Transcriptome mining extends the host range of the Flaviviridae to non-bilaterians

The flavivirids (family Flaviviridae) are a group of positive-sense RNA viruses that include well-documented agents of human disease. Despite their importance and ubiquity, the timescale of flavivirid evolution is uncertain. An ancient origin, spanning millions of years, is supported by their presen...

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Main Authors: Mifsud, Jonathon C. O., Costa, Vincenzo A., Petrone, Mary E., Marzinelli, Ezequiel Miguel, Holmes, Edward C., Harvey, Erin
Other Authors: Singapore Centre for Environmental Life Sciences and Engineering
Format: Journal Article
Language:English
Published: 2024
Subjects:
Online Access:https://hdl.handle.net/10356/173625
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author Mifsud, Jonathon C. O.
Costa, Vincenzo A.
Petrone, Mary E.
Marzinelli, Ezequiel Miguel
Holmes, Edward C.
Harvey, Erin
author2 Singapore Centre for Environmental Life Sciences and Engineering
author_facet Singapore Centre for Environmental Life Sciences and Engineering
Mifsud, Jonathon C. O.
Costa, Vincenzo A.
Petrone, Mary E.
Marzinelli, Ezequiel Miguel
Holmes, Edward C.
Harvey, Erin
author_sort Mifsud, Jonathon C. O.
collection NTU
description The flavivirids (family Flaviviridae) are a group of positive-sense RNA viruses that include well-documented agents of human disease. Despite their importance and ubiquity, the timescale of flavivirid evolution is uncertain. An ancient origin, spanning millions of years, is supported by their presence in both vertebrates and invertebrates and by the identification of a flavivirus-derived endogenous viral element in the peach blossom jellyfish genome (Craspedacusta sowerbii, phylum Cnidaria), implying that the flaviviruses arose early in the evolution of the Metazoa. To date, however, no exogenous flavivirid sequences have been identified in these hosts. To help resolve the antiquity of the Flaviviridae, we mined publicly available transcriptome data across the Metazoa. From this, we expanded the diversity within the family through the identification of 32 novel viral sequences and extended the host range of the pestiviruses to include amphibians, reptiles, and ray-finned fish. Through co-phylogenetic analysis we found cross-species transmission to be the predominate macroevolutionary event across the non-vectored flavivirid genera (median, 68 per cent), including a cross-species transmission event between bats and rodents, although long-term virus-host co-divergence was still a regular occurrence (median, 23 per cent). Notably, we discovered flavivirus-like sequences in basal metazoan species, including the first associated with Cnidaria. This sequence formed a basal lineage to the genus Flavivirus and was closer to arthropod and crustacean flaviviruses than those in the tamanavirus group, which includes a variety of invertebrate and vertebrate viruses. Combined, these data attest to an ancient origin of the flaviviruses, likely close to the emergence of the metazoans 750-800 million years ago.
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spelling ntu-10356/1736252024-02-22T15:30:23Z Transcriptome mining extends the host range of the Flaviviridae to non-bilaterians Mifsud, Jonathon C. O. Costa, Vincenzo A. Petrone, Mary E. Marzinelli, Ezequiel Miguel Holmes, Edward C. Harvey, Erin Singapore Centre for Environmental Life Sciences and Engineering Medicine, Health and Life Sciences Flaviviridae Pestivirus The flavivirids (family Flaviviridae) are a group of positive-sense RNA viruses that include well-documented agents of human disease. Despite their importance and ubiquity, the timescale of flavivirid evolution is uncertain. An ancient origin, spanning millions of years, is supported by their presence in both vertebrates and invertebrates and by the identification of a flavivirus-derived endogenous viral element in the peach blossom jellyfish genome (Craspedacusta sowerbii, phylum Cnidaria), implying that the flaviviruses arose early in the evolution of the Metazoa. To date, however, no exogenous flavivirid sequences have been identified in these hosts. To help resolve the antiquity of the Flaviviridae, we mined publicly available transcriptome data across the Metazoa. From this, we expanded the diversity within the family through the identification of 32 novel viral sequences and extended the host range of the pestiviruses to include amphibians, reptiles, and ray-finned fish. Through co-phylogenetic analysis we found cross-species transmission to be the predominate macroevolutionary event across the non-vectored flavivirid genera (median, 68 per cent), including a cross-species transmission event between bats and rodents, although long-term virus-host co-divergence was still a regular occurrence (median, 23 per cent). Notably, we discovered flavivirus-like sequences in basal metazoan species, including the first associated with Cnidaria. This sequence formed a basal lineage to the genus Flavivirus and was closer to arthropod and crustacean flaviviruses than those in the tamanavirus group, which includes a variety of invertebrate and vertebrate viruses. Combined, these data attest to an ancient origin of the flaviviruses, likely close to the emergence of the metazoans 750-800 million years ago. Published version E.C.H. is supported by a National Health and Medical Research Council Australian Laureate Fellowship (FL170100022). J.C.O.M. is supported by the Australian Government’s Research Training Program Scholarship. E.M.M. received funding from the Australian Research Council (DP180104041). 2024-02-19T07:33:42Z 2024-02-19T07:33:42Z 2023 Journal Article Mifsud, J. C. O., Costa, V. A., Petrone, M. E., Marzinelli, E. M., Holmes, E. C. & Harvey, E. (2023). Transcriptome mining extends the host range of the Flaviviridae to non-bilaterians. Virus Evolution, 9(1), 1-17. https://dx.doi.org/10.1093/ve/veac124 2057-1577 https://hdl.handle.net/10356/173625 10.1093/ve/veac124 36694816 2-s2.0-85159195728 1 9 1 17 en Virus Evolution © The Author(s) 2023. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. application/pdf
spellingShingle Medicine, Health and Life Sciences
Flaviviridae
Pestivirus
Mifsud, Jonathon C. O.
Costa, Vincenzo A.
Petrone, Mary E.
Marzinelli, Ezequiel Miguel
Holmes, Edward C.
Harvey, Erin
Transcriptome mining extends the host range of the Flaviviridae to non-bilaterians
title Transcriptome mining extends the host range of the Flaviviridae to non-bilaterians
title_full Transcriptome mining extends the host range of the Flaviviridae to non-bilaterians
title_fullStr Transcriptome mining extends the host range of the Flaviviridae to non-bilaterians
title_full_unstemmed Transcriptome mining extends the host range of the Flaviviridae to non-bilaterians
title_short Transcriptome mining extends the host range of the Flaviviridae to non-bilaterians
title_sort transcriptome mining extends the host range of the flaviviridae to non bilaterians
topic Medicine, Health and Life Sciences
Flaviviridae
Pestivirus
url https://hdl.handle.net/10356/173625
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