Microevolutionary traits and comparative population genomics of the emerging pathogenic fungus Cryptococcus gattii

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 371, Issue 1709, 2016, Pages

  Farrer, Rhys A ^a,b   Voelz, Kerstin ^c,d   Henk, Daniel A ^b   Johnston, Simon A ^c,e   Fisher, Matthew C ^b   May, Robin C ^c,d   Cuomo, Christina A ^a  

^a BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d QUEEN ELIZABETH HOSPITAL   (United Kingdom)

^e UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Cryptococcus gattii; Intracellular proliferation; Microevolution; Mitochondrial tubularization

Indexed keywords

COMPARATIVE STUDY; FUNGUS; GENOME; HOST RANGE; LIFE HISTORY TRAIT; MITOCHONDRION; MORBIDITY; PATHOGEN; PATHOGENICITY; VIRULENCE;

BRITISH COLUMBIA; CANADA; PACIFIC NORTHWEST; VANCOUVER ISLAND;

ANIMALIA; CRYPTOCOCCUS GATTII; FUNGI;

CHROMOSOMAL MAPPING; CRYPTOCOCCOSIS; CRYPTOCOCCUS GATTII; FUNGAL GENOME; GENETICS; HOST RANGE; HUMAN; METAGENOMICS; MICROBIOLOGY; MOLECULAR EVOLUTION; PATHOGENICITY; PHYLOGENY; PHYSIOLOGY; VIRULENCE;

CHROMOSOME MAPPING; CRYPTOCOCCOSIS; CRYPTOCOCCUS GATTII; EVOLUTION, MOLECULAR; GENOME, FUNGAL; HOST SPECIFICITY; HUMANS; METAGENOMICS; PHYLOGENY; VIRULENCE;

EID: 84992449490     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2016.0021     Document Type: Article

References (57)

1. Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ. 2012 Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194. (doi:10.1038/nature10947)
2. Martel A et al. 2014 Wildlife disease. Recent introduction of a chytrid fungus endangers Western Palearctic salamanders. Science 346, 630–631. (doi:10.1126/science.1258268)
3. Singh RP et al. 2011 The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annu. Rev. Phytopathol. 49, 465–481. (doi:10.1146/annurev-phyto-072910-095423)
4. Fraser JA et al. 2005 Same-sex mating and the origin of the Vancouver Island Cryptococcus gattii outbreak. Nature 437, 1360–1364. (doi:10.1038/nature04220)
5. Byrnes EJ, III et al. 2010 Emergence and pathogenicity of highly virulent Cryptococcus gattii genotypes in the Northwest United States. PLoS Pathog. 6, e1000850. (doi:10.1371/journal.ppat.1000850)
6. Farrer RA, Henk DA, Garner TWJ, Balloux F, Woodhams DC, Fisher MC. 2013 Chromosomal copy number variation, selection and uneven rates of recombination reveal cryptic genome diversity linked to pathogenicity. PLoS Genet. 9, e1003703. (doi:10.1371/journal.pgen.1003703)
7. Raffaele S et al. 2010 Genome evolution following host jumps in the Irish potato famine pathogen lineage. Science 330, 1540–1543. (doi:10.1126/science.1193070)
8. Datta K et al. 2009 Spread of Cryptococcus gattii into Pacific Northwest region of the United States. Emerg. Infect. Dis. 15, 1185–1191. (doi:10.3201/eid1508.081384)
9. Byrnes EJ et al. 2011 A diverse population of Cryptococcus gattii molecular type VGIII in southern Californian HIV/AIDS patients. PLoS Pathog. 7, e1002205. (doi:10.1371/journal.ppat.1002205)
10. Galanis E, MacDougall L, Kidd S, Morshed M. 2010 Epidemiology of Cryptococcus gattii, British Columbia, Canada, 1999–2007. Emerg. Infect. Dis. 16, 251–257. (doi:10.3201/eid1602.090900)
11. Kidd SE, Guo H, Bartlett KH, Xu J, Kronstad JW. 2005 Comparative gene genealogies indicate that two clonal lineages of Cryptococcus gattii in British Columbia resemble strains from other geographical areas. Eukaryot. Cell 4, 1629–1638. (doi:10.1128/EC.4.10.1629-1638.2005)
12. Hagen F et al. 2015 Recognition of seven species in the Cryptococcus gattii/Cryptococcus neoformans species complex. Fungal Genet. Biol. FG B 78, 16–48. (doi:10.1016/j.fgb.2015.02.009)
13. Byrnes EJ, Bartlett KH, Perfect JR, Heitman J. 2011 Cryptococcus gattii: an emerging fungal pathogen infecting humans and animals. Microbes Infect. Inst. Pasteur 13, 895–907. (doi:10.1016/j.micinf.2011.05.009)
14. Byrnes EJ, Bildfell RJ, Frank SA, Mitchell TG, Marr KA, Heitman J. 2009 Molecular evidence that the range of the Vancouver Island outbreak of Cryptococcus gattii infection has expanded into the Pacific Northwest in the United States. J. Infect. Dis. 199, 1081–1086. (doi:10.1086/597306)
15. Gillece JD et al. 2011 Whole genome sequence analysis of Cryptococcus gattii from the Pacific Northwest reveals unexpected diversity. PLoS ONE 6, e28550. (doi:10.1371/journal.pone.0028550)
16. Engelthaler DM et al. 2014 Cryptococcus gattii in North American Pacific Northwest: whole-population genome analysis provides insights into species evolution and dispersal. mBio 5, e01464-14. (doi:10.1128/mBio.01464-14)
17. Billmyre RB, Croll D, Li W, Mieczkowski P, Carter DA, Cuomo CA, Kronstad JW, Heitman J. 2014 Highly recombinant VGII Cryptococcus gattii population develops clonal outbreak clusters through both sexual macroevolution and asexual microevolution. mBio 5, e01494-14. (doi:10.1128/mBio.01494-14)
18. Feldmesser M, Tucker S, Casadevall A. 2001 Intracellular parasitism of macrophages by Cryptococcus neoformans. Trends Microbiol. 9, 273–278. (doi:10.1016/S0966-842X(01)02035-2)
19. Ma H, Hagen F, Stekel DJ, Johnston SA, Sionov E, Falk R, Polacheck I, Boekhout T, May RC. 2009 The fatal fungal outbreak on Vancouver Island is characterized by enhanced intracellular parasitism driven by mitochondrial regulation. Proc. Natl Acad. Sci. USA 106, 12 980–12 985. (doi:10.1073/pnas.0902963106)
