The mitochondrial genome and a 60-kb nuclear DNA segment from naegleria fowleri, the causative agent of primary amoebic meningoencephalitis

Journal of Eukaryotic Microbiology

Volumn 60, Issue 2, 2013, Pages 179-191

  Herman, Emily K ^a   Greninger, Alexander L ^b   Visvesvara, Govinda S ^c   Marciano Cabral, Francine ^d   Dacks, Joel B ^a   Chiu, Charles Y ^b,e  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

^d VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

amoebic infections; amoebic mitochondrial genome; deep sequencing; encephalitis; genomics; infectious disease; meningitis; PAM; whole genome sequencing

Indexed keywords

PROTOZOAL DNA; PROTOZOAL PROTEIN;

ENCEPHALITIS; GENETIC ANALYSIS; GENOME; INFECTIOUS DISEASE; MENINGITIS; MITOCHONDRION; PATHOGENICITY; PROTOZOAN;

AMEBIASIS; ARTICLE; AUSTRALIA; CENTRAL NERVOUS SYSTEM INFECTION; CHEMISTRY; DNA SEQUENCE; GENE ORDER; GENETICS; HORIZONTAL GENE TRANSFER; ISOLATION AND PURIFICATION; MITOCHONDRIAL GENOME; MOLECULAR GENETICS; NAEGLERIA FOWLERI; NUCLEOTIDE SEQUENCE; PARASITOLOGY; PRIMARY AMEBIC MENINGOENCEPHALITIS; SEQUENCE HOMOLOGY; SYNTENY; UNITED STATES;

AMEBIASIS; AUSTRALIA; CENTRAL NERVOUS SYSTEM PROTOZOAL INFECTIONS; DNA, PROTOZOAN; GENE ORDER; GENE TRANSFER, HORIZONTAL; GENOME, MITOCHONDRIAL; MOLECULAR SEQUENCE DATA; NAEGLERIA FOWLERI; PROTOZOAN PROTEINS; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY; SYNTENY; UNITED STATES;

AUSTRALIA; UNITED STATES;

AMOEBA (GENUS); EUKARYOTA; NAEGLERIA FOWLERI; NAEGLERIA GRUBERI; PROTISTA;

EID: 84874727558     PISSN: 10665234     EISSN: 15507408     Source Type: Journal    
DOI: 10.1111/jeu.12022     Document Type: Article

References (64)

