Black yeast between beauty and beastblackyeast2010.bf.uni-lj.si/fileadmin/userfiles/Lectures/deHoog.pdf · Black yeast between beauty and beast Sybren de Hoog CBS-KNAW Fungal Biodiversity

Black yeast between beauty and beast

Sybren de HoogCBS- KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands

Contents:

Phylogenetic trends

Types of comparable data

Types of speciation

Orders in black yeasts

Glomeromycotina

Pezizomycotina(Euascomycetes)

Saccharomycotina(Hemiascomycetes)

TaphrinomycotinaPucciniomycotina

Ustilaginomycotina

Agaricomycotina

MucoromycotinaBlastocladiomycotinaChytridiomycotinayEntomophthoromycotinaNeocallimastigomycotina

Bayesian tree of 128 evolutionary conserved genes

CBS-KNAW Fungal Biodiversity CentreEbersberger et al. – Nature Precedings

Begerov et al. – Mycologia 2006

CBS-KNAW Fungal Biodiversity CentreXu et al. – PNAS 2007

Predicted secreted proteins

Glomeromycotina

Pezizomycotina(Euascomycetes)

Saccharomycotina(Hemiascomycetes)

TaphrinomycotinaPucciniomycotina

Ustilaginomycotina

Agaricomycotina

MucoromycotinaBlastocladiomycotinaChytridiomycotinayEntomophthoromycotinaNeocallimastigomycotina

Bayesian tree of 128 evolutionary conserved genes

CBS-KNAW Fungal Biodiversity CentreEbersberger et al. – Nature Precedings

ITS-1 of Onygenales (Dermatophytes)

CBS-KNAW Fungal Biodiversity Centre

ITS-1 of Mucorales


Mucorales:

Dermatophytes:


• Morphologically similar over large groups

• Morphologically similar over large groups

• Intragenus (Trichophyton about 20 species) 9.5% ITS diversity

• Intragenus (Mucor about 20 closests species) 47.8% ITS diversity

• Intraspecies ITS stability, e.g. Trichophyton rubrum 1.6% (62 strains)

• Intraspecies ITS stability, e.g. Mucor circinelloides 1.4% (63 strains)

• Interspecies often down to 0-1 base

• Interspecies often 10-35%

• Ecologically homogeneous, keratin-based pathogenicity

• Ecologically homogeneous, hit-and-run strategy

ITS-1 of Ochroconis


Low AFLP diversity in Cladophialophora bantiana

Species with low diversity

CBS-KNAW Fungal Biodiversity CentreBadali et al., in press

[ 10 20 30 40 50 60 70 ][ * * * * * * * ]Hap_1 C-TATGTTTCGACGGCCGCCGGAGGACCGCCTGCG-ATACAG-TA---TA-A-GGGT--CC-TC--CGACCTTTTHap_2 .-.G...........................C...-......-..---..C.-....--..-..--..-......Hap_3 .-.G...........................C...-......-..--C..C.C....--..-..--..-......Hap_4 .-...--------------------------.T.ACC.TTCTGG.CA-G.-.-AAA-GT-A-C.--..-..CC.-Hap_5 .-.G...........................C...-......-..---..C.-....--..-..T-..-......Hap_6 .-.................................-.C....T.C---..-.-....--..-..--.........Hap_7 .-.................................-.C....T.C---..-.-....--..-..--...-....-Hap_8 .-.................................-.C....T.C---..-.-....--..-..--.....-..-Hap_9 .-.G...............................-......-..---..C.-....--..-..--..-......Hap_10 .-.................................-......-..---..-.-....--..-..--........-Hap_11 .T.G...............................A......-..---.C-.-....--..-..--..-.....-Hap_12 .-.................................-.C....T.C---..-.-....--..-..--........-Hap_13 .-.G...............................A......-..---.C-.-....--..-..--..-.....-Hap_14 .-.G...............................-......-..---..C.-....--..-..--..-..-..-Hap_15 .T.G...........................C...-......-..---..C.-....--..-..--..-..-...Hap_16 .-.G...........................C...-......-..---..C.-....--..-..-CA.-.....-Hap_17 .-.G...........................C...-......-..---..C.-....--..-..--..-.....-Hap_18 .-.G...........................C...-......-..---..C.-....--..A..-CA.-.....-Hap_19 .-C.C..............................-.C....T.C---..-.-....-T..-..--.........Hap_20 .-.G...............................A......-..---.C-.-....--..T..--..-..-..-Hap_21 .T...........................A...T.-......-..---..-.-....--..-..--..-.T...-Hap_22 .-.................................-.C....T.C---..-GA....--..-..--.........Hap_23 .-...........................A...T.-......-..---..-.-....--..-..--..--....-Hap_24 .-...........................A...T.-......-..---..-.-....--..-..--T.--....-Hap_25 .-.................................-......-..---..-.-....--..-..-CG.......-Hap_26 .-.................................-......-..---..-.-....--..-..--.......A-Hap_27 .-.G...........................C...-......-..---..C.-....--..-..--..-..-...Hap_28 .-.G...............................A......-..---.C-.-....--..-..--..-......Hap_29 .-.................................-.C....T.C---..-.-....--..-..--.....-...Hap_30 .-...........................A...T.-......-..---..-.-....--..-..--..-.T...-Hap_31 .-.G...............................A......-..---.C-.-....--..-..--..-..--.-Hap_32 .-.G...............................A......-..---.C-.-....--..-..--..-..-...Hap_33 .-...........................A...T.-......-..---..-.-....--..-..--..-.T..A-Hap_34 .-...........................A...T.-......-..---..-.-....--..-..--..-.T....Hap_35 AT...........................A...T.-......-..--C..-.-....T-..-..--..C.T....Hap_36 AC...........................A...T.-......-..---..-.-....--..-..--..-.T....Hap_37 .-.................................-......-..---..-.-....--..-..--...-.....Hap_38 .-.................................-......-..---..-.-....--..-.-----.-.....

