Kibenge F et al. (2024), Parvoviruses of Aquatic Animals.

ECB-ART-53221

Pathogens 2024 Jul 26;138:. doi: 10.3390/pathogens13080625.

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Parvoviruses of Aquatic Animals.

Kibenge F , Kibenge M , Montes de Oca M , Godoy M .

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Family Parvoviridae consists of small, non-enveloped viruses with linear, single-stranded DNA genomes of approximately 4-6 kilobases, subdivided into three subfamilies, Parvovirinae, Densovirinae, and Hamaparvovirinae, and unassigned genus Metalloincertoparvovirus. Parvoviruses of aquatic animals infect crustaceans, mollusks, and finfish. This review describes these parvoviruses, which are highly host-specific and associated with mass morbidity and mortality in both farmed and wild aquatic animals. They include Cherax quadricarinatus densovirus (CqDV) in freshwater crayfish in Queensland, Australia; sea star-associated densovirus (SSaDV) in sunflower sea star on the Northeastern Pacific Coast; Clinch densovirus 1 in freshwater mussels in the Clinch River, Virginia, and Tennessee, USA, in subfamily Densovirinae; hepatopancreatic parvovirus (HPV) and infectious hypodermal and hematopoietic necrosis virus (IHHNV) in farmed shrimp worldwide; Syngnathid ichthamaparvovirus 1 in gulf pipefish in the Gulf of Mexico and parts of South America; tilapia parvovirus (TiPV) in farmed tilapia in China, Thailand, and India, in the subfamily Hamaparvovirinae; and Penaeus monodon metallodensovirus (PmMDV) in Vietnamese P. monodon, in unassigned genus Metalloincertoparvovirus. Also included in the family Parvoviridae are novel parvoviruses detected in both diseased and healthy animals using metagenomic sequencing, such as zander parvovirus from zander in Hungary and salmon parvovirus from sockeye salmon smolts in British Columbia, Canada.

