Sporangiospore size dimorphism is linked to virulence of mucor circinelloides

PLoS Pathogens

Volumn 7, Issue 6, 2011, Pages

  Li, Charles H ^a   Cervantes, Maria ^b   Springer, Deborah J ^a   Boekhout, Teun ^c   Ruiz Vazquez, Rosa M ^b   Torres Martinez, Santiago R ^b   Heitman, Joseph ^a   Lee, Soo Chan ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF MURCIA   (Spain)

^c CBS KNAW FUNGAL BIODIVERSITY CENTRE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

HIGH MOBILITY GROUP A PROTEIN; PHOSPHATE TRANSPORTER; RNA HELICASE;

ARTICLE; ASEXUAL SPORE; FUNGAL SPORE GERMINATION; FUNGAL VIRULENCE; GENE LOCUS; HOST PARASITE INTERACTION; HUMAN; MACROPHAGE; MATING TYPE; MOTH; MUCOR CIRCINELLOIDE; MUCORALES; PHENOTYPIC PLASTICITY; PHYLOGENETIC TREE; SEX DETERMINATION; SEX DIFFERENCE; SPORANGIOSPORE; CELL GROWTH; CELL SIZE; CYTOLOGY; FUNGUS SPORE; GENETICS; INDIVIDUALITY; MUCOR; ORGANELLE SIZE; PATHOGENICITY; PHYLOGENY; PHYSIOLOGY; REPRODUCTION; SCANNING ELECTRON MICROSCOPY; SPORANGIUM; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; VIRULENCE;

FUNGI; LEPIDOPTERA; MUCOR; MUCOR CIRCINELLOIDES; MUCOR CIRCINELLOIDES F. CIRCINELLOIDES; MUCOR CIRCINELLOIDES F. LUSITANICUS; MURINAE;

CELL GROWTH PROCESSES; CELL SIZE; INDIVIDUALITY; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; MUCOR; ORGANELLE SIZE; PHYLOGENY; REPRODUCTION; SPORANGIA; SPORES, FUNGAL; VIRULENCE;

EID: 79959844472     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002086     Document Type: Article

References (73)