Species with high diversity

ITS haplotype diversity in Exophiala dermatitidis

CBS-KNAW Fungal Biodiversity CentreGerrits van den Ende, in prep.

Evolution through selection (sympatric)


Accumulation of virulent genotype / species


Hos

t

Envi

ronm

ent

?

Water in microchannels

Alkaline

Extreme cold

High pressure

Hypersaline

Evolution through mutation and selection


“sloppy space”

Geographic distribution

Evolution via ecological fit: shift to adjacent habitat (peripatric)


!

Double life cycle, epigenetic change


http://www.wandeleninportugal.info/foto_montesinho_coroa.htm�

Monomorphic life cycle, genomic loss


http://www.wandeleninportugal.info/foto_montesinho_coroa.htm�

PoikilotoleranceOligotrophism

Osmotolerance, mycosporinsMelanin, carotenoids

Unsaturated fatty acidsMeristem, EPS

Poor competitors

Pushed away to the edge of life

Dothideales / Capnodiales Chaetothyriales

Extremophily Human pathogenicity

Genomic loss Gain virulence factors

Unspecific habitat Hyperparasitism


K2, Himalaya

8611 m


Dothideales / Capnodiales

Ruibal et al. – Stud. Mycol. 64, 2009

Genomic loss is phylogenetically

successful

Dothideales / Capnodiales

Ruibal et al. – Persoonia 21, 2008

Rock-inhabiting fungi Dothideales

Capnodiales

Chaetothyriales

CBS-KNAW Fungal Biodiversity CentreBadali et al. – Stud. Mycol. 61, 2008

0.1 Rock isolate TRN242Placocarpus schaereri AFTOL 2289Verrucula inconnexaria AFTO L2305100

100

100

96100

Rock isolate TRN107100

95

100

100

Rock isolate TRN488

Cladophialophora hostae CBS 121637Cladophialophora scillae CBS 116464

9882

100100Rock isolate TRN210Rock isolate TRN515Rock isolate TRN508

Cladophialophora sylvestris CBS 350.83Rock isolate TRN475

Cladophialophora minutissima EF016367Cladophialophora minutissima EF016368Cladophialophora humicola CBS 117536100

Rock isolate A95100

Ceramothyrium carniolicum CBS 175.95

97

Rock isolate TRN214Cyphellophora laciniata CBS 190.61Rock isolate TRN436

100 Phialophora europaea CBS 129.96

Cladophialophora proteae CBS 111667Cladophialophora modesta CBS 985.96Sarcinomyces petricola CBS 101157

90 Rock isolateTRN1Rock isolateTRN4Phaeococcomyces CBS 650.76

Glyphium CBS 268.34Coniosporium CBS 885.95

Rock isolate TRN115100

100100

100100

97

Rock isolate TRN247Cladophialophora australiensis CBS 112793Cladophialophora potulentorum CBS 112222

