Genomic Data Reveal Diverse Biological Characteristics of Scleractinian Corals and Promote Effective Coral Reef Conservation

Abstract

Reef-building corals (Scleractinia, Anthozoa, Cnidaria) are the keystone organisms of coral reefs, which constitute the most diverse marine ecosystems. Since the first decoded coral genome reported in 2011, about 40 reference genomes are registered as of 2023. Comparative genomic analyses of coral genomes have revealed genomic characters that may underlie unique biological characteristics and coral diversification. These include existence of genes for biosynthesis of mycosporine-like amino acids, loss of an enzyme necessary for cysteine biosynthesis in family Acroporidae, and lineage-specific gene expansions of DMSP lyase-like genes in the genus Acropora. While symbiosis with endosymbiotic photosynthetic dinoflagellates is a common biological feature among reef-building corals, genes associated with the intricate symbiotic relationship encompass not only those shared by many coral species, but also genes that were uniquely duplicated in each coral lineage, suggesting diversified molecular mechanisms of coral-algal symbiosis. Coral genomic data have also enabled detection of hidden, complex population structures of corals, indicating the need for species-specific, local-scale, carefully considered conservation policies for effective maintenance of corals. Consequently, accumulating coral genomic data from a wide range of taxa and from individuals of a species not only promotes deeper understanding of coral reef biodiversity, but also promotes appropriate and effective coral reef conservation. Considering the diverse biological traits of different coral species and accurately understanding population structure and genetic diversity revealed by coral genomic analyses during coral reef restoration planning could enable us to “archive” coral reef environments that are nearly identical to natural coral reefs.

Significance.

Reef-building corals (Scleractinia, Anthozoa, and Cnidaria) are the keystone organisms of coral reefs, which constitute the most diverse marine ecosystems. Since the first decoded coral genome, unexpected genomic attributes have been revealed, possibly underlying unique biological characteristics and diversification of corals. These include genes for the biosynthesis of photoprotective compounds, loss of an enzyme necessary for cysteine biosynthesis in bleaching-susceptible corals, and lineage-specific gene expansions. In addition, transcriptomic and genomic studies have illuminated diverse molecular mechanisms of coral–algal symbiosis in various coral lineages. Coral genomic data have also enabled the detection of hidden, complex population structures of corals, indicating the need for species-specific, local-scale, carefully considered conservation policies for effective maintenance of corals. Consequently, accumulating coral genome data not only promotes deeper understanding of coral reef biodiversity but also promotes appropriate and effective coral reef conservation.

Significance of Sequencing Scleractinian Coral Genomes

Coral reefs, in shallow, transparent, tropical, and subtropical waters, support the most diverse marine ecosystems on Earth. It is estimated that ∼35% of all marine species (Knowlton et al. 2010) or 830,000 multicellular species (Fisher et al. 2015) exist in or around coral reefs. Coral reef structure consists of calcium carbonate skeletons produced by anthozoan cnidarians known as scleractinian (stony) corals. Reef-building, stony corals harbor endosymbiotic photosynthetic dinoflagellates of the family Symbiodiniaceae, which supply a large part of their photosynthetic products to host corals (Yellowlees et al. 2008), in mutualistic relationships. Various anthropogenic challenges, including ocean acidification and increasing seawater temperatures are impacting coral reefs (Hoegh-Guldberg et al. 2007), and coral bleaching, a breakdown of the mutualism between corals and their symbiotic dinoflagellates, caused mainly by increased ocean temperatures, is one of the major reasons for coral reef declines (De'ath et al. 2012). Bleaching is one of the common consequences of anthropogenic global warming and has been observed with increasing frequency around the world (Hughes et al. 2017; Nakamura 2017). When coral reefs are destroyed, habitats for diverse marine species are lost, eventually resulting in extensive loss of marine biodiversity. Coral reef conservation is therefore one of the most pressing environmental issues of our time.

