Divergent RNA viruses infecting sea lice, major ectoparasites of fish
Sea lice, the major ectoparasites of fish, have significant economic impacts on wild and farmed finfish, and have been implicated in the decline of wild salmon populations. As blood-feeding arthropods, sea lice may also be reservoirs for viruses infecting fish. However, except for two groups of nega...
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| Vydáno v: | PLoS pathogens Ročník 19; číslo 6; s. e1011386 |
|---|---|
| Hlavní autoři: | , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
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United States
Public Library of Science
22.06.2023
Public Library of Science (PLoS) |
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| ISSN: | 1553-7374, 1553-7366, 1553-7374 |
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| Abstract | Sea lice, the major ectoparasites of fish, have significant economic impacts on wild and farmed finfish, and have been implicated in the decline of wild salmon populations. As blood-feeding arthropods, sea lice may also be reservoirs for viruses infecting fish. However, except for two groups of negative-strand RNA viruses within the order
Mononegavirales
, nothing is known about viruses of sea lice. Here, we used transcriptomic data from three key species of sea lice (
Lepeophtheirus salmonis
,
Caligus clemensi
, and
Caligus rogercresseyi
) to identify 32 previously unknown RNA viruses. The viruses encompassed all the existing phyla of RNA viruses, with many placed in deeply branching lineages that likely represent new families and genera. Importantly, the presence of canonical virus-derived small interfering RNAs (viRNAs) indicates that most of these viruses infect sea lice, even though in some cases their closest classified relatives are only known to infect plants or fungi. We also identified both viRNAs and PIWI-interacting RNAs (piRNAs) from sequences of a bunya-like and two qin-like viruses in
C
.
rogercresseyi
. Our analyses showed that most of the viruses found in
C
.
rogercresseyi
occurred in multiple life stages, spanning from planktonic to parasitic stages. Phylogenetic analysis revealed that many of the viruses infecting sea lice were closely related to those that infect a wide array of eukaryotes with which arthropods associate, including fungi and parasitic tapeworms, implying that over evolutionary time there has been cross-phylum and cross-kingdom switching of viruses between arthropods and other eukaryotes. Overall, this study greatly expands our view of virus diversity in crustaceans, identifies viruses that infect and replicate in sea lice, and provides evidence that over evolutionary time, viruses have switched between arthropods and eukaryotic hosts in other phyla and kingdoms. |
|---|---|
| AbstractList | Sea lice, the major ectoparasites of fish, have significant economic impacts on wild and farmed finfish, and have been implicated in the decline of wild salmon populations. As blood-feeding arthropods, sea lice may also be reservoirs for viruses infecting fish. However, except for two groups of negative-strand RNA viruses within the order Mononegavirales, nothing is known about viruses of sea lice. Here, we used transcriptomic data from three key species of sea lice (Lepeophtheirus salmonis, Caligus clemensi, and Caligus rogercresseyi) to identify 32 previously unknown RNA viruses. The viruses encompassed all the existing phyla of RNA viruses, with many placed in deeply branching lineages that likely represent new families and genera. Importantly, the presence of canonical virus-derived small interfering RNAs (viRNAs) indicates that most of these viruses infect sea lice, even though in some cases their closest classified relatives are only known to infect plants or fungi. We also identified both viRNAs and PIWI-interacting RNAs (piRNAs) from sequences of a bunya-like and two qin-like viruses in C. rogercresseyi. Our analyses showed that most of the viruses found in C. rogercresseyi occurred in multiple life stages, spanning from planktonic to parasitic stages. Phylogenetic analysis revealed that many of the viruses infecting sea lice were closely related to those that infect a wide array of eukaryotes with which arthropods associate, including fungi and parasitic tapeworms, implying that over evolutionary time there has been cross-phylum and cross-kingdom switching of viruses between arthropods and other eukaryotes. Overall, this study greatly expands our view of virus diversity in crustaceans, identifies viruses that infect and replicate in sea lice, and provides evidence that over evolutionary time, viruses have switched between arthropods and eukaryotic hosts in other phyla and kingdoms. Sea lice, the major ectoparasites of fish, have significant economic impacts on wild and farmed finfish, and have been implicated in the decline of wild salmon populations. As blood-feeding arthropods, sea lice may also be reservoirs for viruses infecting fish. However, except for two groups of negative-strand RNA viruses within the order Mononegavirales , nothing is known about viruses of sea lice. Here, we used transcriptomic data from three key species of sea lice ( Lepeophtheirus salmonis , Caligus clemensi , and Caligus rogercresseyi ) to identify 32 previously unknown RNA viruses. The viruses encompassed all the existing phyla of RNA viruses, with many placed in deeply branching lineages that likely represent new families and genera. Importantly, the presence of canonical virus-derived small interfering RNAs (viRNAs) indicates that most of these viruses infect sea lice, even though in some cases their closest classified relatives are only known to infect plants or fungi. We also identified both viRNAs and PIWI-interacting RNAs (piRNAs) from sequences