Cladophialophora saturnica CBS 102230Cladophialophora immunda CBS 102227Cladophialophora immunda CBS 102237Cladophialophora arxii CBS 306.94Cladophialophora devriesii CBS 118720Cladophialophora immunda CBS 834.96Cladophialophora immunda CBS 110551Cladophialophora emmonsii CBS 640.96Cladophialophora minourae CBS 556.83Cladophialophora devriesii CBS 147.84Cladophialophora immunda CBS 109797

Cladophialophora bantiana CBS 173.52

Fonsecaea monophora CBS 102243

Capronia pilosella AFTOL 657

Capronia moravica WUC 15.551Capronia munkii AFTOL 656Exophiala dermatitidis AFTOL 668Capronia mansonii CBS 101.67Capronia fungicola CBS 614.96Capronia species 236Capronia species 315Capronia species 26Rhinocladiella anceps CBS 181.65

Capronia species102Capronia parasitica CBS 123.88Exophiala salmonis CBS 157.67

Rhinocladiella mackenziei CBS 650.93

10076

100 100

100

74

72

100

Rock isolate TRN30Exophiala crusticola CBS119970100

Exophiala pisciphila CBS 573.73Exophiala castellanii CBS 158.58Exophiala lecanii-corni CBS 123.3310010094

Exophiala spinifera CBS 899.6899

9697

98

Rock isolate H5

Exophiala bergeri CBS 353.52

Exophiala nishimurae CBS 101538Rock isolate TRN497Rock isolate TRN506Exophiala xenobiotica CBS 115831

Exophiala spinifera CBS 101534Exophiala exophiala CBS 668.76Exophiala oligosperma CBS 725.88Exophiala jeanselmei CBS 507.9090100

99

Rock isolate TRN493Rock isolate TRN14100100

100

8099

Cladophialophora mycetomatis CBS 454.82Cladophialophora mycetomatis CBS 122637

Cladophialophora samoensis CBS 259.83Cladophialophora carrionii CBS 858.96Cladophialophora carrionii CBS 260.83Cladophialophora carrionii CBS 409.96Cladophialophora subtile CBS 122642Cladophialophora yegresii CBS 114405Phialophora verrucosa AFTOL 670Phialophora americana CBS 840.69Capronia semiimmersa AFTOL 658

Rock isolate TRN531Rock isolate TRN486Cladophialophora chaetospira CBS 491.70

Cladophialophora boppii CBS 126.86

75

Fonsecaea pedrosoi CBS 271.37

Her

potr

ichi

ella

ceae

Chae

toth

yria

ceae

Chaetothyriales

Why have black yeast-like fungi such a surprisingly high degree of morbidity in

healthy patients?


Chaetothyriales

OH

OH

Catecholprotocatechuicacid

HO

HO

HO

O

Alkylbenzenes

4-hydroxy-benzoic acid

HO

HO

O

Toluene

Assimilation of highly toxic xenobiotes


Chaetothyriales

Compounds used for assimilation tests

Phenol m-Cresol p-Cresol Benzoic acid Coumarin Syringic acid Vanillic acid

Gallic acid2,5-Dihydroxybenzoic acid m-Coumaric

acidPhloroglucinol Pyrogallol 4-methylcatechol

4-hydroxybenzoic acid

Protocatechuic acid

CatecholL-Phenylalanine L-Tyrosine

L-DopaDopamine Noradrenaline 3,4-dihydrocy

mandelic AcidB B

B P

B

B

A A A A P P

B P

A: abioticB: brainF: fungusP: plant

P F

P

P

F F

P PP

P P

PP

F


MushroomsAmphibian skinFaecesMarine invertebratesOlive, EucalyptusRailway tiesFermented teaHuman brain

Chaetothyriales

Chae

toth

yriales

Her

potr

ichiellace

ae

ROCKPATH

Chae

toth

yriace

ae


TOX

Functional shift?

Chro

mob

last

omyc

osis

Muriform

Meristematic

Rock

Chaetothyriales

Increasing significance of black yeasts

• Extremotolerants, life on Mars, use of melanin, EPS, etc.

• Salt tolerance in agriculture

• Medical and veterinary research

• Bioremediation

Black yeast from beauty to beast – and back!


Documents

Black yeast between beauty and beastblackyeast2010.bf.uni-lj.si/fileadmin/userfiles/Lectures/deHoog.pdf · Black yeast between beauty and beast Sybren de Hoog CBS-KNAW Fungal Biodiversity