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Volume 30, Number 2—February 2024
Research

Piscichuvirus-Associated Severe Meningoencephalomyelitis in Aquatic Turtles, United States, 2009–2021

Weerapong Laovechprasit, Kelsey T. Young, Brian A. Stacy, Steven B. Tillis, Robert J. Ossiboff, Jordan A. Vann, Kuttichantran Subramaniam, Dalen W. Agnew, Elizabeth W. Howerth, Jian Zhang, Shayna Whitaker, Alicia Walker, Andrew M. Orgill, Lyndsey N. Howell, Donna J. Shaver, Kyle Donnelly, Allen M. Foley, and James B. StantonComments to Author 
Author affiliations: University of Georgia, Athens, Georgia, USA (W. Laovechprasit, K.T. Young, E.W. Howerth, J. Zhang, J.B. Stanton); National Oceanic and Atmospheric Administration, Pascagoula, Mississippi, USA (B.A. Stacy, L.N. Howell); University of Florida, Gainesville, Florida, USA (S.B. Tillis, R.J. Ossiboff, J.A. Vann, K. Subramaniam); Michigan State University, Lansing, Michigan, USA (D.W. Agnew); Amos Rehabilitation Keep at University of Texas Marine Science Institute, Port Aransas, Texas, USA (S. Whitaker, A. Walker, A.M. Orgill); National Park Service at Padre Island National Seashore, Corpus Christi, Texas, USA (D.J. Shaver); Brevard Zoo and Sea Turtle Healing Center, Melbourne, Florida, USA (K. Donnelly); Florida Fish and Wildlife Conservation Commission, Jacksonville, Florida, USA (A.M. Foley)

Main Article

Figure 4

Phylogenetic analysis of jingchuviral large protein (L) amino acid sequences from piscichuvirus-infected aquatic turtles with meningoencephalomyelitis, United States, 2009–2021 (black dots), and reference sequences. Complete L amino acid sequences were aligned by using ClustalW (https://www.clustal.org) and refined by using MUSCLE (https://www.ebi.ac.uk/Tools/msa/muscle) with default settings. The phylogenetic analysis was performed on MEGA X (23) by using the maximum-likelihood method and Le Gascuel matrix plus observed amino acid frequencies plus 5 discrete gamma categories distribution with parameter of 1.0728 plus invariant sites with 0.65% sites. The substitution model was constructed with 500 bootstrap replicates. The tree is drawn to scale; bootstrap values are measured in the number of substitutions per site. This analysis included 59 aa sequences. Sequences are color coded based on their genomic structure.

Figure 4. Phylogenetic analysis of jingchuviral large protein (L) amino acid sequences from piscichuvirus-infected aquatic turtles with meningoencephalomyelitis, United States, 2009–2021 (black dots), and reference sequences. Complete L amino acid sequences were aligned by using ClustalW (https://www.clustal.org) and refined by using MUSCLE (https://www.ebi.ac.uk/Tools/msa/muscle) with default settings. The phylogenetic analysis was performed on MEGA X (23) by using the maximum-likelihood method and Le Gascuel matrix plus observed amino acid frequencies plus 5 discrete gamma categories distribution with parameter of 1.0728 plus invariant sites with 0.65% sites. The substitution model was constructed with 500 bootstrap replicates. The tree is drawn to scale; bootstrap values are measured in the number of substitutions per site. This analysis included 59 aa sequences. Sequences are color coded based on their genomic structure.