As keystone species of coral reefs, reef-building corals attract attention not only from biologists but also from the general public. Whole-genome sequencing was initiated relatively soon after the advent of next-generation sequencing (NGS). The first sequenced coral genome was reported in 2011 (Shinzato et al. 2011), the third whole-genome sequence of a cnidarian, following those of a sea anemone, Nematostella vectensis (Putnam et al. 2007) and a hydra, Hydra magnipapillata (Chapman et al. 2010). Subsequently, the first genome sequence from the algal family Symbiodiniaceae was reported in 2013 (Shoguchi et al. 2013). Advances in NGS technology are making whole-genome sequencing more affordable, and the number of genomes registered in the NCBI Genome database is increasing steadily, with ∼6,400 metazoan reference genomes available as of September, 2023. Within the Phylum Cnidaria, which comprises more than 11,000 extant species, 144 reference genomes are registered in NCBI, including a large number of cnidarian species (Table 1). Among the cnidarian reference genomes, 104 are from the Class Anthozoa. Of these, 93 are from the Subclass Hexacorallia, which includes scleractinians, anemones, and zoanthids. Forty are from 9 of the 37 families of stony corals (Scleractinia) (Table 1); however, most of these genomes are from the family Acroporidae (22 species) and the genus Acropora (17 species). The genus Acropora (family Acroporidae) is the iconic coral taxon in extant coral reefs globally and the most diverse scleractinian genus, with around 140 accepted species (Wallace 1999;WoRMS Editorial Board 2023). The high growth rate of Acropora corals contributes significantly to reef growth, providing habitats for diverse marine organisms, island formation, coastal protection, and fisheries (Shinn 1966; Bruckner 2002); thus Acropora corals are important not only for the maintenance of biodiversity but also for human life in regions hosting coral reefs. Nonetheless, Acropora species are highly susceptible to coral bleaching (Marshall and Baird 2000; Loya et al. 2001; Hughes et al. 2018) and are expected to decrease in the near future (Alvarez-Filip et al. 2013). For this reason, the genus Acropora has been used for a variety of coral biological studies and was chosen as the target of the first coral genome sequencing.

Table 1.

Numbers of species and reported reference genomic data in Cnidaria, Anthozoa, and Scleractinia^a

Phylum Cnidaria			Class Anthozoa			Subclass Hexacorallia			Order Scleractinia			Family Acroporidae
Class	Number of speciesb	Number of genomesc	Subclass	Number of speciesb	Number of genomesc	Order	Number of speciesb	Number of genomesc	Family	Number of speciesb	Number of genomesc	Genus	Number of speciesb	Number of genomesc
Anthozoa	7,213	104	Ceriantharia	139	0	Actiniaria	1,177	16	Acroporidae	270	22	Acropora	135	17
Cubozoa	49	6	Hexacorallia	3,489	93	Antipatharia	295	0	Agariciidae	47	1	Alveopora	15	0
Hydrozoa	3,768	11	Octocorallia	3,585	11	Corallimorpharia	49	1	Caryophylliidae	307	2	Anacropora	8	0
Myxozoa	706	8		…	…	Scleractinia	1,678	40	Dendrophylliidae	187	2	Astreopora	17	1
Scyphozoa	242	12		…	…	Zoantharia	290	36	Euphylliidae	23	1	Enigmopora	1	0
Staurozoa	49	3		…	…		…	…	Merulinidae	152	2	Isopora	6	0
	…	…		…	…		…	…	Plerogyridae	14	1	Montipora	88	4
	…	…		…	…		…	…	Pocilloporidae	55	4		…	…
	…	…		…	…		…	…	Poritidae	100	5		…	…

^aAs of September 7, 2023.

^bBased on accepted, marine, extant species in World Register of Marine Species (https://www.marinespecies.org/).

^cBased on reference genomes in NCBI Genome database.

Unexpected Unique Genomic Bases of Corals Revealed by Whole-Genome Sequencing

Comparative genomic analyses of coral genomes have revealed genomic characters that may underlie unique biological characteristics and coral diversification (Fig. 1). Reef-building, stony corals typically inhabit shallow, clear, warm waters, and are constantly exposed to intense UV radiation. Photoprotective compounds, such as mycosporine-like amino acids (MAAs) have been isolated from corals (Shick and Dunlap 2002; Rastogi et al. 2010), but these compounds are thought to have originated from symbiotic algae, as similar compounds have been identified in other algae. In the cyanobacterium, Anabaena variabilis, a short (four-step) pathway encoded by a gene cluster that consists of DHQS-like, O-MT, ATP-grasp, and NRPS-like genes is both necessary and sufficient to convert pentose-phosphate metabolites to shinorine, one of the photoprotective MAAs (Balskus and Walsh 2010). All four members of the cyanobacterial shinorine gene cluster, in which DHQS-like and O-MT genes are fused, are found in both the A. digitifera and N. vectensis genomes (Fig. 1, Shinzato et al. 2011), indicating that both have the ability to synthesize de novo UV-protective compounds, and corals and other cnidarians may not depend on symbiotic algae for MAA synthesis.

