Evolutionary insights into toxins diversity in Ceriantharia (Cnidaria; Anthozoa)

Abstract

Ceriantharians synthesize and inoculate the toxins found in their stinging cells spread throughout the body. For most cnidarians the putative toxins profile can vary widely depending on the tissue function and the environmental conditions faced by these marine invertebrates. Extensive gene duplications events have impacted the diversity of the toxins system of cnidarians and could explain the rapid emergence of novel toxins. On the other hand, it seems for Ceriantharia, the putative toxins profile does not exhibit major variation, despite occupying different ecological niches. Some species of ceriantharians have a planktonic stage that is highly dispersive, while the benthic phase is characterized by semi-sessile polyp. However, the polyp builds a tube involving the entire column that can play an additional function by protecting against predators and competitors, which could decrease the need to synthesize a wide array of toxins. In the present study, we compare the putative toxins of the larva and polyp of Arachnanthus errans based on the functional annotations of the transcriptomes against annotated protein databases. We seek to understand the evolutionary process of two toxin-like protein families using phylogenetic reconstruction methods with target sequences of the transcriptome of nine ceriantharian species. Our exploration revealed that the larva expresses 70 more toxin-like genes than the polyp, which may relate to abiotic and biotic factors the larva experiences. Our phylogenetic analyses suggest duplication events may have occurred in both toxins-like proteins and the two copies of Kunitz-like proteins might have been present in the common ancestor of Ceriantharia.

Keywords: Development stages; Evolution; Functional genomics; RNASeq; Toxin-like genes; Tube-dwelling anemones.

Graphical abstract

Fig. 1

Gene Ontology (GO) classes matching with transcriptome of the larva and polyp of A. errans. a. Venn Diagram of the amount of terms GO associated with larva and polyp transcriptome. b. Number of GO terms identified to three GO categories in the larva transcriptome. c. Number of GO terms identified to three GO categories in the polyp transcriptome. d. Density of GO terms matching with genes of the larva transcriptome. d. Density of GO terms matching with annotated genes of the larva transcriptome. f. REVIGO analysis with the top 50 GO terms matching with larva and polyp transcriptome. BP = Biological process, CC = Cellular component, MF = Molecular function. Blue color corresponds to the larva. Pink color represents the polyp transcriptome. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

Fig. 2

Top 50 of the GO terms matching with annotated genes of the larva and polyp of A. errans. a. GO terms corresponding to the larva transcriptome. b. GO terms corresponding to the polyp transcriptome.

Fig. 3

Families of toxin-like proteins of the larva and polyp of A. errans. a. Venn Diagram of the amount of families assigned to each development stage and quantity of families shared by larva and polyp phase. b. Families of putative toxins present and absent in both stages and frequency with which each family is attributed to transcripts at each stage of A. errans.

Fig. 4

Toxin-like proteins matching with annotated genes and their functions for the larva and polyp transcriptomes. Abbreviations: ABH: AB hydrolase superfamily, ACHE: Acetylcholinesterase, AVIT: AVIT family, Cono: Conopeptide P-like superfamily, CREC: CREC family, CRISP: Cysteine-rich secretory proteins, Cystatin: Cystatin family, FLEC: Ficolin Lectin family, FLMO: Flavin monoamine oxidase family, GCT: Glutaminyl-peptide cyclotransferase family, GH37: Glycoside hydrolase family 37, Kunitz: Venom kunitz-type family, M12A: Peptidase M12A, MACPF: Membrane attack complex/perforin (macpf) family, M12B: Venom metalloproteinase (M12B) family, M13: Peptidase M13 family, MCO:Multicopper oxidase family, N/A: Non-identified protein family, PHOS: Nucleotide pyrophosphatase/phosphodiesterase family, PLA2: Phospholipase A2 family, PLB: Phospholipase B-like family, PLD: Arthropod phospholipase D family, S1: Peptidase S1 family, Scol-01: Scoloptoxin-01 family, Snaclec: Snaclec family, SNTX: SNTX/VTX toxin family, TLEC: Techylectin-like family, Transferrin: Transferrin family, V302: Venom protein 302, VC3: Venom complement C3 homolog family, Venom lectin: True venom lectin family, WAP: Snake waprin family.

Fig. 5

Maximum likelihood (ML) trees resulting from analyses of the ShK-like proteins and Kunitz-like proteins of the Ceriantharia. 1000 bootstrap replicates were performed for each analyses a. ShK-like tree (-lnL 3854.275). b. Kunitz-like ML tree (-lnL 3679.678). The colored circles represent each species and correspond to the colors disposed of in the figures below. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)