1. James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, et al. (2006) Reconstructing the early evolution of fungi using a six-gene phylogeny. Nature 443: 818-822.
2. Lutzoni F, Kauff F, Cox CJ, McLaughlin D, Celio G, et al. (2004) Assembling the fungal tree of life: progress, classification, and evolution of subcellular traits. Am J Bot 91: 1446-1480.
3. Orlowski M, (1991) Mucor dimorphism. Microbiol Mol Biol Rev 55: 234-258.
4. Lübbehüsen TL, Nielsen J, McIntyre M, (2003) Morphology and physiology of the dimorphic fungus Mucor circinelloides (syn. M. racemosus) during anaerobic growth. Mycol Res 107: 223-230.
5. Brown J, (2005) Zygomycosis: An emerging fungal infection. Am J Health Syst Pham 62: 2593-2596.
6. Chayakulkeeree M, Ghannoum M, Perfect J, (2006) Zygomycosis: the re-emerging fungal infection. Eur J Clin Microbiol Infect Dis 25: 215-229.
7. Ribes JA, Vanover-Sams CL, Baker DJ, (2000) Zygomycetes in human disease. Clin Microbiol Rev 13: 236-301.
8. Roden MM, Zaoutis TE, Buchanan WL, Knudsen TA, Sarkisova TA, et al. (2005) Epidemiology and outcome of zygomycosis: a review of 929 reported cases. Clin Infect Dis 41: 634-653.
9. Spellberg B, Edwards J Jr, Ibrahim A, (2005) Novel perspectives on mucormycosis: pathophysiology, presentation, and management. Clin Microbiol Rev 18: 556-569.
10. Kontoyiannis DP, Lionakis MS, Lewis RE, Chamilos G, Healy M, et al. (2005) Zygomycosis in a tertiary-care cancer center in the era of Aspergillus-active antifungal therapy: A case-control observational study of 27 recent cases. J Infect Dis 191: 1350-1360.
11. Marr KA, Carter RA, Crippa F, Wald A, Corey L, (2002) Epidemiology and outcome of mould infections in hematopoietic stem cell transplant Recipients. Clin Infect Dis 34: 909-917.
12. Kontoyiannis DP, Lewis RE, (2006) Invasive zygomycosis: update on pathogenesis, clinical manifestations, and management. Infect Dis Clin North Am 20: 581-607.
13. Ibrahim AS, Gebremariam T, Lin L, Luo G, Husseiny MI, et al. (2010) The high affinity iron permease is a key virulence factor required for Rhizopus oryzae pathogenesis. Mol Microbiol 77: 587-604.
14. Liu M, Spellberg B, Phan QT, Fu Y, Fu Y, et al. (2010) The endothelial cell receptor GRP78 is required for mucormycosis pathogenesis in diabetic mice. J Clin Invest 120: 1914-1924.
15. Kwon-Chung KJ, Bennet JE, (1992) Mucormycosis. Med Mycol Philadelphia Lea & Febiger pp. 524-559.
16. Ibrahim AS, Spellberg B, (2006) Zygomycetes as agents of infectious disease in humans. In: Heitman J, Filler SG, Edwards JE, Mitchell AP, editors. Molecular principles of fungal pathogenesis Washington, DC ASM Press pp. 429-440.
17. Singh N, Aguado JM, Bonatti H, Forrest G, Gupta KL, et al. (2009) Zygomycosis in solid organ transplant recipients: a prospective, matched case-control study to assess risks for disease and outcome. J Infect Dis 200: 1002-1011.
18. Petrikkos GL, (2008) Zygomycosis (Mucormycosis): an emerging or re-emerging disease? Mycol Newsl 1: 31-32.
19. Ibrahim AS, Edwards JE, Bryant R, Spellberg B, (2008) Economic burden of mucormycosis in the United States: can a vaccine be cost-effective? Med Mycol 47: 592-600.
20. Rogers TR, (2008) Treatment of zygomycosis: current and new options. J Antimicrob Chemther 61: i35-40.
21. Wostemeyer J, Schimek C, (2007) Trisporic acid and mating in zygomycetes. In: Heitman J, Kronstad JW, Taylor JW, Casselton LA, editors. Sex in fungi Washington, DC ASM Press.
22. Lee S, Corradi N, Byrnes E, Torres-Martinez S, Dietrich F, et al. (2008) Microsporidia evolved from ancestral sexual fungi. Curr Biol 18: 1675-1679.
23. Idnurm A, Walton FJ, Floyd A, Heitman J, (2008) Identification of the sex genes in an early diverged fungus. Nature 451: 193-196.
24. Gryganskyi AP, Lee SC, Litvintseva AP, Smith ME, Bonito G, et al. (2010) Structure, function, and phylogeny of the mating locus in the Rhizopus oryzae complex. PLoS ONE 5: e15273.
25. Casselton LA, (2008) Fungal sex genes-searching for the ancestors. BioEssays 30: 711-714.
