1. Evolution of the Aspergilli: stuff for genomicists to think about
David M. Geiser
Penn State University, USA

2. Aspergillus evolution
What is Aspergillus?
The major players in the genus and how are they related
Interesting comparative questions about Aspergillus
Studying evolution using genomics and studying genomics using evolution

3. What is Aspergillus?
Aspergillus is a Eurotiomycete (or “Plectomycete”)
Aspergillus species appear to have a common evolutionary origin
this is a weak inference
Aspergillus species are diverse in their life histories
Homothallic
Heterothallic
Not seen to undergo sex
Nine different described sexual stages (Emericella, Eurotium, Neosartorya, Petromyces, Fennellia, Sclerocleista, Warcupiella, Hemicarpenteles, Chaetosartorya)

4. Aspergillus is a Eurotiomycete
18S rDNA
Geiser and
Lo Buglio
2001

5. Eurotiomycetes
Thallic (Ascosphaerales, Onygenales) and Phialidic (Eurotiales) anamorphs
Asci produced naked, in wefts of hyphae (gymnothecia) or in a solid enclosed fruiting body (cleistothecia)
Cleistothecia may be borne in a stroma
Many human and animal pathogens
Onygenales: Cocci, Histo, Blasto, dermatophytes
Eurotiales: Aspergillus, P. marneffei
Very chemically creative
An ectomycorrhizal fungus! (Elaphomyces)
NO LICHENIZED FUNGI
Osmophiles, thermophiles
Industrial fungi

6. Conidiation in the Plectomycetes
thallic (T): Onygenales, Ascosphaerales
blastic (B): Eurotiales T
biseriate B T B T B B
uniseriate
Geiser and LoBuglio 2001

7. Ascomatal types in the Eurotiomycetes
cleistothecia borne in a stroma (C/S)
cleistothecia not borne in a stroma (C)
stroma, with no cleistothecia (S)
no cleistothecia and no stroma (N)
Trichocoma
Eupenicillium
Emericella
Petromyces
C/S
C/S
C/S
Gymnoascus
Onygena S S
Monascus
Byssochlamys
Ascosphaera
Eurotium C C C
nutriocyte N
Geiser and LoBuglio 2001

8. Sexual stages associated phylogenetically with important Aspergillus spp.
Emericella and Aspergillus nidulans
True cleistothecium surrounded by a stroma of hülle cells
Petromyces and A. flavus/oryzae/parasiticus/niger (?)
Cleistothecia embedded in a stroma (sclerotia)
Neosartorya and A. fumigatus
Cleistothecia/gymnothecia with wall composed of cottony hyphae.

9. Aspergillus phylogenetics
Not a lot of data useful for inferring large-scale relationships
Take many of the trees I show with a grain of salt…

10. Aspergillus -- monophyletic?
18S rDNA
Aspergillus -- monophyletic?
Tamura, M.
Kawahara, K.
Sugiyama, J.
2000.

12. Aspergillus 25S rDNA tree
Based on a single locus, ~600 bp
Backbone of tree gets poor support
Major traditional species groups are supported
The morphologists did/are doing a pretty good job

13. Emericella sexual stage cleistothecium surrounded
Petromyces
sexual stage
multiloculate
stroma
Emericella sexual stage
cleistothecium surrounded
by hülle cells (stroma)
Eurotium sexual stage
cleistothecium, no
stroma
Sclerocleista
Warcupiella
Neosartorya sexual stage
cleistothecium composed
of cottony hyphae
Fennellia sexual stage
Chaetosartorya sexual stage

14. Subgenus
Circumdati:
Association with
plants,seeds
psychrotolerance
Xerophilicty/tolerance
heat-resistant ascospores
Thermotolerance
heat-resistant ascospores

15. The players in Aspergillus genomics
Aspergillus nidulans
“Emericella clade”
Aspergillus nidulans group
Aspergillus section Nidulantes
Aspergillus fumigatus
Aspergillus oryzae

16. Emericella clade A. nidulans A. sydowii - coral pathogen Hülle cells
NJ analysis of Steve Peterson’s 25S data
A. nidulans
A. sydowii - coral pathogen
Hülle cells
Homothallics
Putative asexuals
Heterothallic

17. Aspergillosis of sea fan corals
Aspergillus sydowii
in culture: a relative of
A. nidulans!
Geiser, D.M.
Ritchie, K.
Smith, G.
Taylor, J.W.
Nature, 1998
Kiho Kim
Aspergillosis of sea fan coral

18. Sexual versus asexual strategies
Aspergillus heterothallicus - described by June Kwon-Chung (Raper and Fennell 1965)
One of three known heterothallic species (other two are Neosartoryas, clademates with A. fumigatus)
Known asexuals should be predicted to be recombining:
Population genetic evidence: a rich literature
Taylor et al. 2000, Annu. Rev. Phytopath.
MAT locus molecular genetics/phylogenetics
Turgeon, Berbee and others
Homothallics do not necessarily outcross less than heterothallics!

19. Known heterothallics

20. Early events in ascus development in the Eurotiales: designed for homothallism?
Benjamin, 1955

21. The players in Aspergillus genomics
Aspergillus nidulans
Aspergillus fumigatus
Neosartorya clade
Aspergillus fumigatus group
Aspergillus section Fumigati
Aspergillus oryzae

22. Geiser, D.M.
Frisvad, J.
Taylor, J.W.
Mycologia,1998
Beta-tubulin +
rodA hydrophobin
heterothallic
heterothallic

23. Geiser, D.M.
Frisvad, J.
Taylor, J.W.
Mycologia 1998
Beta-tubulin +
rodA hydrophobin

24. Geiser, D.M.
Frisvad, J.
Taylor, J.W.
Mycologia 1998
Beta-tubulin +
rodA hydrophobin

25. Evolution in Aspergillus fumigatus group
Monophyletic
A. fumigatus and N. fischeri are close relatives
Heterothallism derived?
Secondary metabolite data contrasts with benA/rodA phylogeny
Pringle, Taylor and others: asking the question whether it’s asexual

26. The players in Aspergillus genomics
Aspergillus nidulans
Aspergillus fumigatus
Aspergillus oryzae
Petromyces clade
Aspergillus flavus group
Aspergillus Section Circumdati

27. A. flavus, A. oryzae, A. niger and relatives (Petromyces)
NJ analysis of Steve Peterson’s 25S data

28. Geiser, DM
Pitt, JI
Taylor JW
PNAS
1998

29. Geiser, DM
Horn, BW
Dorner, JW
Taylor JW
FG&B
2001

30. Using evolution to do good genomics
Comparative genomics IS evolutionary biology
Conservation of function is an adaptive process
Clark et al Inferring non-neutral evolution from human-chimp-mouse orthologous gene trios. Science 302;

31. The future
Genomics helps traditional evolutionary biologists to do their jobs because it provides tools
Understanding how genes evolve provides a framework for thinking about how they might function