Research in our Lab

The Aspergillus Genetics & Molecular Biology group is established in the Department of Botany (1st floor, left corridor, Microbiology lab) within the Faculty of Biology at the Panepistimioupolis (Kaisariani/ Zografou) of the National and Kapodistrian University of Athens. The Department is relatively well equipped with major facilities for studies on plant and microbial genetics, biochemistry, physiology and molecular biology. Our group is primarily interested in several aspects concerning the expression, function, cell biology and evolution of transporters. Our model organism of choice is the non-pathogenic, filamentous fungus Aspergillus nidulans, a classic model genetic system, since the 1950's.

 

Why Transporters?

·   The cellular membranes are practically impermeable barriers. However, all cells need to control the influx and efflux of solutes and ions, which is  a basic biological process implicated in nutrition, signaling, neurotransmission, homeostasis, cell communication & defense.

·    Transporters & channels control both the influx and efflux of solutes and ions. Approximately 8-20% of all genes in genomes encode transporters and channels, whereas up to 20% of genes in eukaryotic genomes are believed to be involved in the control of expression, cellular sorting, trafficking and turnover of transporters and channels.

·     Several human genetic disorders caused by alterations in transport proteins (e.g cystic fibrosis, diabetes, neurodegeneration, etc).

·     Transporters also act as specific gateways for specific drug delivery to target cells (microbes, pathogens, cancer cells).

·     Transporters are responsible for the pleiotropic or multidrug drug resistance (PDR/MDR), through ABC and MFS efflux proteins (antibiotic resistance, cancer cell resistance to chemicals).

·     Despite their importance, few transporter & channel molecular structures are currently known (<450 unique PDB entries, of which 87 are ion channels/exchangers, 21 are transporters involved in efflux of toxic metabolites or drugs, and 37 are solute transporters, from which only 2 are eukaryotic transporter).

Thus, for understanding how cells function and communicate there is an obvious need for understanding transporters and channels and developing relevant approaches to do that.

 

Why Aspergillus as a model system?

1953 Pontecorvo published the compendium of the genetics of the ascomycete fungus Aspergillus nidulans1. Since 1984, after the development of transformation protocols, A. nidulans has also become a model microbial system for molecular biology and reverse genetics approach. Practically, most of what can be done in Saccharomyces cerevisiae, can be done in A. nidulans. The beautiful and sophisticated system of A. nidulans genetics, molecular and cell biology led to the analysis of multiple metabolic and cellular processes. It suffices to highlight the identification by Claudio Scazzocchio, Herb Arst and co-workers of the crucial actors of nitrogen metabolite and carbon catabolite repression2, the work of Ron Morris and his school3, which matches the Nobel winning work of Paul Nurse and Lee Hartwell, the dissection of conidial development initiated by Bill Timberlake with the introduction of the methodology of cascade hybridisation4, and the recent work of Miguel Angel Penalva on membrane trafficking, Golgi dynamics and endocytosis5.

Other Aspergilli are used in biotechnological processes that range from the production of soja sauce and sake (A. soyae, A. oryzae), to the production of citric acid (A. niger) and the production of heterologous proteins. A. fumigatus has graduated, thanks to immunosuppression, from rare pathogen to one of the most common causes of fatal nosocomial infection. A. flavus, a noxious contaminant of food-stuffs, produces aflatoxin, the most powerful carcinogen known. A. sydowi is an insidious pathogen of gorgonian corals. A issue of Nature carries three articles describing the genomic sequences of A. nidulans6, A. oryzae7 and A. fumigatus8. The differences between A. nidulans and the other two Aspergilli match the differences found between fish and humans, which are separated by 500 million years, suggesting a very rapid rate of divergence in this genus. The A. oryzae genome has 12074 predicted proteins as compared with 9926 for A. fumigatus and 9541 for A. nidulans. The excess of A. oryzae putative genes concerns mainly secondary metabolism, and may be due to horizontal gene transfer, including from prokaryotes. A. nidulans is homothallic, but there are heterothallic species of Aspergillus, while no apparent sexual cycle has been described for A. fumigatus or A. oryzae9.