26. Lee SC, Ni M, Li W, Shertz C, Heitman J, (2010) The evolution of sex: a perspective from the fungal kingdom. Microbiol Mol Biol Rev 74: 298-340.
27. Butler G, Rasmussen MD, Lin MF, Santos MAS, Sakthikumar S, et al. (2009) Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459: 657-662.
28. Reedy JL, Floyd AM, Heitman J, (2009) Mechanistic plasticity of sexual reproduction and meiosis in the Candida pathogenic species complex. Curr Biol 19: 891-899.
29. Metin B, Findley K, Heitman J, (2010) The mating type locus (MAT) and sexual reproduction of Cryptococcus heveanensis: insights into the evolution of sex and sex-determining chromosomal regions in fungi. PLoS Genet 6: e1000961.
30. Rodriguez-Carres M, Findley K, Sun S, Dietrich FS, Heitman J, (2010) Morphological and genomic characterization of Filobasidiella depauperata: a homothallic sibling species of the pathogenic Cryptococcus species complex. PLoS ONE 5: e9620.
31. Schipper MAA, (1976) On Mucor circinelloides, Mucor racemosus, and related species. Stud Mycol 12: 1-40.
32. Mylonakis E, Moreno R, El Khoury JB, Idnurm A, Heitman J, et al. (2005) Galleria mellonella as a model system to study Cryptococcus neoformans pathogenesis. Infect Immun 73: 3842-3850.
33. Chamilos G, Lionakis MS, Lewis RE, Kontoyiannis DP, (2007) Role of mini-host models in the study of medically important fungi. Lancet Infec Dis 7: 42-55.
34. Nicolas FE, de Haro JP, Torres-Martinez S, Ruiz-Vazquez RM, (2007) Mutants defective in a Mucor circinelloides dicer-like gene are not compromised in siRNA silencing but display developmental defects. Fungal Genet Biol 44: 504-516.
35. Idnurm A, James TY, Vilgalys R, (2007) Sex in the rest: mysterious mating in the Chytridiomycota and Zygomycota. In: Heitman J, Kronstad JW, Taylor JW, Casselton LA, editors. Sex in fungi Washington, DC ASM Press.
36. Blakeslee AF, (1904) Sexual reproduction in the Mucorineae. Proc Am Acad Arts Sci 40: 205-319.
37. Orejas M, Peláez MI, Alvarez MI, Eslava AP, (1987) A genetic map of Phycomyces blakesleeanus. Mol Gen Genet 210: 69-76.
38. Michailides TJ, Spotts RA, (1990) Postharvest diseases of pome and stone fruits caused by Mucor piriformis in the Pacific Northwest and California. Plant Dis 74: 537-543.
39. Gauger W, (1975) Further studies on sexuality in azygosporic strains of Mucor hiemalis. Trans Brit Mycol Soc 64: 113-118.
40. Gauger W, (1966) Sexuality of an azygosporic strain of Mucor hiemalis. I. Breakdown of the azygosporic component. Am J Bot 53: 751-755.
41. Fraser JA, Stajich JE, Tarcha EJ, Cole GT, Inglis DO, et al. (2007) Evolution of the mating type locus: insights gained from the dimorphic primary fungal pathogens Histoplasma capsulatum, Coccidioides immitis, and Coccidioides posadasii. Eukaryot Cell 6: 622-629.
42. Li W, Metin B, White TC, Heitman J, (2010) Organization and evolutionary trajectory of the mating type (MAT) locus in the dermatophyte and dimorphic fungal pathogens. Eukaryot Cell 9: 46-58.
43. Heitman J, (2006) Sexual reproduction and the evolution of microbial pathogens. Curr Biol 16: R711-R725.
44. Fan W, Kraus PR, Boily M-J, Heitman J, (2005) Cryptococcus neoformans gene expression during murine macrophage infection. Eukaryot Cell 4: 1420-1433.
45. Nielsen K, Cox GM, Litvintseva AP, Mylonakis E, Malliaris SD, et al. (2005) Cryptococcus neoformans α strains preferentially disseminate to the central nervous system during coinfection. Infect Immun 73: 4922-4933.
46. Kwon-Chung KJ, Edman JC, Wickes BL, (1992) Genetic association of mating types and virulence in Cryptococcus neoformans. Infect Immun 60: 602-605.
47. Nielsen K, Marra RE, Hagen F, Boekhout T, Mitchell TG, et al. (2005) Interaction between genetic background and the mating-type locus in Cryptococcus neoformans virulence potential. Genetics 171: 975-983.
48. Lin X, Huang JC, Mitchell TG, Heitman J, (2006) Virulence attributes and hyphal growth of C. neoformans are quantitative traits and the MATalpha allele enhances filamentation. PLoS Genet 2: e187.
