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

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Abstract

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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Most cited references 51

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Using the Acropora digitifera genome to understand coral responses to environmental change.

Chuya Shinzato, Eiichi Shoguchi, Takeshi Kawashima … (2011)

Despite the enormous ecological and economic importance of coral reefs, the keystone organisms in their establishment, the scleractinian corals, increasingly face a range of anthropogenic challenges including ocean acidification and seawater temperature rise. To understand better the molecular mechanisms underlying coral biology, here we decoded the approximately 420-megabase genome of Acropora digitifera using next-generation sequencing technology. This genome contains approximately 23,700 gene models. Molecular phylogenetics indicate that the coral and the sea anemone Nematostella vectensis diverged approximately 500 million years ago, considerably earlier than the time over which modern corals are represented in the fossil record (∼240 million years ago). Despite the long evolutionary history of the endosymbiosis, no evidence was found for horizontal transfer of genes from symbiont to host. However, unlike several other corals, Acropora seems to lack an enzyme essential for cysteine biosynthesis, implying dependency of this coral on its symbionts for this amino acid. Corals inhabit environments where they are frequently exposed to high levels of solar radiation, and analysis of the Acropora genome data indicates that the coral host can independently carry out de novo synthesis of mycosporine-like amino acids, which are potent ultraviolet-protective compounds. In addition, the coral innate immunity repertoire is notably more complex than that of the sea anemone, indicating that some of these genes may have roles in symbiosis or coloniality. A number of genes with putative roles in calcification were identified, and several of these are restricted to corals. The coral genome provides a platform for understanding the molecular basis of symbiosis and responses to environmental changes.

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Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing.

Patrick Shih, Dongying Wu, Amel Latifi … (2013)

The cyanobacterial phylum encompasses oxygenic photosynthetic prokaryotes of a great breadth of morphologies and ecologies; they play key roles in global carbon and nitrogen cycles. The chloroplasts of all photosynthetic eukaryotes can trace their ancestry to cyanobacteria. Cyanobacteria also attract considerable interest as platforms for "green" biotechnology and biofuels. To explore the molecular basis of their different phenotypes and biochemical capabilities, we sequenced the genomes of 54 phylogenetically and phenotypically diverse cyanobacterial strains. Comparison of cyanobacterial genomes reveals the molecular basis for many aspects of cyanobacterial ecophysiological diversity, as well as the convergence of complex morphologies without the acquisition of novel proteins. This phylum-wide study highlights the benefits of diversity-driven genome sequencing, identifying more than 21,000 cyanobacterial proteins with no detectable similarity to known proteins, and foregrounds the diversity of light-harvesting proteins and gene clusters for secondary metabolite biosynthesis. Additionally, our results provide insight into the distribution of genes of cyanobacterial origin in eukaryotic nuclear genomes. Moreover, this study doubles both the amount and the phylogenetic diversity of cyanobacterial genome sequence data. Given the exponentially growing number of sequenced genomes, this diversity-driven study demonstrates the perspective gained by comparing disparate yet related genomes in a phylum-wide context and the insights that are gained from it.

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The genome of Aiptasia, a sea anemone model for coral symbiosis.

Sebastian Baumgarten, Oleg Simakov, Lisl Esherick … (2015)

The most diverse marine ecosystems, coral reefs, depend upon a functional symbiosis between a cnidarian animal host (the coral) and intracellular photosynthetic dinoflagellate algae. The molecular and cellular mechanisms underlying this endosymbiosis are not well understood, in part because of the difficulties of experimental work with corals. The small sea anemone Aiptasia provides a tractable laboratory model for investigating these mechanisms. Here we report on the assembly and analysis of the Aiptasia genome, which will provide a foundation for future studies and has revealed several features that may be key to understanding the evolution and function of the endosymbiosis. These features include genomic rearrangements and taxonomically restricted genes that may be functionally related to the symbiosis, aspects of host dependence on alga-derived nutrients, a novel and expanded cnidarian-specific family of putative pattern-recognition receptors that might be involved in the animal-algal interactions, and extensive lineage-specific horizontal gene transfer. Extensive integration of genes of prokaryotic origin, including genes for antimicrobial peptides, presumably reflects an intimate association of the animal-algal pair also with its prokaryotic microbiome.