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References
  1. Senko  JF, Burgher  KM, Del Mar Mancha-Cisneros  M, Godley  BJ, Kinan-Kelly  I, Fox  T, et al. Global patterns of illegal marine turtle exploitation. Glob Change Biol. 2022;28:6509–23. DOIPubMedGoogle Scholar
  2. Rhodin  AGJ, Iverson  JB, Bour  R, Fritz  U, Georges  A, Shaffer  HB, et al.; Turtle Taxonomy Working Group. Turtles of the world: annotated checklist and atlas of taxonomy, synonymy, distribution, and conservation status. In: Rhodin AGJ, Iverson JB, van Dijk PP, Stanford CB, Goode EV, Buhlmann, KA, et al., editors. Conservation Biology of Freshwater Turtles and Tortoises: a Compilation Project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group. 9th ed. Chelonian Research Monographs. Rochester (NY): Mercury Print Productions. 2021;8:1–472.
  3. Greenblatt  RJ, Work  TM, Dutton  P, Sutton  CA, Spraker  TR, Casey  RN, et al. Geographic variation in marine turtle fibropapillomatosis. J Zoo Wildl Med. 2005;36:527–30. DOIPubMedGoogle Scholar
  4. Waltzek  TB, Stacy  BA, Ossiboff  RJ, Stacy  NI, Fraser  WA, Yan  A, et al. A novel group of negative-sense RNA viruses associated with epizootics in managed and free-ranging freshwater turtles in Florida, USA. PLoS Pathog. 2022;18:e1010258. DOIPubMedGoogle Scholar
  5. Harding  EF, Russo  AG, Yan  GJH, Mercer  LK, White  PA. Revealing the uncharacterised diversity of amphibian and reptile viruses. ISME Commun. 2022;2:95. DOIPubMedGoogle Scholar
  6. Li  CX, Shi  M, Tian  JH, Lin  XD, Kang  YJ, Chen  LJ, et al. Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. eLife. 2015;4:1–26. DOIPubMedGoogle Scholar
  7. Han  X, Wang  H, Wu  N, Liu  W, Cao  M, Wang  X. Leafhopper Psammotettix alienus hosts chuviruses with different genomic structures. Virus Res. 2020;285:197992. DOIPubMedGoogle Scholar
  8. Shi  M, Lin  XD, Tian  JH, Chen  LJ, Chen  X, Li  CX, et al. Redefining the invertebrate RNA virosphere. Nature. 2016;540:539–43. DOIPubMedGoogle Scholar
  9. Shi  M, Lin  XD, Chen  X, Tian  JH, Chen  LJ, Li  K, et al. The evolutionary history of vertebrate RNA viruses. Nature. 2018;556:197–202. DOIPubMedGoogle Scholar
  10. Hahn  MA, Rosario  K, Lucas  P, Dheilly  NM. Characterization of viruses in a tapeworm: phylogenetic position, vertical transmission, and transmission to the parasitized host. ISME J. 2020;14:1755–67. DOIPubMedGoogle Scholar
  11. Dezordi  FZ, Vasconcelos  CRDS, Rezende  AM, Wallau  GL. In and outs of Chuviridae endogenous viral elements: origin of a potentially new retrovirus and signature of ancient and ongoing arms race in mosquito genomes. Front Genet. 2020;11:542437. DOIPubMedGoogle Scholar
  12. Di Paola  N, Dheilly  NM, Junglen  S, Paraskevopoulou  S, Postler  TS, Shi  M, et al. Jingchuvirales: a new taxonomical framework for a rapidly expanding order of unusual monjiviricete viruses broadly distributed among arthropod subphyla. Appl Environ Microbiol. 2022;88:e0195421. DOIPubMedGoogle Scholar
  13. Argenta  FF, Hepojoki  J, Smura  T, Szirovicza  L, Hammerschmitt  ME, Driemeier  D, et al. Identification of reptarenaviruses, hartmaniviruses and a novel chuvirus in captive Brazilian native boa constrictors with boid inclusion body disease. J Virol. 2020;94:1–19. DOIPubMedGoogle Scholar
  14. Conceição-Neto  N, Yinda  KC, Van Ranst  M, Matthijnssens  J. NetoVIR: modular approach to customize sample preparation procedures for viral metagenomics. In: Moya A, Pérez Brocal V, editors. The Human Virome In Molecular Biology. Totowa (NJ): Humana Press Inc.; 2018. p. 85–95.
  15. Vibin  J, Chamings  A, Collier  F, Klaassen  M, Nelson  TM, Alexandersen  S. Metagenomics detection and characterisation of viruses in faecal samples from Australian wild birds. Sci Rep. 2018;8:8686. DOIPubMedGoogle Scholar
  16. Young  KT, Stephens  JQ, Poulson  RL, Stallknecht  DE, Dimitrov  KM, Butt  SL, et al. Putative novel avian paramyxovirus (AMPV) and reidentification of APMV-2 and APMV-6 to the species level based on wild bird surveillance (United States, 2016–2018). Appl Environ Microbiol. 2022;88:e0046622. DOIPubMedGoogle Scholar