1. Abascal, F., Zardoya, R., &, Posada, D., 2005. ProtTest: selection of best-fit models of protein evolution. Bioinformatics, 21: 2104-2105.
2. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., &, Lipman, D. J., 1990. Basic local alignment search tool. J. Mol. Biol., 215: 403-410.
3. Baverstock, P. R., Illana, S., Christy, P. E., Robinson, B. S., &, Johnson, A. M., 1989. srRNA evolution and phylogenetic relationships of the genus Naegleria (Protista: Rhizopoda). Mol. Biol. Evol., 6: 243-257.
4. Burger, G., Gray, M. W., &, Franz Lang, B., 2003. Mitochondrial genomes: anything goes. Trends Genet., 19: 709-716.
5. Caffrey, C. R., &, Steverding, D., 2009. Kinetoplastid papain-like cysteine peptidases. Mol. Biochem. Parasitol., 167: 12-19.
6. Carter, R., 1972. Primary amoebic meningo-encephalitis. An appraisal of present knowledge. Trans. R. Soc. Trop. Med. Hyg., 66: 193-213.
7. Cermakian, N., Ikeda, T. M., Cedergren, R., &, Gray, M. W., 1996. Sequences homologous to yeast mitochondrial and bacteriophage T3 and T7 RNA polymerases are widespread throughout the eukaryotic lineage. Nucleic Acids Res., 24: 648-654.
8. da Rocha-Azevedo, B., Tanowitz, H. B., &, Marciano-Cabral, F., 2009. Diagnosis of infections caused by pathogenic free-living amoebae. Interdiscip. Perspect. Infect. Dis., 2009: 1-14.
9. Dacks, J. B., Walker, G., &, Field, M. C., 2008a. Implications of the new eukaryotic systematics for parasitologists. Parasitol. Int., 57: 97-104.
10. Dacks, J. B., Kuru, T., Liapounova, N. A., &, Gedamu, L., 2008b. Phylogenetic and primary sequence characterization of cathepsin B cysteine proteases from the oxymonad flagellate Monocercomonoides. J. Eukaryot. Microbiol., 55: 9-17.
11. de Koning, A. P., Brinkman, F. S. L., Jones, S. J. M., &, Keeling, P. J., 2000. Lateral gene transfer and metabolic adaptation in the human parasite Trichomonas vaginalis. Mol. Biol. Evol., 17: 1769-1773.
12. DeBarry, J. D., &, Kissinger, J. C., 2011. Jumbled genomes: missing apicomplexan synteny. Mol. Biol. Evol., 28: 2855-2871.
13. Dou, Z., Carruthers, V. B., Robinson, M. W., &, Dalton, J. P., 2011. Cathepsin proteases in Toxoplasma gondii. Cysteine proteases of pathogenic organisms. Springer US., 712: 49-61.
14. Drummond, A., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Duran, C., Field, M., Heled, J., Kearse, M., Markowitz, S., Moir, R., Stones-Havas, S., Sturrock, S., Thierer, T., &, Wilson, A., 2010. Geneious v5.5. Available at: http://www.geneious.com.
15. DuBois, K., Abodeely, M., Sajid, M., Engel, J., &, McKerrow, J., 2006. Giardia lamblia cysteine proteases. Parasitol. Res., 99: 313-316.
16. Dyrløv Bendtsen, J., Nielsen, H., von Heijne, G., &, Brunak, S., 2004. Improved prediction of signal peptides: signalP 3.0. J. Mol. Biol., 340: 783-795.
17. Edgar, R. C., 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res., 32: 1792-1797.
18. Fast, N. M., Law, J. S., Williams, B. A. P., &, Keeling, P. J., 2003. Bacterial catalase in the microsporidian Nosema locustae: implications for microsporidian metabolism and genome evolution. Eukaryot. Cell, 2: 1069-1075.
19. Fritz-Laylin, L. K., Ginger, M. L., Walsh, C., Dawson, S. C., &, Fulton, C., 2011. The Naegleria genome: a free-living microbial eukaryote lends unique insights into core eukaryotic cell biology. Res. Microbiol., 162: 607-618.
20. Fritz-Laylin, L. K., Prochnik, S. E., Ginger, M. L., Dacks, J. B., Carpenter, M. L., Field, M. C., Kuo, A., Paredez, A., Chapman, J., Pham, J., Shu, S., Neupane, R., Cipriano, M., Mancuso, J., Tu, H., Salamov, A., Lindquist, E., Shapiro, H., Lucas, S., Grigoriev, I. V., Cande, W. Z., Fulton, C., Rokhsar, D. S., &, Dawson, S. C., 2010. The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell, 140: 631-642.
21. Ghedin, E., Bringaud, F., Peterson, J., Myler, P., Berriman, M., Ivens, A., Andersson, B. R., Bontempi, E., Eisen, J., Angiuoli, S., Wanless, D., Von Arx, A., Murphy, L., Lennard, N., Salzberg, S., Adams, M. D., White, O., Hall, N., Stuart, K., Fraser, C. M., &, El-Sayed, N. M. A., 2004. Gene synteny and evolution of genome architecture in trypanosomatids. Mol. Biochem. Parasitol., 134: 183-191.
22. Githens, S. I., &, Karnovsky, M. L., 1973. Phagocytosis by the cellular slime mold Polysphondylium pallidum during growth and development. J. Cell Biol., 58: 536-548.
23. Griffin, J. L., 1972. Temperature tolerance of pathogenic and nonpathogenic free-living amoebas. Science, 178: 869-870.