Fig. 1.

Coral genome sequencing has revealed unique biological characteristics, including a shinorine gene cluster in the Acropora digitifera genome, loss of the cystathionine ß-synthase gene from Acropora, and Acropora-specific gene duplications of DMSP lyase-like (DL-l) genes.

When the genome of A. digitifera was first decoded (Shinzato et al. 2011), it was found that cystathionine ß-synthase (CBS), an enzyme necessary for the biosynthesis of a nonessential amino acid, cysteine, was probably lost from the genome. Recent comparative genomic analyses have confirmed that the CBS gene is not found in genomes of the genera Acropora, Montipora, or Astreopora, the most basal genus in the Acroporidae (Shinzato et al. 2021a). Comparisons of the genomic region around the CBS gene in coral genomes showed that although syntenic relationships of neighboring orthologous genes are conserved, the locus is missing from Acropora genomes (Fig. 1, Shinzato et al. 2021b). Since Acropora corals are susceptible to bleaching, it is likely that Acropora depends on symbiotic algae not only for photosynthetic products but also for cysteine. This possible dependence on symbiotic algae may be a partial explanation of Acropora's high sensitivity to bleaching, but it has been recently shown that Acropora possesses an alternative pathway for cysteine biosynthesis (Salazar et al. 2022).

Dimethlysulfoniopropionate (DMSP) functions in osmoregulation and oxidative stress protection, etc. in phytoplankton and algae, and DMSP lyase mediates cleavage of DMSP into acrylate and dimethyl sulfide (DMS). DMS is a volatile substance that activates cloud formation, reducing solar radiation and ocean temperatures and contributing to atmosphere-ocean feedback. Thus, DMSP lyases in marine organisms, which release DMS into the atmosphere, may influence the local climate. Although DMSP lyases were first identified in marine bacteria, they or genes similar to them, DMSP lyase-like (DL-L), have been found in eukaryotes, not only in unicellular phytoplankton coccolithophores (Emiliania huxleyi) and Symbiodiniaceae but also in scleractinian corals. Interestingly, DL-L genes are the most diverse gene family in Acropora genomes and gene expansions have occurred specifically in the genus Acropora during past warm geological periods (Cretaceous to Early Eocene) (Fig. 1, Shinzato et al. 2021a), suggesting that Acropora-specific duplicated DL-L genes may have enabled them to survive past warming periods, adapt to diverse environments and thrive around the world. Comprehensive molecular phylogenetic analysis using available transcriptome assembly data showed that DL-L genes have been identified not only in scleractinians (Hexacorallia) but also Octocorallia (Anthozoa) and even in a jellyfish, Velella velella, known as “by-the-wind sailor” (Cnidaria: Hydrozoa) (Chiu and Shinzato 2022). Molecular phylogenetic analyses showed that cnidarian DL-L genes from Anthozoa and Hydrozoa share an ancestral DL-L gene in the last common ancestor of Cnidaria, and cnidarian DL-L genes are “ancient genes” in the animal kingdom, dating back to the pre-Cambrian (Fig. 1). Interestingly, cnidarian species in which DL-L genes have been found to date apparently exist only in coral reefs or shallow, warm environments, suggesting that these genes may be essential to survive in such environments (Chiu and Shinzato 2022).

