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Title: Genomic Analysis of the Basal Lineage Fungus Rhizopus oryzae Reveals a Whote-Genome Duplication

Author
item MA, LI-JUN - INST OF MIT & HARVARD
item IBRAHIM, ASHRAF - LA BIOMEDICAL RESEARCH
item Skory, Christopher - Chris
item GRABHERR, MANFRED - INST OF MIT & HARVARD
item BURGER, GERTRAUD - UNIV OF MONTREAL
item LANG, FRANZ - UNIV OF MONTREAL
item ABE, AYUMI - HOKKAIDO UNIV, JAPAN
item BUTLER, MARGI - UNIV OF OTAGO, NEW ZEALAN
item CALVO, SARAH - INST OF MIT & HARVARD
item CORROCHANO, LUIS - UNIV OF SEVILLA, SPAIN
item ELIAS, MAREK - CHARLES UNIV IN PRAGUE
item ENGELS, REINHARD - INST OF MIT & HARVARD
item FU, JIANMIN - UNIV OF TX HEALTH SCI CEN
item HANSBERG, WILHELM - UNIV DE MEXICO
item IDNURM, ALEXANDER - UNIV OF MO, KANSAS CITY
item KIM, JUNG-MI - UNIV OF CA, DAVIS
item KODIRA, CHINNAPPA - INST OF MIT & HARVARD
item KOEHRSEN, MICHAEL - INST OF MIT & HARVARD
item LIU, BO - UNIV OF CA, DAVIS
item MIRANDA-SAAVEDRA, DIEGO - CAMBRIDGE INST OF MED RES
item RODRIGUEZ-ROMERO, JULIO - UNIV DE SEVILLA, SPAIN
item O'LEARY, SINEAD - INST OF MIT & HARVARD
item ORTIZ-CASTELLANOS, LUCILA - UNIDAD IRAPUATO, MEXICO
item POULTER, RUSSELL - UNIV OF OTAGO, N ZEALAND
item RUIZ-HERRERA, JOSE - UNIDAD IRAPUATO, MEXICO
item SHEN, YAOQING - UNIV OF MONTREAL
item SONE, TERUO - HOKKAIDO UNIV, JAPAN
item ZENG, QIANDONG - INST OF MIT & HARVARD
item GALAGAN, JAMES - INST OF MIT & HARVARD
item BIRREN, BRUCE - INST OF MIT & HARVARD
item CUOMO, CHRISTINA - INST OF MIT & HARVARD
item WICKES, BRIAN - UNIV OF TX HEALTH SCI CEN

Submitted to: PLoS Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/23/2009
Publication Date: 6/30/2009
Citation: Ma, L.-J., Ibrahim, A.S., Skory, C.D., Grabherr, M.G., Burger, G., Butler, M., Elias, M., Idnurm, A., Lang, F., Sone, T., Abe, A., Calvo, S.E., Corrochano, L.M., Engels, R., Fu, J., Hansberg, W., Kim, J.-M., Kodira, C.D., Koehrsen, M.J., Liu, B., Miranda-Saavedra, D., O'Leary, S., Ortiz-Castellanos, L., Poulter, R., Rodriguez-Romero, J., Ruiz-Herrera, J., Shen, Y., Zeng, Q., Galagan, J., Birren, B.W., Cuomo, C.A., Wickes, B.L. 2009. Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLoS Genetics. 5(7):e1000549.

Interpretive Summary: Rhizopus is a valuable filamentous fungus that is used for the production of fermented foods, industrial enzymes (e.g., glucoamylase and lipase), organic acids (e.g., lactate and fumarate), and corticosteroids. Even though this fungus is generally regarded as being safe, it is known to be a food spoilage organism, a plant pathogen, and the most prevalent cause of mucormycosis, a life-threatening infection that usually afflicts patients with debilitated immune systems or those with specific underlying abnormalities. The genome of a Rhizopus isolate was sequenced to better understand the genetics of this important organism. Analysis of the genes revealed that this fungus has far more gene duplication than any other organism previously studied. In particular, genes involved in energy production and protein digestion were present in multiple copies and may help to explain why this fungus grows so robustly on many types of plant residues. Additionally, the sequenced genome has already allowed us to more efficiently identify important genes that might serve as targets for improved product formation or inhibition of infectious growth. This study will greatly facilitate our understanding of Rhizopus, as well as other fungi, and should significantly accelerate current research in this area to the benefit of numerous recipients.

Technical Abstract: Rhizopus oryzae is the primary etiologic agent of mucormycosis, an emerging lifethreatening infection. The rapid growth and angioinvasive nature of mucormycotic infections in humans result in an overall mortality rate that exceeds 50%, even with combined surgical and antifungal therapies. As part of the basal lineage of zygomycete fungi, R. oryzae has also been used as a model to study complex life cycles with multicellular stages. Genomic analysis reveals that R. oryzae is the most repetitive fungal genome reported to date, with 35% of its sequence comprised of identifiable repeats, including transposable elements and gene duplicates. The order and genomic arrangement of the gene pairs reveal an ancestral whole-genome duplication (WGD). This WGD, only the second reported in the fungal kingdom, results in complete duplication of all the protein complexes associated with oxidative phosphorylation, the vesicular ATPase and the ubiquitin–proteasome systems. Multiple gene families related to cell growth and signal transduction are expanded as the result of the WGD in combination with recent gene duplications. In connection with the organism’s ability to aggressively invade host tissue, we find large expansions of secreted aspartic protease and subtilase protein families, known fungal virulence factors. Expanded families of cell-wall synthesis enzymes, essential for fungal cell integrity yet absent in the mammalian host, reveal potential targets for novel and zygomycete-specific diagnostic and therapeutic treatments. As an early diverging fungus, R. oryzae shares a higher number of ancestral genes with the metazoa than dikaryotic fungi (ascomycetes and basidiomycetes), demonstrating its utility for the study of eukaryotic regulation and developmental processes that may not be addressed in other fungal model systems.