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Structural and Evolutionary Relationships of Melanin Cascade Proteins in Cnidarian Innate Immunity - PubMed

  • ️Mon Jan 01 2024

Structural and Evolutionary Relationships of Melanin Cascade Proteins in Cnidarian Innate Immunity

Emily W Van Buren et al. Integr Comp Biol. 2024.

Abstract

Melanin is an essential product that plays an important role in innate immunity in a variety of organisms across the animal kingdom. Melanin synthesis is performed by many organisms using the tyrosine metabolism pathway, a general pathway that utilizes a type-three copper oxidase protein, called PO-candidates (phenoloxidase candidates). While melanin synthesis is well-characterized in organisms like arthropods and humans, it is not as well-understood in non-model organisms such as cnidarians. With the rising anthropomorphic climate change influence on marine ecosystems, cnidarians, specifically corals, are under an increased threat of bleaching and disease. Understanding innate immune pathways, such as melanin synthesis, is vital for gaining insights into how corals may be able to fight these threats. In this study, we use comparative bioinformatic approaches to provide a comprehensive analysis of genes involved in tyrosine-mediated melanin synthesis in cnidarians. Eighteen PO-candidates representing five phyla were studied to identify their evolutionary relationship. Cnidarian species were most similar to chordates due to domain presents in the amino acid sequences. From there, functionally conserved domains in coral proteins were identified in a coral disease dataset. Five stony corals exposed to stony coral tissue loss disease were leveraged to identify 18 putative tyrosine metabolism genes, genes with functionally conserved domains to their Homo sapiens counterpart. To put this pathway in the context of coral health, putative genes were correlated to melanin concentration from tissues of stony coral species in the disease exposure dataset. In this study, tyrosinase was identified in stony corals as correlated to melanin concentrations and likely plays a key role in immunity as a resistance trait. In addition, stony coral genes were assigned to all modules within the tyrosine metabolism pathway, indicating an evolutionary conservation of this pathway across phyla. Overall, this study provides a comprehensive analysis of the genes involved in tyrosine-mediated melanin synthesis in cnidarians.

© The Author(s) 2024. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Fig. 1
Fig. 1

Neighbor-joining tree of type-three copper oxidase proteins. The phylogenetic tree depicted was created in MEGAX using the neighbor-joining method. The tree has a sum branch of 11.0307. The percentage of replicate trees in which the associated taxa clustered together are shown next to the branches. There was a total of 965 position in the final dataset. Phyla of each taxa are highlighted on the branches of the tree, showing branching based on phyla. Pfam domains significant in HMMER search for the PO-candidates. Domains include TYR (PF00264.24), LapA - LapA_dom (PF07974.17), Nup188_SH3 - Nup188_SH3-like (PF21094.1), Laminin_EGF (PF00053.28), Hemo_M - Hemocyanin_M (PF00372.23), Hemo_C - Hemocyanin_C (PF03723.18), Hemo_N - Hemocyanin_N (PF03722.18), and TIL (PF01826.21). If multiple Pfam domains were associated with one protein sequence, color assignment was based on top and subsequent Pfam domain hit in HMMER based on e-value per sequence.

Fig. 2
Fig. 2

Melanin concentration by disease status and species. In this study, Kruskal–Wallis test was used to test melanin concentration differences based on disease status and species. There is no significant difference in melanin concentration between status, but there is significant difference between species (chi-squared = 19.061, df = 4, P-value = 0.0007647). Dunn (1964) test on Kruskal–Wallis multiple comparison P-values adjusted with the Holm method are available in Tables 1 and 2. Overall concentration of melanin by species had an inverse relationship to relative risk, with low-susceptible species such as M. cavernosa having a higher concentration of melanin while high-susceptible species such as O. annularis had lower concentrations of melanin.

Fig. 3
Fig. 3

Tyrosine metabolism genes unassigned to a module Pearson correlation plots in this figure, Pearson correlation of rlog expression of 11 tyrosine metabolism genes to melanin concentration are visualized. Melanin concentration is established on the x-axis, and rlog expression on the y-axis. The five stony coral species cnat (C. natan), mcav (M. cavernosa), oann (O. annularis), past (P. asteroides), and pstr (P. strigosa) are colored on the graphs. All genes have a positive correlation (increased expression of gene with increased melanin concentration) except ADH1A, ADH1B, ADH1C, ADH4, and MAOA with negative correlation (decreased melanin concentration with decreased rlog expression).

Fig. 4
Fig. 4

Tyrosine metabolism module membered genes Pearson correlation plots. In this figure, Pearson correlation of rlog expression of eight representative tyrosine metabolism genes to melanin concentration are visualized. Genes are categorized into KEGG module membership (Thyroid Hormone Biosynthesis, Catecholamine Biosynthesis, Melanin Synthesis, and Tyrosine degradation). Melanin concentration is established on the x-axis, and rlog expression on the y-axis. The five stony coral species cnat (C. natan), mcav (M. cavernosa), oann (O. annularis), past (P. asteroides), and pstr (P. strigosa) are colored on the graphs. Genes in modules have a mixed positive and negative correlation relationship to melanin concentration. Positive correlations include TPO, DBH, TYR-like, HPD, and GSTZ1. Negative correlations include PNMT, TAT, and HGD.

Fig. 5
Fig. 5

Adapted tyrosine metabolism pathway in stony corals. The tyrosine metabolism was adapted from KEGG from H. sapiens, the species with the closest evolutionary relationship to the PO-candidates found in cnidarians. Overlayed are the orthogroups correlation to melanin concentration (bolded as eumelanin/melanin on the tyrosine metabolism adapted pathway). Orthogroups are colored based on their correlation to melanin concentration; positive (red), negative (blue), no correlation but present in the orthologs genes (yellow), not present in stony coral (gray). TH, DDC, and FAH were present as orthologous genes in the stony coral expression but were not correlated to melanin concentration. TYRP1 and DCT were considered not found in the orthogroups as they have uniquely evolved in humans.

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