Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 22, Number 12—December 2016
Research

Cutaneous Granulomas in Dolphins Caused by Novel Uncultivated Paracoccidioides brasiliensis

Raquel Vilela, Gregory D. Bossart, Judy A. St. Leger, Leslie M. Dalton, John S. Reif, Adam M. Schaefer, Peter J. McCarthy, Patricia A. Fair, and Leonel MendozaComments to Author 
Author affiliations: Federal University of Minas Gerais, Belo Horizonte, Brazil (R. Vilela); Michigan State University, East Lansing, Michigan, USA (R. Vilela, L. Mendoza); Georgia Aquarium, Atlanta, Georgia, USA (G.D. Bossart); University of Miami Miller School of Medicine, Miami, Florida, USA (G.D. Bossart); SeaWorld, San Diego, California, USA (J.A. St. Leger); SeaWorld, San Antonio, Texas, USA (L.M. Dalton); Colorado State University College of Veterinary Medicine and Biomedical Sciences, Fort Collins, Colorado, USA (J.S. Reif); Florida Atlantic University, Fort Pierce, Florida, USA (A.M. Schaefer, P.J. McCarthy); National Oceanic and Atmospheric Administration, Charleston, South Carolina, USA (P.A. Fair)

Main Article

Figure 4

Unrooted maximum-parsimony phylogenetic trees of A) partial internal transcribed spacer (ITS), B) 2 partial glycoprotein 43 (gp43) (12–14), and C) 2 partial chitin synthase 4 (CHS4) (A. Schaefer, P.J. McCarthy, unpub. data) gene sequences of Paracoccidioides brasiliensis. Sequences were obtained pathogen-infected bottlenose dolphins, Indian River Lagoon, Florida, USA, and compared with homologous sequences of cultivated Paracoccidioides brasiliensis (Pb), P. lutzii (Pi), and uncultivated Lacazia

Figure 4. Unrooted maximum-parsimony phylogenetic trees of A) partial internal transcribed spacer (ITS), B) 2 partial glycoprotein 43 (gp43) (1214), and C) 2 partial chitin synthase 4 (CHS4) (A. Schaefer, P.J. McCarthy, unpub. data) gene sequences of Paracoccidioides brasiliensis. Sequences were obtained pathogen-infected bottlenose dolphins, Indian River Lagoon, Florida, USA, and compared with homologous sequences of cultivated Paracoccidioides brasiliensis (Pb), P. lutzii (Pi), and uncultivated Lacazia loboi (Ll) available in GenBank. Ajellomyeces capsulatus and A. dermatitidis CHS4, gp43, and ITS homologous sequences were used as outgroups. Strain names or accession numbers are shown. Numbers along branches are bootstrap values for 1,000 resamplings obtained by parsimony analysis, which support different clusters. P. brasiliensis ITS sequences from dolphins (14) grouped among cultivated P. brasiliensis ITS sequences. Distance between uncultivated P. brasiliensis from dolphins and cultivated P. brasiliensis from humans is unusually large (box in panel A). Placement of 2 gp43 P. brasiliensis sequences from dolphins (12,13) among cultivated P. brasiliensis strains (boxes in panel B). P. brasiliensis partial CHS4 gene sequences from 2 dolphins placed these sequences (GenBank accession no. KX267767 [A3] and KX267768 [90A]) within the P. brasiliensis cluster (box in panel C). Scale bars indicate nucleotide substitutions per site.