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	Figure 6. The geographic origin of Parvoviridae sequences from marine animal hosts. The Parvoviridae sequences were downloaded from the NCBI Virus Sequences for Discovery portal [64].
	Figure 1. Parvoviridae. Schematic representation of a parvovirus particle showing the non-enveloped, round, T = 1 icosahedral symmetry, 22–28 nm in diameter. The capsid consists of 60 copies of CP protein. (Reproduced from [33]. Source: SwissBioPics. The images are licensed under a Creative Commons Attribution 4.0 International (CC BY 4.0) License https://creativecommons.org/licenses/by/4.0/ (accessed 21 December 2023)).
	Figure 2. The current genera are listed by subfamily in the family Parvoviridae. A star indicates genera affecting marine animal hosts.
	Figure 3. Bayesian inference of the entire Parvoviridae family, based on the SF3 helicase domain (155-aa-long) of the NS1 protein (by the BEAST v.1.10 suite using the LG+I+G substitution model, with a lognormal relaxed clock and Yule speciation model through 100 million generations). The posterior probability values are shown as node labels, if significant (>0.7). The nodes of each genus are labeled with a spot, color coded based on subfamily affiliation. Taxa and viruses introduced in this proposal are highlighted in red. Proposed taxa and viruses in the TP by Duarte et al. (create 1 new species in the genus Chaphamaparvovirus, and 1 new species in the genus Dependoparvovirus, in the family Parvoviridae) are marked with a star (*). (Reproduced from [31] with permission from Dr. Judit J. Pénzes, Chair, ICTV Parvoviridae Study Group.).
	Figure 4. Cladogram of subfamilies Hamaparvovirinae, Parvovirinae, and Densovirinae. The genome organizations of members of the representative genera of the three subfamilies are shown. The novel tilapia parvovirus HMU-HKU-1 discovered in this study is labeled with a red circle (●). The genera and subfamilies described in the newly proposed ICTV parvovirus taxonomic classification are highlighted in red. (Reproduced under Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/ (accessed 21 December 2023)) from [29], Figure 2).
	Figure 5. Summary of parvovirus replication requirements. (1) Most autonomous parvoviruses require mitotically active cells (S/G2 phase) to provide host replication factors to replicate their viral genome. (2) Recently, human bocavirus 1 (HBoV1) was demonstrated to replicate in non-dividing airway epithelial cells through the hijacking of DNA repair machinery [42,43]. (3) Dependoparvoviruses depend on coinfection with a helper virus to undergo productive replication in a host cell. (Reproduced under Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/ (accessed 21 December 2023)) from [38], Figure 4).
	Figure 7. Size variations observed in 50-day-old Penaeus monodon with infectious hypodermal and hematopoietic necrosis virus (IHHNV) (A,B). (Reprinted from Aquaculture, Vol. 289 (3–4), Rai, P., Size variations observed in 50-day-old Penaeus monodon with infectious hypodermal and hematopoietic necrosis virus (IHHNV) (A,B). Reproduced from [146], Figure 10, under Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/ (accessed 21 December 2023))).
	Figure 8. Outbreaks, clinical symptoms, and pathological analysis. (A) Healthy tilapia; (B) tilapia disease outbreak in cage-cultured results in massive mortality (August 2015; Jinmen, Hubei province, China); (C,D) gross pathological signs of infected tilapia, including hemorrhages on the lower jaw, anterior abdominal, and the fin bases, accompanied by exophthalmos eyes and pronounced ocular lesions. (E) Healthy spleen; (F) moderated diseased spleen infected on the 3rd day post TiPV infection; (G,H) severe diseased spleen infected on the 5th day post TiPV infection. Lymphocytes (white arrow) and macrophages (white triangular arrowheads) in diseased spleen sinusoids, necrotic splenocytes (red arrow), virus inclusion body (black arrow), and melanomacrophage centers (asterisk) in affected spleen; (I) healthy brain; (J) moderate diseased brain infected on the 3rd day post TiPV infection, vacuolated neurons with marginated nucleus (red arrow); (K,L) severe diseased brain infected on the 5th day post TiPV infection, vacuolated neurons with marginated nucleus (red arrow), lymphocytes (white arrow) in the blood vessel, edema of cerebral cortex (black arrow). HE staining. Bar = 20 um (A,B,E,F), 50 um (D), 5 um (C). (Reproduced under Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/ (accessed 21 December 2023)) from [25], Figure 1).
	Figure 9. Morphology of the tilapia brain cells (TiBs) and cytopathic effect (CPE) induction on TiBs induced by TiPV and transmission electron micrographs of the TiPV-infected TiB cells. (A) The TiB cells at passage 1, 10 days; (B) the TiB cells at passage 2, 3 days; (C) TiB cells infected with TiPV at passage 3, 5 days post infection; (D) TiB cells infected with TiPV at passage 6, 3 days post infection (bar = 100 μm). (E) Virus particles existed in the cytoplasm and nuclei (white arrow), Nu: nucleus. (bar, 1 μm); (F) high magnification of the region in the white rectangular box indicated in Panel A, virus particles aggregated in the cytoplasm (bar, 200 nm); (G) the virus releasing at the plasma membrane of the TiB cell (bar, 200 nm); (H) purified TiPV particles negatively stained with 2% phosphotungstic acid (bar, 200 nm). (Reproduced under Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/ (accessed 21 December 2023)) from [25], Figure 2).
	Figure 10. Phylogenetic analysis of zander/M5/2015/HUN (OK236393, bold letters) and representatives of 10 genera in the subfamily Parvovirinae based on the ~460 aa long tripartite helicase domain of NS1. The dendrogram was constructed based on an amino acid sequence alignment of tripartite helicase domains by Bayesian Evolutionary Analysis Utility version v1.10.4 (BEAST) [160] using the LG + I + G + F substitution model, a lognormal relaxed clock, and Yule process, throughout 10,000,000 generations. The tree is drawn to scale with branch lengths measured in the average number of substitutions per time unit. PV = parvovirus. (Reproduced under Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/ (accessed 21 December 2023)) from [5], Figure 2).