Genome analysis of Parmales, the sister group of diatoms, reveals the evolutionary specialization of diatoms from phago-mixotrophs to photoautotrophs
Abstract The order Parmales (class Bolidophyceae) is a minor group of pico-sized eukaryotic marine phytoplankton that contains species with cells surrounded by silica plates. Previous studies revealed that Parmales is a member of ochrophytes and sister to diatoms (phylum Bacillariophyta), the most s...
| Main Authors: | , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2023-07-01
|
| Series: | Communications Biology |
| Online Access: | https://doi.org/10.1038/s42003-023-05002-x |
| _version_ | 1797784487533215744 |
|---|---|
| author | Hiroki Ban Shinya Sato Shinya Yoshikawa Kazumasa Yamada Yoji Nakamura Mutsuo Ichinomiya Naoki Sato Romain Blanc-Mathieu Hisashi Endo Akira Kuwata Hiroyuki Ogata |
| author_facet | Hiroki Ban Shinya Sato Shinya Yoshikawa Kazumasa Yamada Yoji Nakamura Mutsuo Ichinomiya Naoki Sato Romain Blanc-Mathieu Hisashi Endo Akira Kuwata Hiroyuki Ogata |
| author_sort | Hiroki Ban |
| collection | DOAJ |
| description | Abstract The order Parmales (class Bolidophyceae) is a minor group of pico-sized eukaryotic marine phytoplankton that contains species with cells surrounded by silica plates. Previous studies revealed that Parmales is a member of ochrophytes and sister to diatoms (phylum Bacillariophyta), the most successful phytoplankton group in the modern ocean. Therefore, parmalean genomes can serve as a reference to elucidate both the evolutionary events that differentiated these two lineages and the genomic basis for the ecological success of diatoms vs. the more cryptic lifestyle of parmaleans. Here, we compare the genomes of eight parmaleans and five diatoms to explore their physiological and evolutionary differences. Parmaleans are predicted to be phago-mixotrophs. By contrast, diatoms have lost genes related to phagocytosis, indicating the ecological specialization from phago-mixotrophy to photoautotrophy in their early evolution. Furthermore, diatoms show significant enrichment in gene sets involved in nutrient uptake and metabolism, including iron and silica, in comparison with parmaleans. Overall, our results suggest a strong evolutionary link between the loss of phago-mixotrophy and specialization to a silicified photoautotrophic life stage early in diatom evolution after diverging from the Parmales lineage. |
| first_indexed | 2024-03-13T00:40:36Z |
| format | Article |
| id | doaj.art-61b92f68a9e446d29fa355ee059735e3 |
| institution | Directory Open Access Journal |
| issn | 2399-3642 |
| language | English |
| last_indexed | 2024-03-13T00:40:36Z |
| publishDate | 2023-07-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Communications Biology |
| spelling | doaj.art-61b92f68a9e446d29fa355ee059735e32023-07-09T11:21:40ZengNature PortfolioCommunications Biology2399-36422023-07-016111410.1038/s42003-023-05002-xGenome analysis of Parmales, the sister group of diatoms, reveals the evolutionary specialization of diatoms from phago-mixotrophs to photoautotrophsHiroki Ban0Shinya Sato1Shinya Yoshikawa2Kazumasa Yamada3Yoji Nakamura4Mutsuo Ichinomiya5Naoki Sato6Romain Blanc-Mathieu7Hisashi Endo8Akira Kuwata9Hiroyuki Ogata10Bioinformatics Center, Institute for Chemical Research, Kyoto University, Gokasho, UjiDepartment of Marine Science and Technology, Fukui Prefectural UniversityDepartment of Marine Science and Technology, Fukui Prefectural UniversityDepartment of Marine Science and Technology, Fukui Prefectural UniversityBioinformatics and Biosciences Division, Fisheries Stock Assessment Center, Fisheries Resources Institute, Japan Fisheries Research and Education AgencyPrefectural University of KumamotoGraduate School of Arts and Sciences, University of Tokyo, KomabaBioinformatics Center, Institute for Chemical Research, Kyoto University, Gokasho, UjiBioinformatics Center, Institute for Chemical Research, Kyoto University, Gokasho, UjiShiogama field station, Fisheries Resources Institute, Japan Fisheries Research and Education AgencyBioinformatics Center, Institute for Chemical Research, Kyoto University, Gokasho, UjiAbstract The order Parmales (class Bolidophyceae) is a minor group of pico-sized eukaryotic marine phytoplankton that