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Author and article information

Contributors

Eiichi Shoguchi: 81-98-966-8653 , eiichi@oist.jp

Girish Beedessee: girish.beedessee@oist.jp

Ipputa Tada: br091422@gmail.com

Kanako Hisata: kanako@oist.jp

Takeshi Kawashima: kawashima38@gmail.com

Takeshi Takeuchi: t.takeuchi@oist.jp

Nana Arakaki: nana.arakaki@oist.jp

Manabu Fujie: fujie@oist.jp

Ryo Koyanagi: koyanagi@oist.jp

Michael C. Roy: mcroy@oist.jp

Masanobu Kawachi: kawachi.masanobu@nies.go.jp

Michio Hidaka: hidaka@sci.u-ryukyu.ac.jp

Noriyuki Satoh: norisky@oist.jp

Chuya Shinzato: 81-98-966-8653 , c.shinzato@aori.u-tokyo.ac.jp

Journal

Journal ID (nlm-ta): BMC Genomics

Journal ID (iso-abbrev): BMC Genomics

Title: BMC Genomics

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2164

Publication date (Electronic): 14 June 2018

Publication date PMC-release: 14 June 2018

Publication date Collection: 2018

Volume: 19

Electronic Location Identifier: 458

Affiliations

[1 ]ISNI 0000 0000 9805 2626, GRID grid.250464.1, Marine Genomics Unit, , Okinawa Institute of Science and Technology Graduate University, ; Onna, Okinawa, 904-0495 Japan

[2 ]ISNI 0000 0004 1763 208X, GRID grid.275033.0, Present address: Department of Genetics, School of Life Science, , The Graduate University for Advanced Studies, ; 1111, Yata, Mishima-shi, Shizuoka, 411-8540 Japan

[3 ]ISNI 0000 0004 0466 9350, GRID grid.288127.6, Present address: Center for Information Biology, , National Institute of Genetics, ; Mishima, 411-8540 Japan

[4 ]ISNI 0000 0000 9805 2626, GRID grid.250464.1, DNA Sequencing Section, , Okinawa Institute of Science and Technology Graduate University, ; Onna, Okinawa, 904-0495 Japan

[5 ]ISNI 0000 0000 9805 2626, GRID grid.250464.1, Instrumental Analysis Section, , Okinawa Institute of Science and Technology Graduate University, ; Onna, Okinawa, 904-0495 Japan

[6 ]ISNI 0000 0001 0746 5933, GRID grid.140139.e, Center for Environmental Biology and Ecosystem Studies, , National Institute for Environmental Studies, ; Tsukuba, 305-8506 Japan

[7 ]ISNI 0000 0001 0685 5104, GRID grid.267625.2, Department of Chemistry, Biology and Marine Science, , University of the Ryukyus, ; Nishihara, Okinawa, 903-0213 Japan

[8 ]ISNI 0000 0001 2151 536X, GRID grid.26999.3d, Atmosphere and Ocean Research Institute, , The University of Tokyo, ; Kashiwanoha, Kashiwa, 277-8564 Japan

Article

Publisher ID: 4857

DOI: 10.1186/s12864-018-4857-9

PMC ID: 6001144

PubMed ID: 29898658

SO-VID: 87137962-6660-4620-a52f-8e14f2aa9d61

License:

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.

History

Date received : 1 March 2018

Date accepted : 6 June 2018

Custom metadata

ScienceOpen disciplines: Genetics

Keywords: dinoflagellates,evolutionary genomics,symbiodinium,mycosporine-like amino acids,symbiosis

Data availability:

ScienceOpen disciplines: Genetics

Keywords: dinoflagellates, evolutionary genomics, symbiodinium, mycosporine-like amino acids, symbiosis

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

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Abstract

Background

Results

Conclusions

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Genes & Diseases

Most cited references 51

Using the Acropora digitifera genome to understand coral responses to environmental change.

Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing.

The genome of Aiptasia, a sea anemone model for coral symbiosis.

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