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Eukaryotic Cell, August 2007, p. 1380-1391, Vol. 6, No. 8
1535-9778/07/$08.00+0     doi:10.1128/EC.00229-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Coding Tandem Repeats Generate Diversity in Aspergillus fumigatus Genes{triangledown} ,{dagger}

Emma Levdansky,1,{ddagger} Jacob Romano,1,{ddagger} Yona Shadkchan,1 Haim Sharon,1 Kevin J. Verstrepen,2,3 Gerald R. Fink,4 and Nir Osherov1*

Department of Human Microbiology, Sackler School of Medicine, Tel-Aviv University, Ramat-Aviv 69978, Tel-Aviv, Israel,1 FAS Center for Systems Biology, Harvard University, 7 Divinity Ave., Cambridge, Massachusetts 02138,2 Department of Molecular and Microbial Systems, K. U. Leuven, Faculty of Applied Bioscience and Engineering, Kasteelpark Arenberg 22, B-3001 Leuven, Belgium,3 Whitehead Institute for Biomedical Research/Massachusetts Institute of Technology, Nine Cambridge Center, Cambridge, Massachusetts4

Received 16 July 2006/ Accepted 30 May 2007

Genes containing multiple coding mini- and microsatellite repeats are highly dynamic components of genomes. Frequent recombination events within these tandem repeats lead to changes in repeat numbers, which in turn alters the amino acid sequence of the corresponding protein. In bacteria and yeasts, the expansion of such coding repeats in cell wall proteins is associated with alterations in immunogenicity, adhesion, and pathogenesis. We hypothesized that identification of repeat-containing putative cell wall proteins in the human pathogen Aspergillus fumigatus may reveal novel pathogenesis-related elements. Here, we report that the genome of A. fumigatus contains as many as 292 genes with internal repeats. Fourteen of 30 selected genes showed size variation of their repeat-containing regions among 11 clinical A. fumigatus isolates. Four of these genes, Afu3g08990, Afu2g05150 (MP-2), Afu4g09600, and Afu6g14090, encode putative cell wall proteins containing a leader sequence and a glycosylphosphatidylinositol anchor motif. All four genes are expressed and produce variable-size mRNA encoding a discrete number of repeat amino acid units. Their expression was altered during development and in response to cell wall-disrupting agents. Deletion of one of these genes, Afu3g08990, resulted in a phenotype characterized by rapid conidial germination and reduced adherence to extracellular matrix suggestive of an alteration in cell wall characteristics. The Afu3g08990 protein was localized to the cell walls of dormant and germinating conidia. Our findings suggest that a subset of the A. fumigatus cell surface proteins may be hypervariable due to recombination events in their internal tandem repeats. This variation may provide the functional diversity in cell surface antigens which allows rapid adaptation to the environment and/or elusion of the host immune system.

* Corresponding author. Mailing address: Department of Human Microbiology, Sackler School of Medicine, Tel-Aviv University, Ramat-Aviv 69978, Tel-Aviv, Israel. Phone: 972-3-640-9599. Fax: 972-3-640-9160. E-mail: nosherov{at}post.tau.ac.il

{triangledown} Published ahead of print on 8 June 2007.

{dagger} Supplemental material for this article may be found at http://ec.asm.org/.

{ddagger} Both authors contributed equally to this work.

Eukaryotic Cell, August 2007, p. 1380-1391, Vol. 6, No. 8
1535-9778/07/$08.00+0     doi:10.1128/EC.00229-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



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