Corallimorpharian transcriptomes and their use to understand phylogeny and symbiosis in the Hexacorallia

Lin, Mei-Fang (2016) Corallimorpharian transcriptomes and their use to understand phylogeny and symbiosis in the Hexacorallia. PhD thesis, James Cook University.

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Abstract

Corallimorpharia, also known as coral-like anemones, belong to the sub-order Hexacorallia, the class Anthozoa, the phylum Cnidaria. Cnidaria is a group of the simplest animals at the tissue level of organization, which reflect ancestral characteristics and hence are important for understanding the evolution of metazoan genomes and developmental mechanisms. Morphologically, corallimorpharians resemble actinarians in the absence of a calcareous skeleton, but have internal anatomy more similar to scleractinians (corals) than to actinarians (sea anemones). Corallimorpharia comprises about 46 nominal species and generally these are minor components of the benthos in a wide range of habitats, which has led to corallimorpharian taxonomy and phylogeny being largely ignored in favor of their more obvious relatives.

Corallimorpharians are typical hexacorallians in several respects, e.g. 48.2% of corallimorpharians harbor endosymbiotic dinoflagellate algae (zooxanthellae) belonging to the genus Symbiodinium, there are both shallow water and deep-sea species (Append A), and they have similar overall symmetry of body structure. Phylogenetic relationships between corallimorpharians and scleractinians remain particularly controversial and, on the basis of mitochondrial genome data, two main hypotheses have been proposed for their evolution. The "naked coral" hypothesis states that scleractinians were skeleton-less in the early Triassic, a time when carbonate deposition was suppressed globally, and corallimorpharians arose by skeleton loss from a scleractinian ancestor at a later time (during the mid-Cretaceous) when the oceans had higher CO₂ levels. By contrast, the "scleractinian monophyly" hypothesis has corals as a monophylic lineage, with the Corallimorpharia as a close sister clade. According to Kitahara et al. (2014), the fundamental disagreement between the phylogenies based on nucleotide and amino acid sequences for mt proteins stems from the fact that none of the available models for sequence evolution adequately account for the observed data. Comparison of corallimorpharian and scleractinian mt genome architectures has shown that gene order in one species of corallimorpharian, Corallimorphus profundus (Moseley, 1877), is very similar to the canonical organization in scleractinians, indicating that this organism most closely reflects the coral <-> corallimorpharian transition (Lin et al., 2014).

In this study, three corallimorpharian transcriptomes were generated, and phylogenomic analyses of these used to provide insights into evolutionary relationships between scleractinians and corallimorpharians. The results strongly support scleractinian monophyly. Moreover, surveying the corallimorpharian transcriptomes led to the identification of homolologs of some skeletal organic matrix proteins (SOMPs) that were previously considered to be restricted to scleractinians; this is particularly significant given that surprisingly few of the proteins identified in the skeletal proteome are scleractinian-specific. Comparison of the carbonic anhydrase (CA) inventories of corallimorpharians with those of corals indicates that scleractinians have specifically expanded the secreted and membrane-associated type CAs, whereas similar complexity is observed in the two groups with respect to other CA types. Additionally the similar numbers and distribution of the various CA types between the non-symbiotic corallimorpharians Corynactis and Ricordea, which normally host Symbiodinium, suggest that, whereas an expansion of the CA repertoire has been necessary to enable calcification, it may not be a requirement to enable symbiosis. These data also indicated that the evolution of calcification in scleractinians required relatively few completely new genes.

Prior to the present work, little was known about corallimorpharian-algal symbioses. This study investigated gene expression profiles of a tropical corallimorpharian during the re-establishment of symbiosis, providing the first large-scale dataset of this kind. The comparison of corallimorpharian transcriptomes under the symbiotic and aposymbiotic states indicated the similar responses of those shown in the scleractinians and anemones. The comprehensive comparison of genomic data from symbiotic, aposymbiotic and nonsymbiotic cnidarians supports the previous idea that host genes involved in symbiosis recognition and innate immune response for Symbiodinium tolerance play important roles in the establishment of symbiosis. Finally, the transcriptomic data indicate that glycogen biosynthesis occurs during the re-establishment of symbiosis in corallimorpharians, and that glycogen synthesis is likely to be more active during re-infection with a homologous rather than heterologous Symbiodinium strains. An additional interesting finding was the identification of a suite of genes unique to symbiotic corallimorpharians that were upregulated during the establishment of symbiosis. Although the functions of these genes remain to be explored, it is tempting to speculate to interpret this as evidence for the independent evolution of symbiosis in corallimorpharians.

Item ID: 48579
Item Type: Thesis (PhD)
Keywords: Anthozoa, carbonic anhydrase, coral calcification, Corallimorpharia, corallimorpharian, evolution, molecular evolution, phylogenomics, reinfection, Scleractinia, skeletal organic matrix proteins, symbiosis, zoantharia
Additional Information:

Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter III: Lin, Mei-Fang, Moya, Aurelie, Ying, Hua, Chen, Chaolun Allen, Cooke, Ira, Ball, Eldon E., Forȇt, Sylvain, and Miller, David J. (2017) Analyses of corallimorpharian transcriptomes provide new perspectives on the evolution of calcification in the Scleractinia (corals). Genome Biology and Evolution, 9 (1). pp. 150-160.

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Date Deposited: 24 Apr 2017 01:28
FoR Codes: 06 BIOLOGICAL SCIENCES > 0604 Genetics > 060408 Genomics @ 50%
06 BIOLOGICAL SCIENCES > 0601 Biochemistry and Cell Biology > 060102 Bioinformatics @ 40%
06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060309 Phylogeny and Comparative Analysis @ 10%
SEO Codes: 96 ENVIRONMENT > 9603 Climate and Climate Change > 960305 Ecosystem Adaptation to Climate Change @ 50%
97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 30%
96 ENVIRONMENT > 9606 Environmental and Natural Resource Evaluation > 960604 Environmental Management Systems @ 20%
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