of a bunya-like and two qin-like viruses in C . rogercresseyi . Our analyses showed that most of the viruses found in C . rogercresseyi occurred in multiple life stages, spanning from planktonic to parasitic stages. Phylogenetic analysis revealed that many of the viruses infecting sea lice were closely related to those that infect a wide array of eukaryotes with which arthropods associate, including fungi and parasitic tapeworms, implying that over evolutionary time there has been cross-phylum and cross-kingdom switching of viruses between arthropods and other eukaryotes. Overall, this study greatly expands our view of virus diversity in crustaceans, identifies viruses that infect and replicate in sea lice, and provides evidence that over evolutionary time, viruses have switched between arthropods and eukaryotic hosts in other phyla and kingdoms. Sea lice, the major ectoparasites of fish, have significant economic impacts on wild and farmed finfish, and have been implicated in the decline of wild salmon populations. As blood-feeding arthropods, sea lice may also be reservoirs for viruses infecting fish. However, except for two groups of negative-strand RNA viruses within the order Mononegavirales, nothing is known about viruses of sea lice. Here, we used transcriptomic data from three key species of sea lice (Lepeophtheirus salmonis, Caligus clemensi, and Caligus rogercresseyi) to identify 32 previously unknown RNA viruses. The viruses encompassed all the existing phyla of RNA viruses, with many placed in deeply branching lineages that likely represent new families and genera. Importantly, the presence of canonical virus-derived small interfering RNAs (viRNAs) indicates that most of these viruses infect sea lice, even though in some cases their closest classified relatives are only known to infect plants or fungi. We also identified both viRNAs and PIWI-interacting RNAs (piRNAs) from sequences of a bunya-like and two qin-like viruses in C. rogercresseyi. Our analyses showed that most of the viruses found in C. rogercresseyi occurred in multiple life stages, spanning from planktonic to parasitic stages. Phylogenetic analysis revealed that many of the viruses infecting sea lice were closely related to those that infect a wide array of eukaryotes with which arthropods associate, including fungi and parasitic tapeworms, implying that over evolutionary time there has been cross-phylum and cross-kingdom switching of viruses between arthropods and other eukaryotes. Overall, this study greatly expands our view of virus diversity in crustaceans, identifies viruses that infect and replicate in sea lice, and provides evidence that over evolutionary time, viruses have switched between arthropods and eukaryotic hosts in other phyla and kingdoms. Sea lice are parasitic copepods and the major ectoparasites of fish. They have significant impacts on wild and farmed fish, and have been implicated in the decline of salmon populations; yet, viruses of sea lice are largely unknown. Here, we analyzed transcriptomes and small RNAs from three key species of sea lice and identified 32 previously unknown RNA viruses, many of which were actively replicating. Not only do these data greatly expand the known viral diversity in copepods, phylogenetic analysis provides evidence that over evolutionary time there has been extensive transmission of viruses between arthropods and other eukaryotes. Viruses replicating in sea lice included hypo-like and sobemo-like viruses, which previously were not known to infect arthropods. This study advances our view of the diversity and evolution of RNA viruses associated with sea lice, obtains genetic blueprints of viruses infecting sea lice, and provides approaches that may be further used to identify unknown viral pathogens in other ecologically and economically important crustaceans. Sea lice, the major ectoparasites of fish, have significant economic impacts on wild and farmed finfish, and have been implicated in the decline of wild salmon populations. As blood-feeding arthropods, sea lice may also be reservoirs for viruses infecting fish. However, except for two groups of negative-strand RNA viruses within the order Mononegavirales, nothing is known about viruses of sea lice. Here, we used transcriptomic data from three key species of sea lice (Lepeophtheirus salmonis, Caligus clemensi, and Caligus rogercresseyi) to identify 32 previously unknown RNA viruses. The viruses encompassed all the existing phyla of RNA viruses, with many placed in deeply branching lineages that likely represent new families and genera. Importantly, the presence of canonical virus-derived small interfering RNAs (viRNAs) indicates that most of these viruses infect sea lice, even though in some cases their closest classified relatives are only known to infect plants or fungi. We also identified both viRNAs and PIWI-interacting RNAs (piRNAs) from sequences of a bunya-like and two qin-like viruses in C. rogercresseyi. Our analyses showed that most of the viruses found in C. rogercresseyi occurred in multiple life stages, spanning from planktonic to parasitic stages. Phylogenetic analysis revealed that many of the viruses infecting sea lice were closely related to those that infect a wide array of eukaryotes with which arthropods associate, including fungi and parasitic tapeworms, implying that over evolutionary time there has been cross-phylum and cross-kingdom switching of viruses between arthropods and other eukaryotes. Overall, this study greatly expands our view of virus diversity in crustaceans, identifies viruses that infect and replicate in sea lice, and provides evidence that over evolutionary time, viruses have switched between arthropods and eukaryotic hosts in other phyla and kingdoms.Sea lice, the major ectoparasites of fish, have