#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Genomic Transition to Pathogenicity in Chytrid Fungi


Understanding the molecular mechanisms of pathogen emergence is central to mitigating the impacts of novel infectious disease agents. The chytrid fungus Batrachochytrium dendrobatidis (Bd) is an emerging pathogen of amphibians that has been implicated in amphibian declines worldwide. Bd is the only member of its clade known to attack vertebrates. However, little is known about the molecular determinants of - or evolutionary transition to - pathogenicity in Bd. Here we sequence the genome of Bd's closest known relative - a non-pathogenic chytrid Homolaphlyctis polyrhiza (Hp). We first describe the genome of Hp, which is comparable to other chytrid genomes in size and number of predicted proteins. We then compare the genomes of Hp, Bd, and 19 additional fungal genomes to identify unique or recent evolutionary elements in the Bd genome. We identified 1,974 Bd-specific genes, a gene set that is enriched for protease, lipase, and microbial effector Gene Ontology terms. We describe significant lineage-specific expansions in three Bd protease families (metallo-, serine-type, and aspartyl proteases). We show that these protease gene family expansions occurred after the divergence of Bd and Hp from their common ancestor and thus are localized to the Bd branch. Finally, we demonstrate that the timing of the protease gene family expansions predates the emergence of Bd as a globally important amphibian pathogen.


Vyšlo v časopise: Genomic Transition to Pathogenicity in Chytrid Fungi. PLoS Pathog 7(11): e32767. doi:10.1371/journal.ppat.1002338
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002338

Souhrn

Understanding the molecular mechanisms of pathogen emergence is central to mitigating the impacts of novel infectious disease agents. The chytrid fungus Batrachochytrium dendrobatidis (Bd) is an emerging pathogen of amphibians that has been implicated in amphibian declines worldwide. Bd is the only member of its clade known to attack vertebrates. However, little is known about the molecular determinants of - or evolutionary transition to - pathogenicity in Bd. Here we sequence the genome of Bd's closest known relative - a non-pathogenic chytrid Homolaphlyctis polyrhiza (Hp). We first describe the genome of Hp, which is comparable to other chytrid genomes in size and number of predicted proteins. We then compare the genomes of Hp, Bd, and 19 additional fungal genomes to identify unique or recent evolutionary elements in the Bd genome. We identified 1,974 Bd-specific genes, a gene set that is enriched for protease, lipase, and microbial effector Gene Ontology terms. We describe significant lineage-specific expansions in three Bd protease families (metallo-, serine-type, and aspartyl proteases). We show that these protease gene family expansions occurred after the divergence of Bd and Hp from their common ancestor and thus are localized to the Bd branch. Finally, we demonstrate that the timing of the protease gene family expansions predates the emergence of Bd as a globally important amphibian pathogen.


Zdroje

1. SmithKFGueganJF 2010 Changing Geographic Distributions of Human Pathogens. Annual Review of Ecology, Evolution, and Systematics, Vol 41 Palo Alto Annual Reviews 231 250

2. WoolhouseMGauntE 2007 Ecological origins of novel human pathogens. Crit Rev Microbiol 33 231 242

3. HoskissonPATrevorsJT 2010 Shifting trends in pathogen dynamics on a changing planet. Antonie Van Leeuwenhoek 98 423 427

4. BergerLSpeareRDaszakPGreenDECunninghamAA 1998 Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc Natl Acad Sci U S A 95 9031 9036

5. LipsKRBremFBrenesRReeveJDAlfordRA 2006 Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc Natl Acad Sci U S A 103 3165 3170

6. LöttersSLa MarcaEStuartSGagliardoRVeithM 2004 A new dimension of current biodiversity loss. Herpetotropicos 1 29 31

7. SkerrattLFBergerLSpeareRCashinsSMcDonaldKR 2007 Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4 125 134

8. JamesTYLetcherPMLongcoreJEMozley-StandridgeSEPorterD 2006 A molecular phylogeny of the flagellated fungi (Chytridiomycota) and description of a new phylum (Blastocladiomycota). Mycologia 98 860 871

9. RosenblumEBStajichJEMaddoxNEisenMB 2008 Global gene expression profiles for life stages of the deadly amphibian pathogen Batrachochytrium dendrobatidis. Proc Natl Acad Sci U S A 105 17034 17039

10. BurmesterAShelestEGlöcknerGHeddergottCSchindlerS 2011 Comparative and functional genomics provide insights into the pathogenicity of dermatophytic fungi. Genome Biol 12 R7

11. MonodM 2008 Secreted Proteases from Dermatophytes. Mycopathologia 166 285 294

12. MonodMCapocciaSLéchenneBZauggCHoldomM 2002 Secreted proteases from pathogenic fungi. Int J Med Microbiol 292 405 419

13. da SilvaBAdos SantosALSBarreto-BergterEPintoMR 2006 Extracellular peptidase in the fungal pathogen Pseudallescheria boydii. Curr Microbiol 53 18 22