20. Bose I, Reese AJ, Ory JJ, Janbon G, Doering TL. 2003 A yeast under cover: the capsule of Cryptococcus neoformans. Eukaryot. Cell 2, 655–663. (doi:10.1128/EC.2.4.655-663.2003)
21. Ma H, Croudace JE, Lammas DA, May RC. 2006 Expulsion of live pathogenic yeast by macrophages. Curr. Biol. 16, 2156–2160. (doi:10.1016/j.cub.2006.09.032)
22. Alvarez M, Casadevall A. 2006 Phagosome extrusion and host-cell survival after Cryptococcus neoformans phagocytosis by macrophages. Curr. Biol. 16, 2161–2165. (doi:10.1016/j.cub.2006.09.061)
23. D’Souza CA et al. 2011 Genome variation in Cryptococcus gattii, an emerging pathogen of immunocompetent hosts. mBio 2, e00342-10.(doi:10.1128/mBio.00342-10)
24. Farrer RA et al. 2015 Genome evolution and innovation across the four major lineages of Cryptococcus gattii. mBio 6, e00868-15. (doi:10.1128/mBio.00868-15)
25. Voelz K, Johnston SA, Smith LM, Hall RA, Idnurm A, May RC. 2014 ‘Division of labour’ in response to host oxidative burst drives a fatal Cryptococcus gattii outbreak. Nat. Commun. 5, 5194. (doi:10.1038/ncomms6194)
26. Staats CC, Kmetzsch L, Schrank A, Vainstein MH. 2013 Fungal zinc metabolism and its connections to virulence. Front. Cell. Infect. Microbiol. 3, 65. (doi:10.3389/fcimb.2013.00065)
27. Clarke DL, Woodlee GL, McClelland CM, Seymour TS, Wickes BL. 2001 The Cryptococcus neoformans STE11a gene is similar to other fungal mitogenactivated protein kinase kinase kinase (MAPKKK) genes but is mating type specific. Mol. Microbiol. 40, 200–213. (doi:10.1046/j.1365-2958.2001.02375.x)
28. Urbany C, Neuhaus HE. 2008 Citrate uptake into Pectobacterium atrosepticum is critical for bacterial virulence. Mol. Plant-Microbe Interact. MPMI 21, 547–554. (doi:10.1094/MPMI-21-5-0547)
29. Griffiths EJ et al. 2012 A defect in ATP-citrate lyase links acetyl-CoA production, virulence factor elaboration and virulence in Cryptococcus neoformans. Mol. Microbiol. 86, 1404–1423. (doi:10.1111/mmi.12065)
30. Oppenheim RD et al. 2014 BCKDH: the missing link in apicomplexan mitochondrial metabolism is required for full virulence of Toxoplasma gondii and Plasmodium berghei. PLoS Pathog. 10, e1004263. (doi:10.1371/journal.ppat.1004263)
31. Brüggemann H et al. 2006 Virulence strategies for infecting phagocytes deduced from the in vivo transcriptional program of Legionella pneumophila. Cell. Microbiol. 8, 1228–1240. (doi:10.1111/j.1462-5822.2006.00703.x)
32. Herrmann V, Eidner A, Rydzewski K, Blädel I, Jules M, Buchrieser C, Eisenreich W, Heuner K. 2011 GamA is a eukaryotic-like glucoamylase responsible for glycogen-and starch-degrading activity of Legionella pneumophila. Int. J. Med. Microbiol. 301, 133–139. (doi:10.1016/j.ijmm.2010.08.016)
33. Steenbergen JN, Shuman HA, Casadevall A. 2001 Cryptococcus neoformans interactions with amoebae suggest an explanation for its virulence and intracellular pathogenic strategy in macrophages. Proc. Natl Acad. Sci. USA 98, 15 245–15 250. (doi:10.1073/pnas.261418798)
34. Hnisz D, Majer O, Frohner IE, Komnenovic V, Kuchler K. 2010 The Set3/Hos2 histone deacetylase complex attenuates cAMP/PKA signaling to regulate morphogenesis and virulence of Candida albicans. PLoS Pathog 6, e1000889. (doi:10.1371/journal.ppat.1000889)
35. O’Meara TR, Alspaugh JA. 2012 The Cryptococcus neoformans capsule: a sword and a shield. Clin. Microbiol. Rev. 25, 387–408. (doi:10.1128/CMR.00001-12)
36. Moyrand F, Chang YC, Himmelreich U, Kwon-Chung KJ, Janbon G. 2004 Cas3p belongs to a sevenmember family of capsule structure designer proteins. Eukaryot. Cell 3, 1513–1524. (doi:10.1128/EC.3.6.1513-1524.2004)
37. Yang Z. 2007 PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591. (doi:10.1093/molbev/msm088)