24. Guindon, S., &, Gascuel, O., 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol., 52: 696-704.
25. Hauth, A. M., Maier, U. G., Lang, B. F., &, Burger, G., 2005. The Rhodomonas salina mitochondrial genome: bacteria-like operons, compact gene arrangement and complex repeat region. Nucleic Acids Res., 33: 4433-4442.
26. Heggie, T. W., 2010. Swimming with death: Naegleria fowleri infections in recreational waters. Travel Med. Infect. Dis., 8: 201-206.
27. Isacchi, A., Bernardi, G., &, Bernardi, G., 1993. Compositional compartmentalization of the nuclear genomes of Trypanosoma brucei and Trypanosoma equiperdum. FEBS Lett., 335: 181-183.
28. Izumiyama, S., Yagita, K., Furushima-Shimogawara, R., Asakura, T., Karasudani, T., &, Endo, T., 2003. Occurrence and distribution of Naegleria species in thermal waters in Japan. J. Eukaryot. Microbiol., 50: 514-515.
29. John, D. T., &, John, R. A., 1994. Enhancement of virulence in Naegleria fowleri by growth in Vero-cell cultures. J. Parasitol., 80: 149-151.
30. Kadlec, V., 1975. The effects of some factors on the growth and morphology of Naegleria sp. and three strains of the genus Acanthamoeba. Folia Parasitol., 22: 317-321.
31. Kemble, S. K., Lynfield, R., DeVries, A. S., Drehner, D. M., Pomputius, W. F., Beach, M. J., Visvesvara, G. S., da Silva, A. J., Hill, V. R., Yoder, J. S., Xiao, L., Smith, K. E., &, Danila, R., 2012. Fatal Naegleria fowleri infection acquired in Minnesota: possible expanded range of a deadly thermophilic organism. Clin. Infect. Dis., 54: 805-809.
32. Kim, J.-H., Yang, A.-H., Sohn, H.-J., Kim, D., Song, K.-J., &, Shin, H.-J., 2009. Immunodominant antigens in Naegleria fowleri; excretory-secretory proteins were potential pathogenic factors. Parasitol. Res., 105: 1675-1681.
33. Kissoon-Singh, V., Mortimer, L., Chadee, K., Robinson, M. W., &, Dalton, J. P., 2011. Entamoeba histolytica cathepsin-like enzymes. Cysteine proteases of pathogenic organisms. Springer US., 712: 62-83.
34. Lagesen, K., Hallin, P., Rødland, E. A., Stærfeldt, H.-H., Rognes, T., &, Ussery, D. W., 2007. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res., 35: 3100-3108.
35. Lang, B. F., Burger, G., O'Kelly, C. J., Cedergren, R., Golding, G. B., Lemieux, C., Sankoff, D., Turmel, M., &, Gray, M. W., 1997. An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature, 387: 493-497.
36. Law, R. H. P., Smooker, P. M., Irving, J. A., Piedrafita, D., Ponting, R., Kennedy, N. J., Whisstock, J. C., Pike, R. N., &, Spithill, T. W., 2003. Cloning and expression of the major secreted cathepsin B-like protein from juvenile Fasciola hepatica and analysis of immunogenicity following liver fluke infection. Infect. Immun., 71: 6921-6932.
37. Lawande, R. V., Abraham, S. N., John, I., &, Egler, L. J., 1979. Recovery of soil amebas from the nasal passages of children during the dusty Harmattan period in Zaria. Am. J. Clin. Pathol., 71: 201-203.
38. Maddison, W. P., &, Maddison, D. R., 1989. Interactive analysis of phylogeny and character evolution using the computer program MacClade. Folia Primatol., 53: 190-202.
39. Marande, W., Lukeš, J., &, Burger, G., 2005. Unique mitochondrial genome structure in diplonemids, the sister group of kinetoplastids. Eukaryot. Cell, 4: 1137-1146.
40. Marchler-Bauer, A., Lu, S., Anderson, J. B., Chitsaz, F., Derbyshire, M. K., DeWeese-Scott, C., Fong, J. H., Geer, L. Y., Geer, R. C., Gonzales, N. R., Gwadz, M., Hurwitz, D. I., Jackson, J. D., Ke, Z., Lanczycki, C. J., Lu, F., Marchler, G. H., Mullokandov, M., Omelchenko, M. V., Robertson, C. L., Song, J. S., Thanki, N., Yamashita, R. A., Zhang, D., Zhang, N., Zheng, C., &, Bryant, S. H., 2010. CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res., 39: D225-D229.
41. Marciano-Cabral, F., &, Cabral, G. A., 2007. The immune response to Naegleria fowleri amebae and pathogenesis of infection. FEMS Immunol. Med. Microbiol., 51: 243-259.
42. Marciano-Cabral, F. M., &, Fulford, D. E., 1986. Cytopathology of pathogenic and nonpathogenic Naegleria species for cultured rat neuroblastoma cells. Appl. Environ. Microbiol., 51: 1133-1137.
43. Martinez, A., &, Visvesvara, G. S., 1997. Free-living, amphizoic and opportunistic amebas. Brain Pathol., 7: 583-598.