49. Ibrahim AS, Spellberg B, Avanessian V, Fu Y, Edwards JE Jr, (2005) Rhizopus oryzae adheres to, is phagocytosed by, and damages endothelial cells in vitro. Infect Immun 73: 778-783.
50. Suzuki T, Ushikoshi S, Morita H, Fukuoka H, (2007) Aqueous extracts of Rhizopus oryzae induce apoptosis in human promyelocytic leukemia cell line HL-60. J Health Sci 53: 760-765.
51. Zaragoza O, Garcia-Rodas R, Nosanchuk JD, Cuenca-Estrella M, Rodriguez-Tudela JL, et al. (2010) Fungal cell gigantism during mammalian infection. PLoS Pathog 6: e1000945.
52. Okagaki LH, Strain AK, Nielsen JN, Charlier C, Baltes NJ, et al. (2010) Cryptococcal cell morphology affects host cell interactions and pathogenicity. PLoS Pathog 6: e1000953.
53. Hung C-Y, Xue J, Cole GT, (2007) Virulence mechanisms of Coccidioides. Ann N Y Acad Sci 1111: 225-235.
54. Huppert M, Sun SH, Harrison JL, (1982) Morphogenesis throughout saprobic and parasitic cycles of Coccidioides immitis. Mycopathologia 78: 107-122.
55. Stout DL, Shaw CR, (1974) Genetic distance among certain species of Mucor. Mycologia 66: 969-977.
56. Kwon-Chung KJ, (1973) Studies on Emmonsiella capsulata. I. Heterothallism and development of the ascocarp. Mycologia 65: 109-121.
57. Coppin E, Debuchy R, Arnaise S, Picard M, (1997) Mating types and sexual development in filamentous ascomycetes. Microbiol Mol Biol Rev 61: 411-428.
58. Turgeon BG, Yoder OC, (2000) Proposed nomenclature for mating type genes of filamentous ascomycetes. Fungal Genet Biol 31: 1-5.
59. Lee SC, Corradi N, Doan S, Dietrich FS, Keeling PJ, et al. (2010) Evolution of the sex-related locus and genomic features shared in microsporidia and fungi. PLoS ONE 5: e10539.
60. Xu J, Saunders CW, Hu P, Grant RA, Boekhout T, et al. (2007) Dandruff-associated Malassezia genomes reveal convergent and divergent virulence traits shared with plant and human fungal pathogens. Proc Natl Acad Sci U S A 104: 18730-18735.
61. Bakkeren G, Kronstad JW, (1994) Linkage of mating-type loci distinguishes bipolar from tetrapolar mating in basidiomycetous smut fungi. Proc Natl Acad Sci U S A 91: 7085-7089.
62. Lee N, Bakkeren G, Wong K, Sherwood JE, Kronstad JW, (1999) The mating-type and pathogenicity locus of the fungus Ustilago hordei spans a 500-kb region. Proc Natl Acad Sci U S A 96: 15026-15031.
63. Fraser JA, Diezmann S, Subaran RL, Allen A, Lengeler KB, et al. (2004) Convergent evolution of chromosomal sex-determining regions in the animal and fungal kingdoms. PLoS Biol 2: e384.
64. Lengeler KB, Fox DS, Fraser JA, Allen A, Forrester K, et al. (2002) Mating-type locus of Cryptococcus neoformans: a step in the evolution of sex chromosomes. Eukaryot Cell 1: 704-718.
65. Hesseltine CW, Rogers R, (1987) Dark-period induction of zygospores in Mucor. Mycologia 79: 289-297.
66. Sambrook J, Fritsch EF, Maniatis T, (1989) Molecular cloning: A laboratory manual Cold Spring Harbor, NY Cold Spring Harbor Laboratory Press.
67. Nagy A, Vagvolgyi C, Balla E, Frenczy L, (1994) Electrophoretic karyotype of Mucor circinelloides. Curr Genet 26: 45-48.
68. Diaz-Minguez JM, Lopez-Matas MA, Eslava AP, (1999) Complementary mating types of Mucor circinelloides show electrophoretic karyotype heterogeneity. Curr Genet 36: 383-389.
69. Davidson RC, Blankenship JR, Kraus PR, de Jesus Berrios M, Hull CM, et al. (2002) A PCR-based strategy to generate integrative targeting alleles with large regions of homology. Microbiology 148: 2607-2615.
70. Nicolas FE, Torres-Martinez S, Ruiz-Vazquez RM, (2003) Two classes of small antisense RNAs in fungal RNA silencing triggered by non-integrative transgenes. EMBO J 22: 3983-3991.
71. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
72. Guindon S, Gascuel O, (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
73. Huson DH, Richter DC, Rausch C, Dezulian T, Franz M, et al. (2007) Dendroscope: An interactive viewer for large phylogenetic trees. BMC Bioinformatics 8: 460.