Dataset Information

Horizontal transfer of a natterin-like toxin encoding gene within the holobiont of the reef building coral Acropora digitifera (Cnidaria: Anthozoa: Scleractinia) and across multiple animal linages.

ABSTRACT: Phylogenetic evidence is provided for horizontal transfer of a natterin-like toxin encoding gene from fungi into the genome of the coral Acropora digitifera. Sequencing analysis of the coral tissues supported that a fungal taxon predicted to be the most likely gene donor was represented in the coral microbiome. Further bioinformatics data suggested widespread recruitment of the natterin-like gene into venomous terrestrial invertebrates, and repositioning of this gene to non-toxic functions in non-venomous teleost fish.

SUBMITTER: Gacesa R

PROVIDER: S-EPMC7284397 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Horizontal transfer of a natterin-like toxin encoding gene within the holobiont of the reef building coral <i>Acropora digitifera</i> (Cnidaria: Anthozoa: Scleractinia) and across multiple animal linages.

Gacesa Ranko R Hung Julia Yun-Hsuan JY Bourne David G DG Long Paul F PF

Journal of venom research 20200417

Phylogenetic evidence is provided for horizontal transfer of a natterin-like toxin encoding gene from fungi into the genome of the coral <i>Acropora digitifera</i>. Sequencing analysis of the coral tissues supported that a fungal taxon predicted to be the most likely gene donor was represented in the coral microbiome. Further bioinformatics data suggested widespread recruitment of the natterin-like gene into venomous terrestrial invertebrates, and repositioning of this gene to non-toxic function ...[more]

PMID: 32566125

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Project description:BackgroundGene duplication followed by adaptive selection is a well-accepted process leading to toxin diversification in venoms. However, emergent genomic, transcriptomic and proteomic evidence now challenges this role to be at best equivocal to other processess . Cnidaria are arguably the most ancient phylum of the extant metazoa that are venomous and such provide a definitive ancestral anchor to examine the evolution of this trait.MethodsHere we compare predicted toxins from the translated genome of the coral Acropora digitifera to putative toxins revealed by proteomic analysis of soluble proteins discharged from nematocysts, to determine the extent to which gene duplications contribute to venom innovation in this reef-building coral species. A new bioinformatics tool called HHCompare was developed to detect potential gene duplications in the genomic data, which is made freely available ( https://github.com/rgacesa/HHCompare ).ResultsA total of 55 potential toxin encoding genes could be predicted from the A. digitifera genome, of which 36 (65 %) had likely arisen by gene duplication as evinced using the HHCompare tool and verified using two standard phylogeny methods. Surprisingly, only 22 % (12/55) of the potential toxin repertoire could be detected following rigorous proteomic analysis, for which only half (6/12) of the toxin proteome could be accounted for as peptides encoded by the gene duplicates. Biological activities of these toxins are dominatedby putative phospholipases and toxic peptidases.ConclusionsGene expansions in A. digitifera venom are the most extensive yet described in any venomous animal, and gene duplication plays a significant role leading to toxin diversification in this coral species. Since such low numbers of toxins were detected in the proteome, it is unlikely that the venom is evolving rapidly by prey-driven positive natural selection. Rather we contend that the venom has a defensive role deterring predation or harm from interspecific competition and overgrowth by fouling organisms. Factors influencing translation of toxin encoding genes perhaps warrants more profound experimental consideration.

Project description:BackgroundUnderstanding the mechanisms by which natural populations cope with environmental stress is paramount to predict their persistence in the face of escalating anthropogenic impacts. Reef-building corals are increasingly exposed to local and global stressors that alter nutritional status causing reduced fitness and mortality, however, these responses can vary considerably across species and populations.Methodology/principal findingsWe compare the expression of 22 coral host genes in individuals from an inshore and an offshore reef location using quantitative Reverse Transcription-PCR (qRT-PCR) over the course of 26 days following translocation into a shaded, filtered seawater environment. Declines in lipid content and PSII activity of the algal endosymbionts (Symbiodinium ITS-1 type C2) over the course of the experiment indicated that heterotrophic uptake and photosynthesis were limited, creating nutritional deprivation conditions. Regulation of coral host genes involved in metabolism, CO2 transport and oxidative stress could be detected already after five days, whereas PSII activity took twice as long to respond. Opposing expression trajectories of Tgl, which releases fatty acids from the triacylglycerol storage, and Dgat1, which catalyses the formation of triglycerides, indicate that the decline in lipid content can be attributed, at least in part, by mobilisation of triacylglycerol stores. Corals from the inshore location had initially higher lipid content and showed consistently elevated expression levels of two genes involved in metabolism (aldehyde dehydrogenase) and calcification (carbonic anhydrase).Conclusions/significanceCoral host gene expression adjusts rapidly upon change in nutritional conditions, and therefore can serve as an early signature of imminent coral stress. Consistent gene expression differences between populations indicate that corals acclimatize and/or adapt to local environments. Our results set the stage for analysis of these processes in natural coral populations, to better understand the responses of coral communities to global climate change and to develop more efficient management strategies.

Dataset Information

Horizontal transfer of a natterin-like toxin encoding gene within the holobiont of the reef building coral Acropora digitifera (Cnidaria: Anthozoa: Scleractinia) and across multiple animal linages.

Publications

Horizontal transfer of a natterin-like toxin encoding gene within the holobiont of the reef building coral <i>Acropora digitifera</i> (Cnidaria: Anthozoa: Scleractinia) and across multiple animal linages.

Similar Datasets

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