What clearly distinguishes A. nidulans from S. cerevisiae and other model yeasts is its mode of polar life10. Cell polarity is, for example, highly demanding in special mechanisms for rapid protein exocytosis and endocytosis along very long cells, the apical parts of which possessing additional needs on membrane trafficking, as compared to sub-apical parts or non-polar cells like yeasts. In fact, genetic evidence in filamentous fungi shows that rapid endocytosis of membrane proteins followed by their re-delivery to the plasma membrane generates and maintains polarity11. Interestingly, the molecular mechanisms underlying fungal polarity are analogous or/and homologous to those found in the cells of higher animals, such as mammalian neurons12.

References

1.    Pontecorvo G, Roper JA, Hemmons L.M, MacDonald KD and Bufton AWJ. (1953). The Genetics of Aspergillus nidulans. Adv Genet 5: 144-238.

2.    Arst HNJr and Cove DJ. (1973). Nitrogen Metabolite Repression in Aspergillus nidulans. Mol Gen Genet 126:111-141.

3.    Morris NR and Enos AP. (1992). Mitotic gold in a mold. Trends Genet 8:32-37.

4.    Timberlake WE. (1990). Molecular Genetics of Aspergillus Development. Ann Rev Genet 24:5-36.

5.    Pantazopoulou A, Penalva MA. (2009). Organization and dynamics of the A. nidulans Golgi during apical extension and mitosis. Mol Biol Cell 20: 4335-7

6.    Galagan JE. et al. (2005). Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438:1106-1115.

7.    Machida M. et al. (2005). Genome sequencing and analysis of Aspergillus oryzae. Nature 438:1157-11661.

8.    Nierman WC. et al. (2005) Genomic sequence of the pathogenic and allergenic fungus Aspergillus fumigatus. Nature 438:1151-1156.

9.    Geiser DM, Timberlake WE and Arnold ML. (1996). Loss of Meiosis in Aspergillus. Mol Biol Evol 13:809-817.

10.   Fischer R, Zekert N, Takeshita N. (2008). Polarized growth in fungi--interplay between the cytoskeleton, positional markers and membrane domains. Mol Microbiol 68:813-26.

11.   Taheri-Talesh N, Horio T, Araujo-Bazán L, Dou X, Espeso EA, Peñalva MA, Osmani SA, Oakley BR. (2008). The tip growth apparatus of Aspergillus nidulans. Mol Biol Cell 19:1439-49.

12.   Egan MJ, McClintock MA, Reck-Peterson SL. (2012). Microtubule-based transport in filamentous fungi. Curr Opin Microbiol 15:637-45.

13.   Casselton L and Zolan M. (2002). The art and design of genetic screens: filamentous fungi. Nat Rev Genet 3:683-697

Why Aspergillus particularly for studying transporters?

·         Fine knowledge of metabolism & easiness of knock-out/reverse genetics

·        Easily scored phenotypes on toxic analogues (e.g. 8-azaguanine, oxypurinol, allopurinol, 5-FC, 5-FU,5-FUd)

·         Direct genetic selection of transporter mutations or suppressors-conditional, specificity or affinity mutants

·         Easy radiolabelled solute uptake assays with germinating conidiospores

·         Use of GFP, RFP to distinguish functional, trafficking & turnover mutants

·         Rich repertoire of transport proteins-all basic families found in metazoa-703 putative transporter/channels  [81.5 secondary active transporters, 11.8% primary-active transporters, 4.4% channels]

A, Growth tests of wild-type and transporter null mutants of A. nidulans on toxic purine analogues (5|FU, 5FUI, OX) or purines as N sources (UA, AD, HX, ALL). B, Confocal fluorescence microscopic view of A. nidulans expressing a functional UapA-GFP transporter. C, Germination of A. nidulans conidiospores and generation of germlings (very young mycelia). D, Radiolabelled uptake studies of purine transporter at a stage prior germlings development.