Comparative analysis of the genomes of Stylophora pistillata and Acropora digitifera provides evidence for extensive differences between species of corals

Abstract

Stony corals form the foundation of coral reef ecosystems. Their phylogeny is characterized by a deep evolutionary divergence that separates corals into a robust and complex clade dating back to at least 245 mya. However, the genomic consequences and clade-specific evolution remain unexplored. In this study we have produced the genome of a robust coral, Stylophora pistillata, and compared it to the available genome of a complex coral, Acropora digitifera. We conducted a fine-scale gene-based analysis focusing on ortholog groups. Among the core set of conserved proteins, we found an emphasis on processes related to the cnidarian-dinoflagellate symbiosis. Genes associated with the algal symbiosis were also independently expanded in both species, but both corals diverged on the identity of ortholog groups expanded, and we found uneven expansions in genes associated with innate immunity and stress response. Our analyses demonstrate that coral genomes can be surprisingly disparate. Future analyses incorporating more genomic data should be able to determine whether the patterns elucidated here are not only characteristic of the differences between S. pistillata and A. digitifera but also representative of corals from the robust and complex clade at large.

Figure 1

Comparison of genic composition of the genomes of S. pistillata and A. digitifera. Genes were assigned to closest genera based on BLASTP best hits, and distribution was visualized in chord diagrams (top 6 genera are shown, remaining hits are summed up in ‘others’). The inlet shows a simplified phylogeny of the phylum Cnidaria to ease orientation and interpretation. (A) Both coral genomes appear similar in composition when queried against the combined NCBI ‘nr’ database and the Aiptasia gene models. The proportion of matching genes in S. pistillata and A. digitifera to other organisms is color-coded as follows: S. pistillata/A. digitifera genes with best matches to Aiptasia (dark green), to Nematostella (light green), to Branchiostoma (lancelet, greenish-yellow), to Saccoglossus (acorn worm, yellow), to Lingula (brachiopod, dark yellow), to Strongylocentrotus (sea urchin, orange), and to ‘others’ (dark orange). Genes without any matches are in red (S. pistillata) and blue (A. digitifera). (B) If coral genomic gene sets are included (i.e., genes from S. pistillata are allowed to match against A. digitifera and vice versa), many more A. digitifera genes match homologs in S. pistillata homologs than vice versa. As a consequence of the asymmetrical matching, the number of A. digitifera matches to other genera is vastly reduced. The proportion of matching genes between S. pistillata and A. digitifera to each other and other organisms is color-coded as follows: S. pistillata and A. digitifera genes matching each other (blue); S. pistillata/A. digitifera genes with best matches to Aiptasia (dark green), to Nematostella (light green), to Lingula (brachiopod, dark yellow), to Saccoglossus (acorn worm, yellow), to Strongylocentrotus (sea urchin, dark yellow), to Crassostrea (oyster, orange); and to ‘others’ (dark orange); S. pistillata genes without any matches (red).

Figure 2

Classification of genomic protein sets of S. pistillata and A. digitifera according to evolutionary relationship. 25,769 S. pistillata proteins were compared to 23,523 A. digitifera proteins and assigned to four categories: (i) one-to-one orthologs (black), (ii) many-to-one and many-to-many orthologs (dark grey), (iii) species-specific proteins without homologs in other species (intermediate gray), and (iv) proteins without easily discernible orthologous relationships (light grey).

Figure 3

Overview of processes and proteins associated with gene expansions in S. pistillata and A. digitifera. (A) Gene Ontology (GO) enrichment of Biological Process (BP) category (p < 0.05) of many-to-one and many-to-many orthologs for S. pistillata and A. digitifera (Dataset S5). (B) Ortholog groups with independently expanded genes in both coral species show different degrees of expansions in both corals and featured many immunity-related genes (Dataset S6). Notably, the NLRC3 examples belong to three distinct ortholog groups (Dataset S6). BMP-1 = Bone Morphogenetic Protein 1; CA = Carbonic Anhyrdase; TNFR19 = Tumor necrosis factor receptor superfamily member 19; TLR1 = Toll-like receptor 1; NLRC3 = NOD-like receptor C3.

Figure 4

Gene expansion of orthologs in S. pistillata and A. digitifera. Maximum Likelihood phylogenetic trees were constructed using RAxML with 1,000 bootstraps. Bootstrap support is indicated at branches of phylogenetic trees. (A) Ortholog expansion displaying a many-to-many relationship for a NOD-like receptor family member, in which A. digitifera harbors 52 proteins in comparison to S. pistillata that harbors only 5 proteins. (B) Ortholog expansion displaying a many-to-one relationship of a TRAF (TNF receptor-associated factor 3) homolog with expansion in S. pistillata (3 genes) and one corresponding counterpart in A. digitifera. (C) Ortholog expansion displaying a many-to-one relationship of a member of the NOD-like receptor family member (NLRC3) with a particularly pronounced expansion in A. digitifera (55 genes) and only one corresponding counterpart in S. pistillata.