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The cnidarian parasite utilizes inherited and recruited venom-like compounds during infection.

作者信息

Americus Benjamin, Hams Nicole, Klompen Anna M L, Alama-Bermejo Gema, Lotan Tamar, Bartholomew Jerri L, Atkinson Stephen D

机构信息

Department of Microbiology, Oregon State University, Corvallis, Oregon, United States of America.

Columbia River Fish and Wildlife Conservation Office, U.S. Fish and Wildlife Service, Vancouver, Washington, United States of America.

出版信息

PeerJ. 2021 Dec 15;9:e12606. doi: 10.7717/peerj.12606. eCollection 2021.


DOI:10.7717/peerj.12606
PMID:35003924
原文链接:https://pmc.ncbi.nlm.nih.gov/articles/PMC8684318/
Abstract

BACKGROUND: Cnidarians are the most ancient venomous organisms. They store a cocktail of venom proteins inside unique stinging organelles called nematocysts. When a cnidarian encounters chemical and physical cues from a potential threat or prey animal, the nematocyst is triggered and fires a harpoon-like tubule to penetrate and inject venom into the prey. Nematocysts are present in all Cnidaria, including the morphologically simple Myxozoa, which are a speciose group of microscopic, spore-forming, obligate parasites of fish and invertebrates. Rather than predation or defense, myxozoans use nematocysts for adhesion to hosts, but the involvement of venom in this process is poorly understood. Recent work shows some myxozoans have a reduced repertoire of venom-like compounds (VLCs) relative to free-living cnidarians, however the function of these proteins is not known. METHODS: We searched for VLCs in the nematocyst proteome and a time-series infection transcriptome of , a myxozoan parasite of salmonid fish. We used four parallel approaches to detect VLCs: BLAST and HMMER searches to preexisting cnidarian venom datasets, the machine learning tool ToxClassifier, and structural modeling of nematocyst proteomes. Sequences that scored positive by at least three methods were considered VLCs. We then mapped their time-series expressions in the fish host and analyzed their phylogenetic relatedness to sequences from other venomous animals. RESULTS: We identified eight VLCs, all of which have closely related sequences in other myxozoan datasets, suggesting a conserved venom profile across Myxozoa, and an overall reduction in venom diversity relative to free-living cnidarians. Expression of the VLCs over the 3-week fish infection varied considerably: three sequences were most expressed at one day post-exposure in the fish's gills; whereas expression of the other five VLCs peaked at 21 days post-exposure in the intestines, coinciding with the formation of mature parasite spores with nematocysts. Expression of VLC genes early in infection, prior to the development of nematocysts, suggests venoms in have been repurposed to facilitate parasite invasion and proliferation within the host. Molecular phylogenetics suggested some VLCs were inherited from a cnidarian ancestor, whereas others were more closely related to sequences from venomous non-Cnidarian organisms and thus may have gained qualities of venom components convergent evolution. The presence of VLCs and their differential expression during parasite infection enrich the concept of what functions a "venom" can have and represent targets for designing therapeutics against myxozoan infections.

摘要
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/1b6e/8684318/085f5ca84d37/peerj-09-12606-g005.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/1b6e/8684318/3c06d81a77de/peerj-09-12606-g001.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/1b6e/8684318/58a82d5d3a01/peerj-09-12606-g002.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/1b6e/8684318/d72b6587d4a5/peerj-09-12606-g003.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/1b6e/8684318/a3cd23cd5b1a/peerj-09-12606-g004.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/1b6e/8684318/085f5ca84d37/peerj-09-12606-g005.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/1b6e/8684318/3c06d81a77de/peerj-09-12606-g001.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/1b6e/8684318/58a82d5d3a01/peerj-09-12606-g002.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/1b6e/8684318/d72b6587d4a5/peerj-09-12606-g003.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/1b6e/8684318/a3cd23cd5b1a/peerj-09-12606-g004.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/1b6e/8684318/085f5ca84d37/peerj-09-12606-g005.jpg

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引用本文的文献

[1]
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[2]
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[3]
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: a cnidarian parasite of annelids and salmonids.

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[5]
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本文引用的文献

[1]
Recruitment of toxin-like proteins with ancestral venom function supports endoparasitic lifestyles of Myxozoa.

PeerJ. 2021-4-26

[2]
Serine protease inhibitors of the whirling disease parasite Myxobolus cerebralis (Cnidaria, Myxozoa): Expression profiling and functional predictions.

PLoS One. 2021

[3]
A tale of two fish: Comparative transcriptomics of resistant and susceptible steelhead following exposure to Ceratonova shasta highlights differences in parasite recognition.

PLoS One. 2021

[4]
An atypical and functionally diverse family of Kunitz-type cysteine/serine proteinase inhibitors secreted by the helminth parasite Fasciola hepatica.

Sci Rep. 2020-11-26

[5]
Toxin-like neuropeptides in the sea anemone unravel recruitment from the nervous system to venom.

Proc Natl Acad Sci U S A. 2020-11-3

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Mar Drugs. 2020-10-6

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Genetic Diversity of Serine Protease Inhibitors in Myxozoan (Cnidaria, Myxozoa) Fish Parasites.

Microorganisms. 2020-9-29

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PI16 attenuates response to sorafenib and represents a predictive biomarker in hepatocellular carcinoma.

Cancer Med. 2020-10

[9]
Transcriptomic Analysis of Four Cerianthid (Cnidaria, Ceriantharia) Venoms.

Mar Drugs. 2020-8-5

[10]
A comparison of the structure and function of nematocysts in free-living and parasitic cnidarians (Myxozoa).

Int J Parasitol. 2020-9

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