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Photoreceptor Diversification Accompanies the Evolution of Anthozoa.

ABSTRACT: Anthozoan corals are an ecologically important group of cnidarians, which power the productivity of reef ecosystems. They are sessile, inhabit shallow, tropical oceans and are highly dependent on sun- and moonlight to regulate sexual reproduction, phototaxis, and photosymbiosis. However, their exposure to high levels of sunlight also imposes an increased risk of UV-induced DNA damage. How have these challenging photic environments influenced photoreceptor evolution and function in these animals? To address this question, we initially screened the cnidarian photoreceptor repertoire for Anthozoa-specific signatures by a broad-scale evolutionary analysis. We compared transcriptomic data of more than 36 cnidarian species and revealed a more diverse photoreceptor repertoire in the anthozoan subphylum than in the subphylum Medusozoa. We classified the three principle opsin classes into distinct subtypes and showed that Anthozoa retained all three classes, which diversified into at least six subtypes. In contrast, in Medusozoa, only one class with a single subtype persists. Similarly, in Anthozoa, we documented three photolyase classes and two cryptochrome (CRY) classes, whereas CRYs are entirely absent in Medusozoa. Interestingly, we also identified one anthozoan CRY class, which exhibited unique tandem duplications of the core functional domains. We next explored the functionality of anthozoan photoreceptors in the model species Exaiptasia diaphana (Aiptasia), which recapitulates key photo-behaviors of corals. We show that the diverse opsin genes are differentially expressed in important life stages common to reef-building corals and Aiptasia and that CRY expression is light regulated. We thereby provide important clues linking coral evolution with photoreceptor diversification.

SUBMITTER: Gornik SG

PROVIDER: S-EPMC8097283 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Gene duplication facilitates functional diversification and provides greater phenotypic flexibility to an organism. Expanded gene families arise through repeated gene duplication but the extent of functional divergence that accompanies each paralogous gene is generally unexplored because of the difficulty in isolating the effects of single family members. The telomere-associated (TLO) gene family is a remarkable example of gene family expansion, with 14 members in the more pathogenic Candida albicans relative to two TLO genes in the closely-related species C. dubliniensis. TLO genes encode interchangeable Med2 subunits of the major transcriptional regulatory complex Mediator. To identify biological functions associated with each C. albicans TLO, expression of individual family members was regulated using a Tet-ON system and the strains were assessed across a range of phenotypes involved in growth and virulence traits. All TLOs affected multiple phenotypes and a single phenotype was often affected by multiple TLOs, including simple phenotypes such as cell aggregation and complex phenotypes such as virulence in a Galleria mellonella model of infection. No phenotype was regulated by all TLOs, suggesting neofunctionalization or subfunctionalization of ancestral properties among different family members. Importantly, regulation of three phenotypes could be mapped to individual polymorphic sites among the TLO genes, including an indel correlated with two phenotypes, growth in sucrose and macrophage killing. Different selective pressures have operated on the TLO sequence, with the 5' conserved Med2 domain experiencing purifying selection and the gene/clade-specific 3' end undergoing extensive positive selection that may contribute to the impact of individual TLOs on phenotypic variability. Therefore, expansion of the TLO gene family has conferred unique regulatory properties to each paralog such that it influences a range of phenotypes. We posit that the genetic diversity associated with this expansion contributed to C. albicans success as a commensal and opportunistic pathogen.

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Photoreceptor Diversification Accompanies the Evolution of Anthozoa.

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