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Two divergent Symbiodinium genomes reveal conservation of a gene cluster for sunscreen biosynthesis and recently lost genes

BACKGROUND: The marine dinoflagellate, Symbiodinium, is a well-known photosynthetic partner for coral and other diverse, non-photosynthetic hosts in subtropical and tropical shallows, where it comprises an essential component of marine ecosystems. Using molecular phylogenetics, the genus Symbiodiniu...

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Autores principales: Shoguchi, Eiichi, Beedessee, Girish, Tada, Ipputa, Hisata, Kanako, Kawashima, Takeshi, Takeuchi, Takeshi, Arakaki, Nana, Fujie, Manabu, Koyanagi, Ryo, Roy, Michael C., Kawachi, Masanobu, Hidaka, Michio, Satoh, Noriyuki, Shinzato, Chuya
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6001144/
https://www.ncbi.nlm.nih.gov/pubmed/29898658
http://dx.doi.org/10.1186/s12864-018-4857-9
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author Shoguchi, Eiichi
Beedessee, Girish
Tada, Ipputa
Hisata, Kanako
Kawashima, Takeshi
Takeuchi, Takeshi
Arakaki, Nana
Fujie, Manabu
Koyanagi, Ryo
Roy, Michael C.
Kawachi, Masanobu
Hidaka, Michio
Satoh, Noriyuki
Shinzato, Chuya
author_facet Shoguchi, Eiichi
Beedessee, Girish
Tada, Ipputa
Hisata, Kanako
Kawashima, Takeshi
Takeuchi, Takeshi
Arakaki, Nana
Fujie, Manabu
Koyanagi, Ryo
Roy, Michael C.
Kawachi, Masanobu
Hidaka, Michio
Satoh, Noriyuki
Shinzato, Chuya
author_sort Shoguchi, Eiichi
collection PubMed
description BACKGROUND: The marine dinoflagellate, Symbiodinium, is a well-known photosynthetic partner for coral and other diverse, non-photosynthetic hosts in subtropical and tropical shallows, where it comprises an essential component of marine ecosystems. Using molecular phylogenetics, the genus Symbiodinium has been classified into nine major clades, A-I, and one of the reported differences among phenotypes is their capacity to synthesize mycosporine-like amino acids (MAAs), which absorb UV radiation. However, the genetic basis for this difference in synthetic capacity is unknown. To understand genetics underlying Symbiodinium diversity, we report two draft genomes, one from clade A, presumed to have been the earliest branching clade, and the other from clade C, in the terminal branch. RESULTS: The nuclear genome of Symbiodinium clade A (SymA) has more gene families than that of clade C, with larger numbers of organelle-related genes, including mitochondrial transcription terminal factor (mTERF) and Rubisco. While clade C (SymC) has fewer gene families, it displays specific expansions of repeat domain-containing genes, such as leucine-rich repeats (LRRs) and retrovirus-related dUTPases. Interestingly, the SymA genome encodes a gene cluster for MAA biosynthesis, potentially transferred from an endosymbiotic red alga (probably of bacterial origin), while SymC has completely lost these genes. CONCLUSIONS: Our analysis demonstrates that SymC appears to have evolved by losing gene families, such as the MAA biosynthesis gene cluster. In contrast to the conservation of genes related to photosynthetic ability, the terminal clade has suffered more gene family losses than other clades, suggesting a possible adaptation to symbiosis. Overall, this study implies that Symbiodinium ecology drives acquisition and loss of gene families. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-4857-9) contains supplementary material, which is available to authorized users.
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spelling pubmed-60011442018-06-26 Two divergent Symbiodinium genomes reveal conservation of a gene cluster for sunscreen biosynthesis and recently lost genes Shoguchi, Eiichi Beedessee, Girish Tada, Ipputa Hisata, Kanako Kawashima, Takeshi Takeuchi, Takeshi Arakaki, Nana Fujie, Manabu Koyanagi, Ryo Roy, Michael C. Kawachi, Masanobu Hidaka, Michio Satoh, Noriyuki Shinzato, Chuya BMC Genomics Research Article BACKGROUND: The marine dinoflagellate, Symbiodinium, is a well-known photosynthetic partner for coral and other diverse, non-photosynthetic hosts in subtropical and tropical shallows, where it comprises an essential component of marine ecosystems. Using molecular phylogenetics, the genus Symbiodinium has been classified into nine major clades, A-I, and one of the reported differences among phenotypes is their capacity to synthesize mycosporine-like amino acids (MAAs), which absorb UV radiation. However, the genetic basis for this difference in synthetic capacity is unknown. To understand genetics underlying Symbiodinium diversity, we report two draft genomes, one from clade A, presumed to have been the earliest branching clade, and the other from clade C, in the terminal branch. RESULTS: The nuclear genome of Symbiodinium clade A (SymA) has more gene families than that of clade C, with larger numbers of organelle-related genes, including mitochondrial transcription terminal factor (mTERF) and Rubisco. While clade C (SymC) has fewer gene families, it displays specific expansions of repeat domain-containing genes, such as leucine-rich repeats (LRRs) and retrovirus-related dUTPases. Interestingly, the SymA genome encodes a gene cluster for MAA biosynthesis, potentially transferred from an endosymbiotic red alga (probably of bacterial origin), while SymC has completely lost these genes. CONCLUSIONS: Our analysis demonstrates that SymC appears to have evolved by losing gene families, such as the MAA biosynthesis gene cluster. In contrast to the conservation of genes related to photosynthetic ability, the terminal clade has suffered more gene family losses than other clades, suggesting a possible adaptation to symbiosis. Overall, this study implies that Symbiodinium ecology drives acquisition and loss of gene families. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-4857-9) contains supplementary material, which is available to authorized users. BioMed Central 2018-06-14 /pmc/articles/PMC6001144/ /pubmed/29898658 http://dx.doi.org/10.1186/s12864-018-4857-9 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Shoguchi, Eiichi
Beedessee, Girish
Tada, Ipputa
Hisata, Kanako
Kawashima, Takeshi
Takeuchi, Takeshi
Arakaki, Nana
Fujie, Manabu
Koyanagi, Ryo
Roy, Michael C.
Kawachi, Masanobu
Hidaka, Michio
Satoh, Noriyuki
Shinzato, Chuya
Two divergent Symbiodinium genomes reveal conservation of a gene cluster for sunscreen biosynthesis and recently lost genes
title Two divergent Symbiodinium genomes reveal conservation of a gene cluster for sunscreen biosynthesis and recently lost genes
title_full Two divergent Symbiodinium genomes reveal conservation of a gene cluster for sunscreen biosynthesis and recently lost genes
title_fullStr Two divergent Symbiodinium genomes reveal conservation of a gene cluster for sunscreen biosynthesis and recently lost genes
title_full_unstemmed Two divergent Symbiodinium genomes reveal conservation of a gene cluster for sunscreen biosynthesis and recently lost genes
title_short Two divergent Symbiodinium genomes reveal conservation of a gene cluster for sunscreen biosynthesis and recently lost genes
title_sort two divergent symbiodinium genomes reveal conservation of a gene cluster for sunscreen biosynthesis and recently lost genes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6001144/
https://www.ncbi.nlm.nih.gov/pubmed/29898658
http://dx.doi.org/10.1186/s12864-018-4857-9
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