14. LetcherPMPowellMJChurchillPFChambersJG 2006 Ultrastructural and molecular phylogenetic delineation of a new order, the Rhizophydiales (Chytridiomycota). Mycol Res 110 898 915

15. RachowiczLJKnappRAMorganJATSticeMJVredenburgVT 2006 Emerging infectious disease as a proximate cause of amphibian mass mortality. Ecology 87 1671 1683

16. NotredameCHigginsDGHeringaJ 2000 T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 302 205 217

17. Capella-GutiérrezSSilla-MartínezJMGabaldónT 2009 trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25 1972 1973

18. BarrDJS 1986 Allochytridium expandens rediscovered - morphology, physiology and zoospore ultrastructure. Mycologia 78 439 448

19. ZolanMEPukkilaPJ 1986 Inheritance of DNA methylation in Coprinus cinereus. Mol Cell Biol 6 195 200

20. DeweyC 2007 Aligning multiple whole genomes with Mercator and MAVID. Methods Mol Biol 395 221 236

21. CantarelBLKorfIRobbSMCParraGRossE 2008 MAKER: An easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res 18 188 196

22. Ter-HovhannisyanVLomsadzeAChernoffYOBorodovskyM 2008 Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training. Genome Res 18 1979 1990

23. FinnRDMistryJTateJCoggillPHegerA 2010 The Pfam protein families database. Nucleic Acids Res 38 D211 D222

24. ParraGBradnamKKorfI 2007 CEGMA: a pipeline to accurately annotate core genes in eukaryotic genornes. Bioinformatics 23 1061 1067

25. AltschulSFGishWMillerWMyersEWLipmanDJ 1990 Basic local alignment search tool. J Mol Biol 215 403 410

26. LiLStoeckertCJRoosDS 2003 OrthoMCL: Identification of ortholog groups for eukaryotic genomes. Genome Res 13 2178 2189

27. BoyleEIWengSAGollubJJinHBotsteinD 2004 GO::TermFinder - open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics 20 3710 3715

28. EdgarRC 2004 MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32 1792 1797

29. StamatakisALudwigTMeierH 2005 RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21 456 463

30. YangZH 2007 PAML 4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol 24 1586 1591

31. HanadaKZouCLehti-ShiuMDShinozakiKShiuSH 2008 Importance of lineage-specific expansion of plant tandem duplicates in the adaptive response to environmental stimuli. Plant Physiol 148 993 1003

32. YangZHBielawskiJP 2000 Statistical methods for detecting molecular adaptation. Trends Ecol Evol 15 496 503

33. LynchMConeryJS 2000 The evolutionary fate and consequences of duplicate genes. Science 290 1151 1155

34. LongcoreJEPessierAPNicholsDK 1999 Batrachochytrium dendrobatidis gen et sp nov, a chytrid pathogenic to amphibians. Mycologia 91 219 227

35. VoylesJYoungSBergerLCampbellCVoylesWF 2009 Pathogenesis of Chytridiomycosis, a Cause of Catastrophic Amphibian Declines. Science 326 582 585

36. JoussonOLéchenneBBontemsOCapocciaSMignonB 2004 Multiplication of an ancestral gene encoding secreted fungalysin preceded species differentiation in the dermatophytes Trichophyton and Microsporum. Microbiology 150 301 310

37. SharptonTJStajichJERounsleySDGardnerMJWortmanJR 2009 Comparative genomic analyses of the human fungal pathogens Coccidioides and their relatives. Genome Res 19 1722 1731

38. KaurRMaBCormackBP 2007 A family of glycosylphosphatidylinositol-linked aspartyl proteases is required for virulence of Candida glabrata. Proc Natl Acad Sci U S A 104 7628 7633

39. MonodMBorg-von ZepelinM 2002 Secreted aspartic proteases as virulence factors of Candida species. Biol Chem 383 1087 1093

40. GaillardinC 2010 Lipases as Pathogenicity Factors of Fungi. TimmisKN Handbook of Hydrocarbon and Lipid Microbiology Springer 3259 3268

41. BrunkeSHubeB 2006 MfLIP1, a gene encoding an extracellular lipase of the lipid-dependent fungus Malassezia furfur. Microbiology 152 547 554

42. HaasBJKamounSZodyMCJiangRHYHandsakerRE 2009 Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461 393 398

43. KamounS 2006 A catalogue of the effector secretome of plant pathogenic oomycetes. Annu Rev Phytopathol 44 41 60

44. Cavalier-SmithTChaoEEY 2006 Phylogeny and megasystematics of phagotrophic heterokonts (kingdom Chromista). J Mol Evol 62 388 420

45. FreemanKRMartinAPKarkiDLynchRCMitterMS 2009 Evidence that chytrids dominate fungal communities in high-elevation soils. Proc Natl Acad Sci U S A 106 18315 18320

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2011 Číslo 11
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#