44. Matsuzaki, M., Misumi, O., Shin-i, T., Maruyama, S., Takahara, M., Miyagishima, S.-Y., Mori, T., Nishida, K., Yagisawa, F., Nishida, K., Yoshida, Y., Nishimura, Y., Nakao, S., Kobayashi, T., Momoyama, Y., Higashiyama, T., Minoda, A., Sano, M., Nomoto, H., Oishi, K., Hayashi, H., Ohta, F., Nishizaka, S., Haga, S., Miura, S., Morishita, T., Kabeya, Y., Terasawa, K., Suzuki, Y., Ishii, Y., Asakawa, S., Takano, H., Ohta, N., Kuroiwa, H., Tanaka, K., Shimizu, N., Sugano, S., Sato, N., Nozaki, H., Ogasawara, N., Kohara, Y., &, Kuroiwa, T., 2004. Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature, 428: 653-657.
45. Pernin, P., Ataya, A., &, Cariou, M. L., 1992. Genetic structure of natural populations of the free-living amoeba, Naegleria lovaniensis. Evidence for sexual reproduction. Heredity, 68: 173-181.
46. Richards, T. A., Dacks, J. B., Jenkinson, J. M., Thornton, C. R., &, Talbot, N. J., 2006. Evolution of filamentous plant pathogens: gene exchange across eukaryotic kingdoms. Curr. Biol., 16: 1857-1864.
47. Roger, A. J., &, Simpson, A. G. B., 2009. Evolution: revisiting the root of the eukaryotic tree. Curr. Biol., 9: R165-R167.
48. Ronquist, F., &, Huelsenbeck, J. P., 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19: 1572-1574.
49. Salavati, R., Panigrahi, A. K., &, Stuart, K. D., 2001. Mitochondrial ribonuclease P activity of Trypanosoma brucei. Mol. Biochem. Parasitol., 115: 109-117.
50. Schattner, P., Brooks, A. N., &, Lowe, T. M., 2005. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res., 33: W686-W689.
51. Serrano-Luna, J., Cervantes-Sandoval, I., Tsutsumi, V., &, Shibayama, M., 2007. A biochemical comparison of proteases from pathogenic Naegleria fowleri and non-pathogenic Naegleria gruberi. J. Eukaryot. Microbiol., 54: 411-417.
52. Sheehan, K. B., Ferris, M. J., &, Benson, J. M., 2003. Detection of Naegleria sp. in a thermal, acidic stream in Yellowstone National Park. J. Eukaryot. Microbiol., 50: 263-265.
53. Slot, J. C., &, Rokas, A., 2011. Horizontal transfer of a large and highly toxic secondary metabolic gene cluster between Fungi. Curr. Biol., 21: 134-139.
54. Somanna, A., Mundodi, V., &, Gedamu, L., 2002. Functional analysis of cathepsin B-like cysteine proteases from Leishmania donovani complex: evidence for the activation of latent transforming growth factor β. J. Biol. Chem., 277: 25305-25312.
55. Stamatakis, A., 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22: 2688-2690.
56. Valach, M., Farkas, Z., Fricova, D., Kovac, J., Brejova, B., Vinar, T., Pfeiffer, I., Kucsera, J., Tomaska, L., Lang, B. F., &, Nosek, J., 2011. Evolution of linear chromosomes and multipartite genomes in yeast mitochondria. Nucleic Acids Res., 39: 4202-4219.
57. Vargas-Zepeda, J., Gõmez-Alcalá, A. V., Vázquez- Morales, J. A., Licea-Amaya, L., De Jonckheere, J. F., &, Lares-Villa, F., 2005. Successful treatment of Naegleria fowleri meningoencephalitis by using intravenous amphotericin B, fluconazole and rifampicin. Arch. Med. Res., 36: 83-86.
58. Villalobo, E., Moch, C., Fryd-Versavel, G., Fleury-Aubusson, A., &, Morin, L. Ø., 2003. Cysteine proteases and cell differentiation: excystment of the ciliated protist Sterkiella histriomuscorum. Eukaryot. Cell, 2: 1234-1245.
59. Visvesvara, G. S., &, Stehr-Green, J. K., 1990. Epidemiology of free-living ameba infections. J. Eukaryot. Microbiol., 37: 25s-33s.
60. Visvesvara, G. S., Moura, H., &, Schuster, F. L., 2007. Pathogenic and opportunistic free-living amoebae: Acanthamoeba spp., Balamuthia mandrillaris, Naegleria fowleri, and Sappinia diploidea. FEMS Immunol. Med. Microbiol., 50: 1-26.
61. Westenberger, S., Cerqueira, G., El-Sayed, N., Zingales, B., Campbell, D., &, Sturm, N., 2006. Trypanosoma cruzi mitochondrial maxicircles display species- and strain-specific variation and a conserved element in the non-coding region. BMC Genomics, 7: 60.
62. Yoder, J. S., Eddy, B. A., Visvesvara, G. S., Capewell, L., &, Beach, M. J., 2010. The epidemiology of primary amoebic meningoencephalitis in the USA, 1962-2008. Epidemiol. Infect., 138: 968-975.
63. Yoder, J. S., Straif-Bourgeois, S., Roy, S. L., Moore, T. A., Visvesvara, G. S., Ratard, R. C., Hill, V., Wilson, J. D., Linscott, A. J., Crager, R., Kozak, N. A., Sriram, R., Narayanan, J., Mull, B., Kahler, A. M., Schneeberger, C., Da Silva, A. J., &, Beach, M. J., 2012. Primary amebic meningoencephalitis deaths associated with sinus irrigation using contaminated tap water. Clin. Infect. Dis., 55: e79-85. doi: 10.1093/cid/cis626.
64. Zhou, L., Sriram, R., Visvesvara, G. S., &, Xiao, L., 2003. Genetic variations in the internal transcribed spacers and mitochondrial small subunit rRNA gene of Naegleria spp. J. Eukaryot. Microbiol., 50: 522-526.