Identification and phylogenetic analysis of Dirofilaria ursi (Nematoda: Filarioidea) from Wisconsin black bears (Ursus americanus) and its wolbachia endosymbiont

Journal of Parasitology

Volumn 96, Issue 2, 2010, Pages 412-419

  Michalski, Michelle L ^a   Bain, Odile ^a,b   Fischer, Kerstin ^a,c   Fischer, Peter U ^a,c   Kumar, Sanjay ^a,d   Foster, Jeremy M ^a,d  

^a UNIVERSITY OF WISCONSIN OSHKOSH   (United States)

^b MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Molecular Parasitology Division   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM; BEAR; BLOOD; ENDOSYMBIONT; HUNTING; IDENTIFICATION KEY; IMMUNOASSAY; MORPHOLOGY; NEMATODE; PHYLOGENETICS; PHYLOGENY;

ANIMAL TISSUE; ARTICLE; BEAR; DIROFILARIA; DIROFILARIA URSI; DNA SEQUENCE; ENDOSYMBIONT; HOST PARASITE INTERACTION; MICROFILARIASIS; MOLECULAR PHYLOGENY; MORPHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE IDENTIFICATION; PARASITE PREVALENCE; WOLBACHIA;

ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; DIROFILARIA; DIROFILARIASIS; DNA, BACTERIAL; DNA, HELMINTH; DNA, RIBOSOMAL; DOGS; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMERASE CHAIN REACTION; PREVALENCE; RNA, RIBOSOMAL, 5S; SEQUENCE ALIGNMENT; SYMBIOSIS; URSIDAE; WISCONSIN; WOLBACHIA;

UNITED STATES; WISCONSIN;

BACTERIA (MICROORGANISMS); DIROFILARIA; DIROFILARIA IMMITIS; DIROFILARIA REPENS; FILARIOIDEA; NEMATODA; ONCHOCERCA; SIMULIIDAE; URSUS AMERICANUS; WOLBACHIA;

EID: 77953597017     PISSN: 00223395     EISSN: None     Source Type: Journal    
DOI: 10.1645/GE-2208.1     Document Type: Article

References (47)