significant economic impacts on wild and farmed finfish, and have been implicated in the decline of wild salmon populations. As blood-feeding arthropods, sea lice may also be reservoirs for viruses infecting fish. However, except for two groups of negative-strand RNA viruses within the order Mononegavirales, nothing is known about viruses of sea lice. Here, we used transcriptomic data from three key species of sea lice (Lepeophtheirus salmonis, Caligus clemensi, and Caligus rogercresseyi) to identify 32 previously unknown RNA viruses. The viruses encompassed all the existing phyla of RNA viruses, with many placed in deeply branching lineages that likely represent new families and genera. Importantly, the presence of canonical virus-derived small interfering RNAs (viRNAs) indicates that most of these viruses infect sea lice, even though in some cases their closest classified relatives are only known to infect plants or fungi. We also identified both viRNAs and PIWI-interacting RNAs (piRNAs) from sequences of a bunya-like and two qin-like viruses in C. rogercresseyi. Our analyses showed that most of the viruses found in C. rogercresseyi occurred in multiple life stages, spanning from planktonic to parasitic stages. Phylogenetic analysis revealed that many of the viruses infecting sea lice were closely related to those that infect a wide array of eukaryotes with which arthropods associate, including fungi and parasitic tapeworms, implying that over evolutionary time there has been cross-phylum and cross-kingdom switching of viruses between arthropods and other eukaryotes. Overall, this study greatly expands our view of virus diversity in crustaceans, identifies viruses that infect and replicate in sea lice, and provides evidence that over evolutionary time, viruses have switched between arthropods and eukaryotic hosts in other phyla and kingdoms. |
| Audience | Academic |
| Author | Suttle, Curtis A. Hunt, Brian P. V. Hirai, Junya Chang, Tianyi |
| AuthorAffiliation | Division of Clinical Research, UNITED STATES 6 Department of Botany, University of British Columbia, Vancouver, Canada 3 Hakai Institute, Campbell River, Canada 4 Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Japan 5 Department of Microbiology and Immunology, University of British Columbia, Vancouver, Canada 1 Department of Earth, Ocean and Atmospheric Sciences, University of British Columbia, Vancouver, Canada 2 Institute for the Oceans and Fisheries, University of British Columbia, Vancouver, Canada |
| AuthorAffiliation_xml | – name: 6 Department of Botany, University of British Columbia, Vancouver, Canada – name: 5 Department of Microbiology and Immunology, University of British Columbia, Vancouver, Canada – name: 3 Hakai Institute, Campbell River, Canada – name: Division of Clinical Research, UNITED STATES – name: 1 Department of Earth, Ocean and Atmospheric Sciences, University of British Columbia, Vancouver, Canada – name: 4 Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Japan – name: 2 Institute for the Oceans and Fisheries, University of British Columbia, Vancouver, Canada |
| Author_xml | – sequence: 1 givenname: Tianyi orcidid: 0000-0002-3131-4884 surname: Chang fullname: Chang, Tianyi – sequence: 2 givenname: Brian P. V. surname: Hunt fullname: Hunt, Brian P. V. – sequence: 3 givenname: Junya surname: Hirai fullname: Hirai, Junya – sequence: 4 givenname: Curtis A. orcidid: 0000-0002-0372-0033 surname: Suttle fullname: Suttle, Curtis A. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/37347729$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_1016_j_tim_2025_03_005 crossref_primary_10_3389_fgene_2025_1633603 crossref_primary_10_3390_v17070932 crossref_primary_10_1371_journal_ppat_1013255 crossref_primary_10_1073_pnas_2420162122 crossref_primary_10_3390_v17010095 |
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| ContentType | Journal Article |
| Copyright | Copyright: © 2023 Chang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. COPYRIGHT 2023 Public Library of Science 2023 Chang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2023 Chang et al 2023 Chang et al |
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| DOI | 10.1371/journal.ppat.1011386 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Current address: Bigelow Laboratory for Ocean Sciences, Boothbay, Maine, United States of America The authors have declared that no competing interests exist. |
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| Snippet | Sea lice, the major ectoparasites of fish, have significant economic impacts on wild and farmed finfish, and have been implicated in the decline of wild salmon... |
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| SubjectTerms | Analysis Animals Arthropoda Arthropods Biological evolution Biology and life sciences Caligus rogercresseyi Control Copepoda - genetics Crustaceans Diseases Earth Sciences Economic impact Ectoparasites Eukaryotes Fish Fish Diseases Fish populations Fungi Genera Genetic aspects Growth Identification and classification Lice Medicine and Health Sciences Nematodes New families Phylogenetics Phylogeny RNA RNA polymerase RNA viruses RNA Viruses - genetics RNA, Small Interfering Salmon Salmon - genetics Salmon - parasitology Taxonomy Transcriptomics Trees Viral infections Viruses |
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| Title | Divergent RNA viruses infecting sea lice, major ectoparasites of fish |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/37347729 https://www.proquest.com/docview/2838335139 https://www.proquest.com/docview/2829428366 https://pubmed.ncbi.nlm.nih.gov/PMC10287012 https://doaj.org/article/de005ab6e78c47718d8fb2bbade0b618 http://dx.doi.org/10.1371/journal.ppat.1011386 |
| Volume | 19 |
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