including with the origin of land plants. The molecular basis of the evolutionary loss of pyrenoids is a major topic in evolutionary biology. Recently, it was hypothesized that pyrenoid formation is controlled by the hydrophobicity of the two helices on the surface of the Rubisco small subunit (RBCS), but the relationship between hydrophobicity and pyrenoid loss during the evolution of closely related algal/plant lineages has not been examined. Here, we focused on, the Reticulata group of the unicellular green algal genus Chloromonas, within which pyrenoids are present in some species, although they are absent in the closely related species. Results Based on de novo transcriptome analysis and Sanger sequencing of cloned reverse transcription-polymerase chain reaction products, rbcS sequences were determined from 11 strains of two pyrenoid-lacking and three pyrenoid-containing species of the Reticulata group. We found that the hydrophobicity of the RBCS helices was roughly correlated with the presence or absence of pyrenoids within the Reticulata group and that a decrease in the hydrophobicity of the RBCS helices may have primarily caused pyrenoid loss during the evolution of this group. Conclusions Although we suggest that the observed correlation may only exist for the Reticulata group, this is still an interesting study that provides novel insight into a potential mechanism determining initial evolutionary steps of gain and loss of the pyrenoid. |
topic |
Chloromonas Evolution Green algae Hydrophobicity of RBCS helices Pyrenoid Pyrenoid loss |
url |
https://doi.org/10.1186/s12862-020-01733-1 |
work_keys_str_mv |
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