1. ADDISON, E. M. 1980. Transmission of Dirofilaria ursi Yamaguti, 1941. (Nematoda:Onchocercidae) of black bear (Ursus americanus) by blackflies (Simuliidae). Canadian Journal of Zoology 58: 1913-1922.
2. -, AND M. J. PYBUS. 1978. Helminth and arthropod parasites of black bear, Ursus americanus, in central Ontario. Canadian Journal of Zoology 56: 2122-2126.
3. ALTSCHUL, S. F., W. GISH, W. MILLER, E. W. MYERS, AND D. J. LIPMAN. 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403-410.
4. ANDERSON, R. C. 1952. Description and relationships of Dirofilaria ursi Yamaguti, 1941, and a review of the genus Dirofilaria Railliet and Henry, 1911. Transactions of the Royal Canadian Institute 29: 35-65.
5. -, AND O. BAIN. 1976. Keys to genera of the order Spirurida. Part 3. Diplotriaenoidea, Aproctoidea, and Filarioidea. In CIH keys to the nematode parasites of vertebrates, R. C. Anderson, A. G. Chabaud, and S. Willmott (eds.). CABI, Farnham Royal, U.K., p. 59-116.
6. BAIN, O., AND S. BABAYAN. 2003. Behavior of filariae: Morphological and anatomical signatures of their life style within the arthropod and vertebrate hosts. Filaria Journal 2: 16.
7. -, AND A. G. CHABAUD. 1988. Un appareil favorisant l'accouplement des Filaires: Les renflements de la region anterieure du corps. Annales de Parasitologie Humaine & Comparee 63: 376-379.
8. BALDO, L., S. BORDENSTEIN, J. J. WERNEGREEN, AND J. H. WERREN. 2006. Widespread recombination throughout Wolbachia genomes. Molecular Biology and Evolution 23: 437-449.
9. -, J. C. DUNNING HOTOP, K. A. JOLLEY, S. R. BORDENSTEIN, S. A. BIBER, R. R. CHOUDHURY, C. HAYASHI, M. C. MAIDEN, H. TETTELIN, AND J. H. WERREN. 2006. Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Applied Environmental Microbiology 72: 7098-7110.
10. -, AND J. H. WERREN. 2007. Revisiting Wolbachia supergroup typing based on WSP: spurious lineages and discordance with MLST. Current Microbiology 55: 81-87.
11. BANDI, C., J. W. MCCALL, C. GENCHI, S. CORONA, L. VENCO, AND L. SACCHI. 1999. Effects of tetracycline on the filarial worms Brugia pahangi and Dirofilaria immitis and their bacterial endosymbionts Wolbachia. International Journal for Parasitology 29: 357-364.
12. BAZZOCCHI, C., W. JAMNONGLUK, S. L. O'NEILL, T. J. ANDERSON, C. GENCHI, AND C. BANDI. 2000. wsp Gene sequences from the Wolbachia of filarial nematodes. Current Microbiology 41: 96-100.
13. -, M. MORTARINO, G.GRANDI, L.H.KRAMER, C.GENCHI, C. BANDI, M. GENCHI, L. SACCHI, AND J. W. MCCALL. 2008. Combined ivermectin and doxycycline treatment has microfilaricidal and adulticidal activity against Dirofilaria immitis in experimentally infected dogs. International Journal for Parasitology 38: 1401-1410.
14. BORDENSTEIN, S. R., C. PARASKEVOPOULOS, J. C.HOTOPP, P. SAPOUNTZIS, N. LO, C. BANDI, H. TETTELIN, J. H. WERREN, AND K. BOURTZIS. 2009. Parasitism and mutualism in Wolbachia: What the phylogenomic trees can and cannot say. Molecular Biology and Evolution 26: 231-241.
15. BUTTNER, D. W., S. WANJI, C. BAZZOCCHI, O. BAIN, AND P. FISCHER. 2003. Obligatory symbiotic Wolbachia endobacteria are absent from Loa loa. Filaria Journal 2: 10.
16. CANESTRI TROTTI, G., S. PAMPIGLIONE, AND F. RIVASI. 1997. The species of the genus Dirofilaria, Railliet & Henry, 1911. Parassitologia 39: 369-374.
17. CASIRAGHI, M., O. BAIN, R. GUERRERO, C. MARTIN, V. POCACQUA, S. GARDNER, A. FRANCESCHI, AND C. BANDI. 2004. Mapping the presence of Wolbachia pipientis on the phylogeny of filarial nematodes: Evidence for symbiont loss over evolution. Parasitology 34: 191-203.
18. -, S. R. BORDENSTEIN, L. BALDO, N. LO, T. BENINATI, J. J. WERNEGREEN, J. H. WERREN, AND C. BANDI. 2005. Phylogeny of Wolbachia pipientis based on gltA, groEL and ftsZ gene sequences: Clustering of arthropod and nematode symbionts in the F supergroup, and evidence for further diversity in the Wolbachia tree. Microbiology 151: 4015-4022.
19. CRUM, J. M., V. F. NETTLES, AND W. R. DAVIDSON. 1978. Studies on endoparasites of the black bear (Ursus americanus) in the southeastern United States. Journal of Wildlife Disease 14: 178-186.
20. DIES, K. H. 1979. Helminths recovered from black bears in the Peace River region of Northwestern Alberta. Journal of Wildlife Disease 15: 49-50.