contains species with cells surrounded by silica plates. Previous studies revealed that Parmales is a member of ochrophytes and sister to diatoms (phylum Bacillariophyta), the most successful phytoplankton group in the modern ocean. Therefore, parmalean genomes can serve as a reference to elucidate both the evolutionary events that differentiated these two lineages and the genomic basis for the ecological success of diatoms vs. the more cryptic lifestyle of parmaleans. Here, we compare the genomes of eight parmaleans and five diatoms to explore their physiological and evolutionary differences. Parmaleans are predicted to be phago-mixotrophs. By contrast, diatoms have lost genes related to phagocytosis, indicating the ecological specialization from phago-mixotrophy to photoautotrophy in their early evolution. Furthermore, diatoms show significant enrichment in gene sets involved in nutrient uptake and metabolism, including iron and silica, in comparison with parmaleans. Overall, our results suggest a strong evolutionary link between the loss of phago-mixotrophy and specialization to a silicified photoautotrophic life stage early in diatom evolution after diverging from the Parmales lineage.https://doi.org/10.1038/s42003-023-05002-x |
| spellingShingle | Hiroki Ban Shinya Sato Shinya Yoshikawa Kazumasa Yamada Yoji Nakamura Mutsuo Ichinomiya Naoki Sato Romain Blanc-Mathieu Hisashi Endo Akira Kuwata Hiroyuki Ogata Genome analysis of Parmales, the sister group of diatoms, reveals the evolutionary specialization of diatoms from phago-mixotrophs to photoautotrophs Communications Biology |
| title | Genome analysis of Parmales, the sister group of diatoms, reveals the evolutionary specialization of diatoms from phago-mixotrophs to photoautotrophs |
| title_full | Genome analysis of Parmales, the sister group of diatoms, reveals the evolutionary specialization of diatoms from phago-mixotrophs to photoautotrophs |
| title_fullStr | Genome analysis of Parmales, the sister group of diatoms, reveals the evolutionary specialization of diatoms from phago-mixotrophs to photoautotrophs |
| title_full_unstemmed | Genome analysis of Parmales, the sister group of diatoms, reveals the evolutionary specialization of diatoms from phago-mixotrophs to photoautotrophs |
| title_short | Genome analysis of Parmales, the sister group of diatoms, reveals the evolutionary specialization of diatoms from phago-mixotrophs to photoautotrophs |
| title_sort | genome analysis of parmales the sister group of diatoms reveals the evolutionary specialization of diatoms from phago mixotrophs to photoautotrophs |
| url | https://doi.org/10.1038/s42003-023-05002-x |
| work_keys_str_mv | AT hirokiban genomeanalysisofparmalesthesistergroupofdiatomsrevealstheevolutionaryspecializationofdiatomsfromphagomixotrophstophotoautotrophs AT shinyasato genomeanalysisofparmalesthesistergroupofdiatomsrevealstheevolutionaryspecializationofdiatomsfromphagomixotrophstophotoautotrophs AT shinyayoshikawa genomeanalysisofparmalesthesistergroupofdiatomsrevealstheevolutionaryspecializationofdiatomsfromphagomixotrophstophotoautotrophs AT kazumasayamada genomeanalysisofparmalesthesistergroupofdiatomsrevealstheevolutionaryspecializationofdiatomsfromphagomixotrophstophotoautotrophs AT yojinakamura genomeanalysisofparmalesthesistergroupofdiatomsrevealstheevolutionaryspecializationofdiatomsfromphagomixotrophstophotoautotrophs AT mutsuoichinomiya genomeanalysisofparmalesthesistergroupofdiatomsrevealstheevolutionaryspecializationofdiatomsfromphagomixotrophstophotoautotrophs AT naokisato genomeanalysisofparmalesthesistergroupofdiatomsrevealstheevolutionaryspecializationofdiatomsfromphagomixotrophstophotoautotrophs AT romainblancmathieu genomeanalysisofparmalesthesistergroupofdiatomsrevealstheevolutionaryspecializationofdiatomsfromphagomixotrophstophotoautotrophs AT hisashiendo genomeanalysisofparmalesthesistergroupofdiatomsrevealstheevolutionaryspecializationofdiatomsfromphagomixotrophstophotoautotrophs AT akirakuwata genomeanalysisofparmalesthesistergroupofdiatomsrevealstheevolutionaryspecializationofdiatomsfromphagomixotrophstophotoautotrophs AT hiroyukiogata genomeanalysisofparmalesthesistergroupofdiatomsrevealstheevolutionaryspecializationofdiatomsfromphagomixotrophstophotoautotrophs |