  17. Young  KT, Lahmers  KK, Sellers  HS, Stallknecht  DE, Poulson  RL, Saliki  JT, et al. Randomly primed, strand-switching, MinION-based sequencing for the detection and characterization of cultured RNA viruses. J Vet Diagn Invest. 2021;33:202–15. DOIPubMedGoogle Scholar
  18. Kim  D, Song  L, Breitwieser  FP, Salzberg  SL. Centrifuge: rapid and sensitive classification of metagenomic sequences. Genome Res. 2016;26:1721–9. DOIPubMedGoogle Scholar
  19. Kolmogorov  M, Yuan  J, Lin  Y, Pevzner  PA. Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol. 2019;37:540–6. DOIPubMedGoogle Scholar
  20. Wood  DE, Lu  J, Langmead  B. Improved metagenomic analysis with Kraken 2. Genome Biol. 2019;20:257. DOIPubMedGoogle Scholar
  21. Bankevich  A, Nurk  S, Antipov  D, Gurevich  AA, Dvorkin  M, Kulikov  AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:455–77. DOIPubMedGoogle Scholar
  22. Hofacker  IL. Vienna RNA secondary structure server. Nucleic Acids Res. 2003;31:3429–31. DOIPubMedGoogle Scholar
  23. Kumar  S, Stecher  G, Li  M, Knyaz  C, Tamura  K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol. 2018;35:1547–9. DOIPubMedGoogle Scholar
  24. VanDevanter  DR, Warrener  P, Bennett  L, Schultz  ER, Coulter  S, Garber  RL, et al. Detection and analysis of diverse herpesviral species by consensus primer PCR. J Clin Microbiol. 1996;34:1666–71. DOIPubMedGoogle Scholar
  25. Byles  RA. Behavior and ecology of sea turtles from Chesapeake Bay, Behavior and ecology of sea turtles from Chesapeake Bay, Virginia [dissertation]. Williamsburg (VA): College of William and Mary; 1988.
  26. Jackson  GJ Jr, Ross  A. The occurrence of barnacles on the alligator snapping turtle, Macrochelys temminckii (Troost). J Herpetol. 1971;5:188–9. DOIGoogle Scholar
  27. Obijeski  JF, McCauley  J, Skehel  JJ. Nucleotide sequences at the terminal of La Crosse virus RNAs. Nucleic Acids Res. 1980;8:2431–8. DOIPubMedGoogle Scholar
  28. Hsu  MT, Parvin  JD, Gupta  S, Krystal  M, Palese  P. Genomic RNAs of influenza viruses are held in a circular conformation in virions and in infected cells by a terminal panhandle. Proc Natl Acad Sci U S A. 1987;84:8140–4. DOIPubMedGoogle Scholar
  29. Auperin  DD, Romanowski  V, Galinski  M, Bishop  DH. Sequencing studies of pichinde arenavirus S RNA indicate a novel coding strategy, an ambisense viral S RNA. J Virol. 1984;52:897–904. DOIPubMedGoogle Scholar
  30. Fodor  E, Pritlove  DC, Brownlee  GG. The influenza virus panhandle is involved in the initiation of transcription. J Virol. 1994;68:4092–6. DOIPubMedGoogle Scholar
  31. Neumann  G, Hobom  G. Mutational analysis of influenza virus promoter elements in vivo. J Gen Virol. 1995;76:1709–17. DOIPubMedGoogle Scholar
  32. Flick  R, Neumann  G, Hoffmann  E, Neumeier  E, Hobom  G. Promoter elements in the influenza vRNA terminal structure. RNA. 1996;2:1046–57.PubMedGoogle Scholar
  33. Keatts  LO, Robards  M, Olson  SH, Hueffer  K, Insley  SJ, Joly  DO, et al. Implications of zoonoses from hunting and use of wildlife in North American arctic and boreal biomes: pandemic potential, monitoring, and mitigation. Front Public Health. 2021;9:627654. DOIPubMedGoogle Scholar
  34. Fredricks  DN, Relman  DA. Sequence-based identification of microbial pathogens: a reconsideration of Koch’s postulates. Clin Microbiol Rev. 1996;9:18–33. DOIPubMedGoogle Scholar
  35. Heppell  SS. Application of life-history theory and population model analysis to turtle conservation. Copeia. 1998;1998:367–75. DOIGoogle Scholar
  36. Thomas  TM, Granatosky  MC, Bourque  JR, Krysko  KL, Moler  PE, Gamble  T, et al. Taxonomic assessment of Alligator Snapping Turtles (Chelydridae: Macrochelys), with the description of two new species from the southeastern United States. Zootaxa. 2014;3786:141–65. DOIPubMedGoogle Scholar
  37. Folt  B, Guyer  C. Evaluating recent taxonomic changes for alligator snapping turtles (Testudines: Chelydridae). Zootaxa. 2015;3947:447–50. DOIPubMedGoogle Scholar

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Page created: December 21, 2023
Page updated: January 24, 2024
Page reviewed: January 24, 2024
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