21. DUFFY, M. S., T. A. GREAVES, AND M. D. B. BURT. 1994. Helminths of the black bear, Ursus americanus, in New Brunswick. Journal of Parasitology 80: 478-480.
22. EDGAR, R. C. 2004. MUSCLE: A multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
23. FELSENSTEIN, J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783-791.
24. FENN, K., C. CONLON, M. JONES, M. A. QUAIL, N. E. HOLROYD, J. PARKHILL, AND M. BLAXTER. 2006. Phylogenetic relationships of the Wolbachia of nematodes and arthropods. PLoS Pathogens 2: e94.
25. FRECHETTE, J. L., AND M. E. RAU. 1977. Helminths of the black bear in Quebec. Journal of Wildlife Disease 13: 432-434.
26. -, AND -. 1978. Seasonal changes in the prevalence of ova of Diphyllobothrium ursi and Baylisascaris transfuga in the feces of the black bear (Ursus americanus). Journal of Wildlife Disease 14: 342-345.
27. HUANG, H., T.WANG, G.YANG, Z. ZHANG, C. WANG, Z.YANG, L. LUO, L. LIU, J. LAN, AND X. HUANG. 2009. Molecular characterization and phylogenetic analysis of Dirofilaria immitis of China based on COI and 12S rDNA genes. Veterinary Parasitology 160: 175-179.
28. JEYAPRAKASH, A., AND M. A. HOY. 2000. Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Molecular Biology 9: 393-405.
29. KIMURA, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16: 111-120.
30. KRAMER, L. H., B. PASSERI, S. CORONA, L. SIMONCINI, AND M. CASIRAGHI. 2003. Immunohistochemical/immunogold detection and distribution of the endosymbiont Wolbachia of Dirofilaria immitis and Brugia pahangi using a polyclonal antiserum raised against WSP (Wolbachia surface protein). Parasitology Research 89: 381-386.
31. MANVILLE, A. M. 1978. Ecto- and endoparasites of the black bear in northern Wisconsin. Journal of Wildlife Disease 14: 97-100.
32. MCCALL, J. W., C. GENCHI, L. H. KRAMER, J. GUERRERO, AND L. VENCO. 2008. Heartworm disease in animals and humans. Advances in Parasitology 66: 193-285.
33. NEI, M., AND S. KUMAR. 2000. Molecular evolution and phylogenetics. Oxford University Press, New York, New York, 348 p.
34. PENCE, D. B., J. M. CRUM, AND J. A. CONTI. 1983. Ecological analyses of helminth populations in the black bear, Ursus americanus, from North America. Journal of Parasitology 69: 933-950.
35. PUNKOSDY, G. A., D. G. ADDISS, AND P. J. LAMMIE. 2003. Characterization of antibody responses to Wolbachia surface protein in humans with lymphatic filariasis. Infection and Immunity 71: 5104-5114.
36. RZHETSKY, A., AND M. NEI. 1992. A simple method for estimating and testing minimum evolution trees. Molecular Biology and Evolution 9: 945-967.
37. ROGERS, L. L. 1975. Parasites of black bears of the Lake Superior region. Journal of Wildlife Disease 11: 189-192.
38. SAMBROOK, J., AND D. RUSSELL. 2001. Molecular cloning: A laboratory manual, 3rd ed. Cold Spring Harbor Press, Cold Spring Harbor, New York, 2,344 p.
39. TAMURA, K., J. DUdLEY, M. NEI, AND S. KUMAR. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596-1599.
40. TAYLOR, M. J., C. BANDI, AND A. HOERAUF. 2005. Wolbachia bacterial endosymbionts of filarial nematodes. Advances in Parasitology 60: 245-284.
41. UNI, S. 1983. Filarial parasites from the black bear of Japan. Annales de Parasitologie Humaine et Comparee 58: 71-84.
42. -, AND S. TAKADA. 1986. The longitudinal cuticular markings of Dirofilaria immitis adult worm. Japanese Journal of Parasitology 35: 191-199.
43. WATERHOUSE, A. M., J. B. PROCTER, D.M. MARTIN, M. CLAMP, AND G. J. BARTON. 2009. Jalview Version 2-A multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191.
44. WONG, M. M., AND M. E. BRUMMER. 1978. Cuticular morphology of five species of Dirofilaria: A scanning electron microscope study. Journal of Parasitology 64: 108-114.
45. XIE, H., O. BAIN, AND S. A. WILLIAMS. 1994. Molecular phylogenetic studies on filarial parasites based on 5s ribosomal spacer sequences. Parasite 1: 141-151.
46. YAMAGUTI, S. 1941. Studies on the helminth fauna of Japan, Part 35. Japan Journal of Zoology 9: 409-439.
47. YOKOHATA, Y., O. FUJITA, M. KAMIYA, T. FUJITA, K. KANEKO, AND M. OHBAYASHI. 1990. Parasites fromthe Asiatic black bear (Ursus thibetanus) on Kyushu Island, Japan. Journal ofWildlife Disease 26: 137-138.