Main Article

References
  1. Bossart  GD. Suspected acquired immunodeficiency in an Atlantic bottlenosed dolphin with chronic-active hepatitis and lobomycosis. J Am Vet Med Assoc. 1984;185:14134.PubMedGoogle Scholar
  2. Bossart  GD, Schaefer  AM, McCulloch  S, Goldstein  J, Fair  PA, Reif  JS. Mucocutaneous lesions in free-ranging Atlantic bottlenose dolphins Tursiops truncatus from the southeastern USA. Dis Aquat Organ. 2015;115:17584.DOIPubMedGoogle Scholar
  3. deVries  GA, Laarman  JJ. A case of Lobo’s disease in the dolphin Sotalia guianesis. Journal of Aquatic Mammals. 1973;1:2633.
  4. da Lacaz  S, Baruzzi  RG, Rosa  CB. Lobo’s disease [in Portuguese]. São Paulo: Editora da Universidad de IPSIS Gráfica e Editora; 1986.
  5. Migaki  G, Valerio  MG, Irvine  B, Garner  FM. Lobo’s disease in an atlantic bottle-nosed dolphin. J Am Vet Med Assoc. 1971;159:57882.PubMedGoogle Scholar
  6. Woodard  JC. Electron microscopic study of lobomycosis (Loboa loboi). Lab Invest. 1972;27:60612.PubMedGoogle Scholar
  7. Schaefer  AM, Reif  JS, Guzmán  EA, Bossart  GD, Ottuso  P, Snyder  J, et al. Toward the identification, characterization and experimental culture of Lacazia loboi from Atlantic bottlenose dolphin (Tursiops truncatus). Med Mycol. 2016;54:65965.DOIPubMedGoogle Scholar
  8. Silva  ME, Kaplan  W, Miranda  JL. Antigenic relationships between Paracoccidioides loboi and other pathogenic fungi determined by immunofluorescence. Mycopathol Mycol Appl. 1968;36:97106.DOIPubMedGoogle Scholar
  9. Taborda  PR, Taborda  VA, McGinnis  MR. Lacazia loboi gen. nov., comb. nov., the etiologic agent of lobomycosis. J Clin Microbiol. 1999;37:20313.PubMedGoogle Scholar
  10. Herr  RA, Tarcha  EJ, Taborda  PR, Taylor  JW, Ajello  L, Mendoza  L. Phylogenetic analysis of Lacazia loboi places this previously uncharacterized pathogen within the dimorphic Onygenales. J Clin Microbiol. 2001;39:30914.DOIPubMedGoogle Scholar
  11. Vilela  R, Mendoza  L, Rosa  PS, Belone  AF, Madeira  S, Opromolla  DV, et al. Molecular model for studying the uncultivated fungal pathogen Lacazia loboi. J Clin Microbiol. 2005;43:365761.DOIPubMedGoogle Scholar
  12. Vilela  R, Rosa  PS, Belone  AFF, Taylor  JW, Diório  SM, Mendoza  L. Molecular phylogeny of animal pathogen Lacazia loboi inferred from rDNA and DNA coding sequences. Mycol Res. 2009;113:8517.DOIPubMedGoogle Scholar
  13. Rotstein  DS, Burdett  LG, McLellan  W, Schwacke  L, Rowles  T, Terio  KA, et al. Lobomycosis in offshore bottlenose dolphins (Tursiops truncatus), North Carolina. Emerg Infect Dis. 2009;15:58890.DOIPubMedGoogle Scholar
  14. Minakawa  T, Ueda  K, Tanaka  M, Tanaka  N, Kuwamura  M, Izawa  T, et al. Detection of multiple budding yeast cells and a partial sequence of 43-kDa glycoprotein coding gene of Paracoccidioides brasiliensis from a case of lacaziosis in a female Pacific white-sided dolphin (Lagenorhynchus obliquidens). Mycopathologia. 2016;181:5239.DOIPubMedGoogle Scholar
  15. Ueda  K, Sano  A, Yamate  J, Nakagawa  EI, Kuwamura  M, Izawa  T, et al. Two cases of lacaziosis in bottlenose dolphins (Tursiops truncates) in Japan. Case Reports in Veterinary Medicines. 2013;2013 [cited 2016 Sep 2]. https://www.hindawi.com/journals/crivem/2013/318548/
  16. Esperón  F, García-Párraga  D, Bellière  EN, Sánchez-Vizcaíno  JM. Molecular diagnosis of lobomycosis-like disease in a bottlenose dolphin in captivity. Med Mycol. 2012;50:1069.DOIPubMedGoogle Scholar
  17. Thompson  JD, Higgins  DG, Gibson  TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22:467380.DOIPubMedGoogle Scholar
  18. Tamura  K, Peterson  D, Peterson  N, Stecher  G, Nei  M, Kumar  S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28:27319.DOIPubMedGoogle Scholar
  19. Reif  JS, Mazzoil  M, McCulloch  SD, Varela  RA, Goldstein  JD, Fair  PA, et al. Lobomycosis in Atlantic bottlenose dolphins (Tursiops truncatus) from the Indian River Lagoon, Florida. J Am Vet Med Assoc. 2006;228:1048.DOIPubMedGoogle Scholar
  20. Haubold  EM, Cooper  CR Jr, Wen  JW, McGinnis  MR, Cowan  DF. Comparative morphology of Lacazia loboi (syn. Loboa loboi) in dolphins and humans. Med Mycol. 2000;38:914.DOIPubMedGoogle Scholar
  21. Mendoza  L, Belone  AFF, Vilela  R, Rehtanz  M, Bossart  GD, Reif  JS, et al. Use of sera from humans and dolphins with lacaziosis and sera from experimentally infected mice for Western Blot analyses of Lacazia loboi antigens. Clin Vaccine Immunol. 2008;15:1647.DOIPubMedGoogle Scholar
  22. Symmers  WS. A possible case of Lôbo’s disease acquired in Europe from a bottle-nosed dolphin (Tursiops truncatus). Bull Soc Pathol Exot Filiales. 1983;76:77784.PubMedGoogle Scholar
  23. Kiszka  J, Van Bressem  M-F, Pusineri  C. Lobomycosis-like disease and other skin conditions in Indo-Pacific bottlenose dolphins Tursiops aduncus from the Indian Ocean. Dis Aquat Organ. 2009;84:1517.DOIPubMedGoogle Scholar
  24. Paniz-Mondolfi  A, Talhari  C, Sander Hoffmann  L, Connor  DL, Talhari  S, Bermudez-Villapol  L, et al. Lobomycosis: an emerging disease in humans and delphinidae. Mycoses. 2012;55:298309.DOIPubMedGoogle Scholar

Main Article

Page created: November 29, 2016
Page updated: November 29, 2016
Page reviewed: November 29, 2016
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
file_external