Diverse Molecular Mechanisms of Coral–Algal Symbiosis

Most coral species (∼71%), including the genus Acropora, acquire symbionts from the ocean after the planula larval stage (Baird et al. 2009). It is therefore possible to control the timing of symbiosis during developmental stages by adding cultured Symbiodiniaceae in the laboratory (Yamashita et al. 2018). Although Acropora larvae can incorporate various types of Symbiodiniaceae, including nonsymbiotic species under laboratory conditions, Acropora recruits tend to select a limited number of Symbiodiniaceae species as symbionts in nature (Yamashita et al. 2018). Transcriptomic responses of coral larvae are clearly discrete, depending on the Symbiodiniaceae species/strain (Yoshioka et al. 2021, 2022b). For example, the number of genes with altered gene expression level in response to algal infection gradually increase with the duration of inoculation of native symbionts (AJIS2-C2 strain, isolated from an Acropora recruit and dominant symbiotic algae in Acropora early life stages), as do numbers of algae in larvae, whereas increased algal numbers are not observed in larvae inoculated with nonsymbiotic algae. The smaller number of genes activated by non-native algal infections indicates that coral larvae quickly coordinate gene expression when they recognize appropriate algal partners. The gene repertoire specifically involved in symbiosis with native symbionts suggests that when planula larvae harbor native symbionts, they slow metabolic activities and prepare to acquire photosynthetic products from algal symbionts via transporter genes. Since symbiosis-related genes are continuously expressed or suppressed when corals acquire algal symbionts, algal inoculation experiments using primary polyps, the next developmental stage of planula larvae, were performed to correctly distinguish between genes associated with symbiosis and those involved in development (Yoshioka et al. 2023). Consequently, 15 genes that are differentially expressed in response to native symbiont infection have been identified as symbiosis-related genes in Acropora early life stages. Regardless of developmental stage, their expression levels are positively correlated with numbers of algal symbionts in coral cells. Deduced functions of symbiosis-related genes include transporters for metabolic interactions, protection against oxidative stress, immune system, and the Notch-related signaling pathway (Fig. 2, Yoshioka et al. 2023). Interestingly, although some symbiosis-related genes have only a single copy in cnidarians (Fig. 2c), some genes, e.g. sugar transporters, prosaposin-like (a glycoprotein possibly involved in antioxidant responses), and Notch ligand-like, are tandemly arrayed in Acropora genomes and originated by duplication in the common ancestor of Acropora (Fig. 2d), suggesting that gene duplication may have been a driving force for establishment of mutualism with symbiotic algae in each coral lineage.

Fig. 2.

The diverse evolutionary background of possible symbiosis-related coral genes, reflects various mechanisms of molecular symbiosis among coral lineages. a) Possible symbiosis-related genes in early life stages of Acropora tenuis (Yoshioka et al. 2023). b) Hypothetical functions of symbiosis-related genes in early life stages of Acropora tenuis during symbiosis with the native symbiont, Symbiodinium microadriaticum. c) A single-copy, symbiosis-related gene, RNA binding motif protein. d) An Acropora-specific, duplicated, symbiosis-related gene, Solute carrier family 2, facilitated glucose transporter member 8 (SLC2A8-2). Detailed molecular phylogenetic trees are available in Yoshioka et al. (2023).

The genus Montipora also belongs to the family Acroporidae. In contrast to many other corals, Montipora acquires symbionts vertically from parents via eggs (Richmond and Hunter 1990). Interestingly, the genus Astreopora, phylogenetically the basal clade of the Acroporidae, acquires algal symbionts horizontally, like Acropora, suggesting that the vertical transmission mode of symbionts may have originated after the divergence of Acropora and Montipora. Following this hypothesis, an extensive comparative genomic analysis among Acroporidae (Acropora, Montipora, and Astreopora) was performed to explore genomic novelties that might explain biological traits unique to Montipora (Yoshioka et al. 2022a). The Montipora genome contains more gene families not shared with other acroporid lineages than Acropora or Astreopora. In addition, comparative transcriptomic analysis of the early life stages of Montipora and Acropora showed that unique genes in Montipora will undoubtedly have no expression in Acropora. Furthermore, 40 gene families under positive selection in Montipora genomes have been identified, 30 of which are specific to Montipora. Among those 30 gene families, 27 are expressed in early life stages, suggesting that these gene family lineages may be essential for symbiosis with maternally inherited symbiotic algae in Montipora.

Taken together, while symbiosis is a common biological feature among reef-building corals, genes associated with the intricate symbiotic relationship encompass not only those shared by many coral species but also genes that were uniquely duplicated in Acropora or acquired by Montipora. In other words, it can be inferred that genes involved in symbiosis in each coral lineage have been fine-tuned throughout evolutionary history.

