Comparative mitochondrial genomics of cryptophyte algae: gene shuffling and dynamic mobile genetic elements
Abstract Background Cryptophytes are an ecologically important group of algae comprised of phototrophic, heterotrophic and osmotrophic species. This lineage is of great interest to evolutionary biologists because their plastids are of red algal secondary endosymbiotic origin. Cryptophytes have a cle...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2018-04-01
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| Series: | BMC Genomics |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s12864-018-4626-9 |
| _version_ | 1818989347788029952 |
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| author | Jong Im Kim Hwan Su Yoon Gangman Yi Woongghi Shin John M. Archibald |
| author_facet | Jong Im Kim Hwan Su Yoon Gangman Yi Woongghi Shin John M. Archibald |
| author_sort | Jong Im Kim |
| collection | DOAJ |
| description | Abstract Background Cryptophytes are an ecologically important group of algae comprised of phototrophic, heterotrophic and osmotrophic species. This lineage is of great interest to evolutionary biologists because their plastids are of red algal secondary endosymbiotic origin. Cryptophytes have a clear phylogenetic affinity to heterotrophic eukaryotes and possess four genomes: host-derived nuclear and mitochondrial genomes, and plastid and nucleomorph genomes of endosymbiotic origin. Results To gain insight into cryptophyte mitochondrial genome evolution, we sequenced the mitochondrial DNAs of five species and performed a comparative analysis of seven genomes from the following cryptophyte genera: Chroomonas, Cryptomonas, Hemiselmis, Proteomonas, Rhodomonas, Storeatula and Teleaulax. The mitochondrial genomes were similar in terms of their general architecture, gene content and presence of a large repeat region. However, gene order was poorly conserved. Characteristic features of cryptophyte mtDNAs included large syntenic clusters resembling α-proteobacterial operons that encode bacteria-like rRNAs, tRNAs, and ribosomal protein genes. The cryptophyte mitochondrial genomes retain almost all genes found in many other eukaryotes including the nad, sdh, cox, cob, and atp genes, with the exception of sdh2 and atp3. In addition, gene cluster analysis showed that cryptophytes possess a gene order closely resembling the jakobid flagellates Jakoba and Reclinomonas. Interestingly, the cox1 gene of R. salina, T. amphioxeia, and Storeatula species was found to contain group II introns encoding a reverse transcriptase protein, as did the cob gene of Storeatula species CCMP1868. Conclusions These newly sequenced genomes increase the breadth of data available from algae and will aid in the identification of general trends in mitochondrial genome evolution. While most of the genomes were highly conserved, extensive gene arrangements have shuffled gene order, perhaps due to genome rearrangements associated with hairpin-containing mobile genetic elements, tRNAs with palindromic sequences, and tandem repeat sequences. The cox1 and cob gene sequences suggest that introns have recently been acquired during cryptophyte evolution. Comparison of phylogenetic trees based on plastid and mitochondrial genome data sets underscore the different evolutionary histories of the host and endosymbiont components of present-day cryptophytes. |
| first_indexed | 2024-12-20T19:37:02Z |
| format | Article |
| id | doaj.art-3693c07478954e9296f95d8c19f0d6a4 |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-12-20T19:37:02Z |
| publishDate | 2018-04-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-3693c07478954e9296f95d8c19f0d6a42022-12-21T19:28:37ZengBMCBMC Genomics1471-21642018-04-0119111410.1186/s12864-018-4626-9Comparative mitochondrial genomics of cryptophyte algae: gene shuffling and dynamic mobile genetic elementsJong Im Kim0Hwan Su Yoon1Gangman Yi2Woongghi Shin3John M. Archibald4Department of Biology, Chungnam National UniversityDepartment of Biological Sciences, Sungkyunkwan UniversityDepartment of Multimedia Engineering, Dongguk UniversityDepartment of Biology, Chungnam National UniversityDepartment of Biochemistry and Molecular Biology, Dalhousie UniversityAbstract Background Cryptophytes are an ecologically important group of algae comprised of phototrophic, heterotrophic and osmotrophic species. This lineage is of great interest to evolutionary biologists because their plastids are of red algal secondary endosymbiotic origin. Cryptophytes have a clear phylogenetic affinity to heterotrophic eukaryotes and possess four genomes: host-derived nuclear and mitochondrial genomes, and plastid and nucleomorph genomes of endosymbiotic origin. Results To gain insight into cryptophyte mitochondrial genome evolution, we sequenced the mitochondrial DNAs of five species and performed a comparative analysis of seven genomes from the following cryptophyte genera: Chroomonas, Cryptomonas, Hemiselmis, Proteomonas, Rhodomonas, Storeatula and Teleaulax. The mitochondrial genomes were similar in terms of their general architecture, gene content and presence of a large repeat region. However, gene order was poorly conserved. Characteristic features of cryptophyte mtDNAs included large syntenic clusters resembling α-proteobacterial operons that encode bacteria-like rRNAs, tRNAs, and ribosomal protein genes. The cryptophyte mitochondrial genomes retain almost all genes found in many other eukaryotes including the nad, sdh, cox, cob, and atp genes, with the exception of sdh2 and atp3. In addition, gene cluster analysis showed that cryptophytes possess a gene order closely resembling the jakobid flagellates Jakoba and Reclinomonas. Interestingly, the cox1 gene of R. salina, T. amphioxeia, and Storeatula species was found to contain group II introns encoding a reverse transcriptase protein, as did the cob gene of Storeatula species CCMP1868. Conclusions These newly sequenced genomes increase the breadth of data available from algae and will aid in the identification of general trends in mitochondrial genome evolution. While most of the genomes were highly conserved, extensive gene arrangements have shuffled gene order, perhaps due to genome rearrangements associated with hairpin-containing mobile genetic elements, tRNAs with palindromic sequences, and tandem repeat sequences. The cox1 and cob gene sequences suggest that introns have recently been acquired during cryptophyte evolution. Comparison of phylogenetic trees based on plastid and mitochondrial genome data sets underscore the different evolutionary histories of the host and endosymbiont components of present-day cryptophytes.http://link.springer.com/article/10.1186/s12864-018-4626-9CryptophytesGenome re-arrangementMitochondrial genomeMobile genetic elements |
| spellingShingle | Jong Im Kim Hwan Su Yoon Gangman Yi Woongghi Shin John M. Archibald Comparative mitochondrial genomics of cryptophyte algae: gene shuffling and dynamic mobile genetic elements BMC Genomics Cryptophytes Genome re-arrangement Mitochondrial genome Mobile genetic elements |
| title | Comparative mitochondrial genomics of cryptophyte algae: gene shuffling and dynamic mobile genetic elements |
| title_full | Comparative mitochondrial genomics of cryptophyte algae: gene shuffling and dynamic mobile genetic elements |
| title_fullStr | Comparative mitochondrial genomics of cryptophyte algae: gene shuffling and dynamic mobile genetic elements |
| title_full_unstemmed | Comparative mitochondrial genomics of cryptophyte algae: gene shuffling and dynamic mobile genetic elements |
| title_short | Comparative mitochondrial genomics of cryptophyte algae: gene shuffling and dynamic mobile genetic elements |
| title_sort | comparative mitochondrial genomics of cryptophyte algae gene shuffling and dynamic mobile genetic elements |
| topic | Cryptophytes Genome re-arrangement Mitochondrial genome Mobile genetic elements |
| url | http://link.springer.com/article/10.1186/s12864-018-4626-9 |
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