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Whole-Genome Sequencing Highlights Conservative Genomic Strategies of a Stress-Tolerant, Long-Lived Scleractinian Coral, Porites australiensis Vaughan, 1918.

ABSTRACT: Massive corals of the genus Porites, common, keystone reef builders in the Indo-Pacific Ocean, are distinguished by their relative stress tolerance and longevity. In order to identify genetic bases of these attributes, we sequenced the complete genome of a massive coral, Porites australiensis. We developed a genome assembly and gene models of comparable quality to those of other coral genomes. Proteome analysis identified 60 Porites skeletal matrix protein genes, all of which show significant similarities to genes from other corals and even to those from a sea anemone, which has no skeleton. Nonetheless, 30% of its skeletal matrix proteins were unique to Porites and were not present in the skeletons of other corals. Comparative genomic analyses showed that genes widely conserved among other organisms are selectively expanded in Porites. Specifically, comparisons of transcriptomic responses of P. australiensis and Acropora digitifera, a stress-sensitive coral, reveal significant differences in regard to genes that respond to increased water temperature, and some of the genes expanded exclusively in Porites may account for the different thermal tolerances of these corals. Taken together, widely shared genes may have given rise to unique biological characteristics of Porites, massive skeletons and stress tolerance.

SUBMITTER: Shinzato C

PROVIDER: S-EPMC8691061 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Global warming is a key issue that causes coral bleaching mainly because of the thermosensitivity of zooxanthellae. Compared with the well-studied zooxanthellae Symbiodiniaceae in coral holobionts, we rarely know about other coral symbiotic algae, let alone their thermal tolerance. In this study, a zoochlorellae, Symbiochlorum hainanensis, isolated from the coral Porites lutea, was proven to have a threshold temperature of 38°C. Meanwhile, unique high-temperature tolerance mechanisms were suggested by integrated transcriptomics and real-time quantitative PCR, physiological and biochemical analyses, and electron microscopy observation. Under heat stress, S. hainanensis shared some similar response strategies with zooxanthellae Effrenium sp., such as increased ascorbate peroxidase, glutathione peroxidase, superoxide dismutase activities and chlorophyll a, thiamine, and thiamine phosphate contents. In particular, more chloroplast internal layered structure, increased CAT activity, enhanced selenate reduction, and thylakoid assembly pathways were highlighted for S. hainanensis's high-temperature tolerance. Notably, it is the first time to reveal a whole selenate reduction pathway from SeO42- to Se2- and its contribution to the high-temperature tolerance of S. hainanensis. These unique mechanisms, including antioxidation and maintaining photosynthesis homeostasis, efficiently ensure the high-temperature tolerance of S. hainanensis than Effrenium sp. Compared with the thermosensitivity of coral symbiotic zooxanthellae Symbiodiniaceae, this study provides novel insights into the high-temperature tolerance mechanisms of coral symbiotic zoochlorellae S. hainanensis, which will contribute to corals' survival in the warming oceans caused by global climate change.ImportanceThe increasing ocean temperature above 31°C-32°C might trigger a breakdown of the coral-Symbiodiniaceae symbioses or coral bleaching because of the thermosensitivity of Symbiodiniaceae; therefore, the exploration of alternative coral symbiotic algae with high-temperature tolerance is important for the corals' protection under warming oceans. This study proves that zoochlorellae Symbiochlorum hainanensis can tolerate 38°C, which is the highest temperature tolerance known for coral symbiotic algae to date, with unique high-temperature tolerance mechanisms. Particularly, for the first time, an internal selenium antioxidant mechanism of coral symbiotic S. hainanensis to high temperature was suggested.

Project description:Massive scleractinian corals of the genus Porites are important reef builders in the Indo-Pacific, and they are more resistant to thermal stress than other stony corals, such as the genus Acropora. Because coral health and survival largely depend on the interaction between a coral host and its symbionts, it is important to understand the molecular interactions of an entire "coral holobiont". We simultaneously sequenced transcriptomes of Porites australiensis and its symbionts using the Illumina Hiseq2000 platform. We obtained 14.3 Gbp of sequencing data and assembled it into 74,997 contigs (average: 1,263 bp, N50 size: 2,037 bp). We successfully distinguished contigs originating from the host (Porites) and the symbiont (Symbiodinium) by aligning nucleotide sequences with the decoded Acropora digitifera and Symbiodinium minutum genomes. In contrast to previous coral transcriptome studies, at least 35% of the sequences were found to have originated from the symbionts, indicating that it is possible to analyze both host and symbiont transcriptomes simultaneously. Conserved protein domain and KEGG analyses showed that the dataset contains broad gene repertoires of both Porites and Symbiodinium. Effective utilization of sequence reads revealed that the polymorphism rate in P. australiensis is 1.0% and identified the major symbiotic Symbiodinium as Type C15. Analyses of amino acid biosynthetic pathways suggested that this Porites holobiont is probably able to synthesize most of the common amino acids and that Symbiodinium is potentially able to provide essential amino acids to its host. We believe this to be the first molecular evidence of complementarity in amino acid metabolism between coral hosts and their symbionts. We successfully assembled genes originating from both the host coral and the symbiotic Symbiodinium to create a snapshot of the coral holobiont transcriptome. This dataset will facilitate a deeper understanding of molecular mechanisms of coral symbioses and stress responses.

Dataset Information

Whole-Genome Sequencing Highlights Conservative Genomic Strategies of a Stress-Tolerant, Long-Lived Scleractinian Coral, Porites australiensis Vaughan, 1918.

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