Coral Genomes Reveal Complex Unexplored Population Structure and Have Implications for Coral Restoration Efforts

Coral genome information has been applied to ecological research and coral reef conservation efforts. For proper maintenance and conservation of corals, understanding genetic diversity, connectivity among different locations, and population structure are important, and genetic markers, such as microsatellites, are widely used for such studies. DNA sequences that are highly conserved among coral species have been identified using whole-genomic data of corals, and universal microsatellite markers that may be applicable to all Acropora species have been developed (Shinzato et al. 2014). These markers have been used to study the population structure of A. tenuis in the Ryukyu Islands, Japan (Zayasu et al. 2016) and to investigate genetic diversity of cultured corals to ensure the same or higher level of genetic diversity as in the wild population (Zayasu et al. 2018; Zayasu and Suzuki 2019).

Whole-genomic data enable the acquisition of millions of single nucleotide polymorphisms (SNPs) from individual corals, revealing the finest details of coral population structure. A population genomic study of A. digitifera using whole-genomic SNP data suggested limited larval dispersal in the southern Ryukyu Islands, despite its being a broadcast spawner (Shinzato et al. 2015). A recent study using whole-genomic SNP data from more than 300 individual A. digitifera throughout the Ryukyu Islands shed light on the unexpectedly complex population structure in the Ryukyu Islands. Genetic similarities between the southernmost and northernmost locations in the Ryukyu Islands, separated by >1,000 km, and several subpopulations in intermediate locations revealed limited genetic admixture (Tsuchiya et al. 2022). Whole-genomic SNP analysis also revealed different population structures of two Acropora species at a small island in Okinawa Prefecture, Japan, despite the same reproductive mode. There was no detectable structure in A. digitifera, although two distinct genetic clades with little or no admixture were detected in A. tenuis, possibly representing the existence of two reproductively isolated cryptic species (Zayasu et al. 2021). Recent studies also show that genomic analyses could reveal the genetic basis of coral thermal tolerance and could facilitate accurate predictions of coral adaptation to future ocean warming (e.g. Dixon et al. 2015; Bay et al. 2017; Fuller et al. 2020).

Concluding Remarks

Coral genomic data have highlighted diverse biological characters among stony corals, e.g. loss of CBS genes in the family Acroporidae, suggesting different degrees of dependence on symbiotic algae, depending on the coral lineage, MAA gene clusters, specific gene expansions of DL-L genes in Acropora (Fig. 1), and lineage-specific symbiosis-related genes, suggesting diversified molecular mechanisms of coral–algal symbiosis (Fig. 2). Various reef-building corals with different biological characteristics interact to support the rich biodiversity of coral reefs, and it is important to comprehend these diverse characteristics for studying coral biology and coral conservation. High-resolution population genomic studies using genome-wide SNP analyses have also revealed hidden, complex population structures of corals, indicating that when establishing effective coral conservation plans, careful, local-scale, and species-specific conservation policies will be needed. Moreover, similar, unexpected population complexities may be expected for marine species other than scleractinian corals with similar reproductive modes, especially broadcast spawners. Coral genome information, boosted by NGS advances, is accumulating steadily, and 12 reference genomes of the family Symbiodiniaceae have been reported in NCBI as of September 2023. Accumulating coral genomic data from a wide range of taxa and from individuals of a species not only promotes deeper understanding of coral reef biodiversity but also promotes appropriate and effective coral reef conservation. Considering the diverse biological traits of different coral species and accurately understanding population structure and genetic diversity revealed by coral genomic analyses during coral reef restoration planning could enable us to “archive” coral reef environments that are nearly identical to natural coral reefs. Hopefully, coral genome analysis will contribute to the preservation of the richness of coral reefs for future generations.

Funding

Preparation of the manuscript was partially supported by Japan Society for the Promotion of Science (JSPS) KAKENHI grants (20H03235 and 20K21860 for C.S.) and Grant-in-Aid for JSPS Fellows to Y.Y. (20J21301 and 23KJ2129).

Data Availability

No new data were generated or analyzed in support of this research.