38. Chiranand W, McLeod I, Zhou H, Lynn JJ, Vega LA, Myers H, Yates JR, Lorenz MC, Gustin MC. 2008 CTA4 transcription factor mediates induction of nitrosative stress response in Candida albicans. Eukaryot. Cell 7, 268–278. (doi:10.1128/EC.00240-07)
39. Kalayoglu MV, Morrison RP, Morrison SG, Yuan Y, Byrne GI. 2000 Chlamydial virulence determinants in atherogenesis: the role of chlamydial lipopolysaccharide and heat shock protein 60 in macrophage-lipoprotein interactions. J. Infect. Dis. 181(Suppl 3), S483–S489. (doi:10.1086/315619)
40. Dobbin CA, Smith NC, Johnson AM. 2002 Heat shock protein 70 is a potential virulence factor in murine toxoplasma infection via immunomodulation of host NF-kappa B and nitric oxide. J. Immunol. (Baltimore MD 1950) 169, 958–965.
41. Brown JS, Gilliland SM, Holden DW. 2001 A Streptococcus pneumoniae pathogenicity island encoding an ABC transporter involved in iron uptake and virulence. Mol. Microbiol. 40, 572–585. (doi:10.1046/j.1365-2958.2001.02414.x)
42. Rodriguez GM, Smith I. 2006 Identification of an ABC transporter required for iron acquisition and virulence in Mycobacterium tuberculosis. J. Bacteriol. 188, 424–430. (doi:10.1128/JB.188.2.424-430.2006)
43. Angelini C, Bello L, Spinazzi M, Ferrati C. 2009 Mitochondrial disorders of the nuclear genome. Acta Myol. 28, 16–23.
44. Farrer RA, Henk DA, MacLean D, Studholme DJ, Fisher MC. 2013 Using false discovery rates to benchmark SNP-callers in next-generation sequencing projects. Sci. Rep. 3, 1512. (doi:10.1038/srep01512)
45. Hu G, Chen SH, Qiu J, Bennett JE, Myers TG, Williamson PR. 2014 Microevolution during serial mouse passage demonstrates FRE3 as a virulence adaptation gene in Cryptococcus neoformans. mBio 5, pe00941-14. (doi:10.1128/mBio.00941-14)
46. Wartenberg A et al. 2014 Microevolution of Candida albicans in macrophages restores filamentation in a nonfilamentous mutant. PLoS Genet. 10, e1004824. (doi:10.1371/journal.pgen.1004824)
47. Brunke S et al. 2014 One small step for a yeast–microevolution within macrophages renders Candida glabrata hypervirulent due to a single point mutation. PLoS Pathog. 10, e1004478. (doi:10.1371/journal.ppat.1004478)
48. Korte A, Vilhjálmsson BJ, Segura V, Platt A, Long Q, Nordborg M. 2012 A mixed-model approach for genome-wide association studies of correlated traits in structured populations. Nat. Genet. 44, 1066–1071. (doi:10.1038/ng.2376)
49. Sironi M, Cagliani R, Forni D, Clerici M. 2015 Evolutionary insights into host–pathogen interactions from mammalian sequence data. Nat. Rev. Genet. 16, 224–236. (doi:10.1038/nrg3905)
50. Kryazhimskiy S, Plotkin JB. 2008 The population genetics of dN/dS. PLoS Genet. 4, e1000304. (doi:10.1371/journal.pgen.1000304)
51. Voelz K et al. 2013 Transmission of hypervirulence traits via sexual reproduction within and between lineages of the human fungal pathogen Cryptococcus gattii. PLoS Genet. 9, e1003771. (doi:10.1371/journal.pgen.1003771)
52. Springer DJ et al. 2014 Cryptococcus gattii VGIII isolates causing infections in HIV/AIDS patients in Southern California: identification of the local environmental source as arboreal. PLoS Pathog. 10, e10004285. (doi:10.1371/journal.ppat.1004285)
53. Li H. 2013 Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. (ihttps://arxiv.org/abs/1303.3997).
54. Li H et al. 2009 The sequence alignment/map format and SAMtools. Bioinforma. Oxf. Engl. 25, 2078–2079. (doi:10.1093/bioinformatics/btp352)
55. McKenna A et al. 2010 The genome analysis toolkit: a MapReduce framework for analyzing nextgeneration DNA sequencing data. Genome Res. 20, 1297–1303. (doi:10.1101/gr.107524.110)
56. Emanuelsson O, Brunak S, von Heijne G, Nielsen H. 2007 Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2, 953–971. (doi:10.1038/nprot.2007.131)
57. Yang Z, Nielsen R. 2000 Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol. Biol. Evol. 17, 32–43. (doi:10.1093/oxfordjournals.molbev.a026236)