Germination of Penicillium paneum Conidia Is Regulated by 1-Octen-3-ol, a Volatile Self-Inhibitor

ABSTRACT Penicillium paneum is an important contaminant of cereal grains which is able to grow at low temperature, low pH, high levels of carbon dioxide, and under acid conditions. P. paneum produces mycotoxins, which may be harmful to animals and humans. We found that conidia in dense suspensions showed poor germination, suggesting the presence of a self-inhibitor. A volatile compound(s) produced by these high-density conditions also inhibited mycelial growth of different species of fungi belonging to a variety of genera, suggesting a broad action range. The heat-stable compound was isolated by successive centrifugation of the supernatant obtained from spore suspensions with a density of 109 conidia ml−1. By using static headspace analyses, two major peaks were distinguished, with the highest production of these metabolites after 22 h of incubation at 25°C and shaking at 140 rpm. Gas chromatography coupled with mass spectra analysis revealed the compounds to be 3-octanone and 1-octen-3-ol. Notably, only the latter compound appeared to block the germination process at different developmental stages of the conidia (swelling and germ tube formation). In this study, 1-octen-3-ol influenced different developmental processes during the P. paneum life cycle, including induction of microcycle conidiation and inhibition of spore germination. Therefore, the compound can be considered a fungal hormone during fungal development.

[1]  T. Abee,et al.  An antifungal compound produced by Bacillus subtilis YM 10-20 inhibits germination of Penicillium roqueforti conidiospores. , 2003, Journal of applied microbiology.

[2]  T. Joh,et al.  Purification and characterization of lipoxygenase from Pleurotus ostreatus. , 2002, Journal of agricultural and food chemistry.

[3]  A. M. Calvo,et al.  Genetic Connection between Fatty Acid Metabolism and Sporulation in Aspergillus nidulans * , 2001, The Journal of Biological Chemistry.

[4]  J. Schnürer,et al.  Effect of the biocontrol yeast Pichia anomala on interactions between Penicillium roqueforti, Penicillium carneum, and Penicillium paneum in moist grain under restricted air supply. , 2000 .

[5]  Arpin,et al.  10-Oxo-trans-8-decenoic acid (ODA): production, biological activities, and comparison with other hormone-like substances in Agaricus bisporus* , 2000, Enzyme and microbial technology.

[6]  J. Schnürer,et al.  Growth of Penicillium roqueforti, P. carneum, and P. paneum during malfunctioning airtight storage of high-moisture grain cultivars , 1999 .

[7]  A. M. Calvo,et al.  Sporogenic Effect of Polyunsaturated Fatty Acids on Development of Aspergillus spp , 1999, Applied and Environmental Microbiology.

[8]  J. Schnürer,et al.  Fungal volatiles as indicators of food and feeds spoilage. , 1999, Fungal genetics and biology : FG & B.

[9]  Y. Hadar,et al.  1-Octen-3-ol and 13-hydroperoxylinoleate are products of distinct pathways in the oxidative breakdown of linoleic acid by Pleurotus pulmonarius , 1997 .

[10]  M. Beltran-Garcia,et al.  Volatile Compounds Secreted by the Oyster Mushroom (Pleurotus ostreatus) and Their Antibacterial Activities , 1997 .

[11]  C. Noël-Suberville,et al.  Fatty Acid Content and Some Flavor Compound Release in Two Strains of Agaricus bisporus, According to Three Stages of Development , 1997 .

[12]  J. Frisvad,et al.  Reclassification of the Penicillium roqueforti group into three species on the basis of molecular genetic and biochemical profiles. , 1996, Microbiology.

[13]  J. Frisvad,et al.  Characterization of volatile metabolites from 47 Penicillium taxa , 1995 .

[14]  R. Nicholson,et al.  A VOLATILE SELF-INHIBITOR FROM COLLETOTRICHUM GRAMINICOLA , 1993 .

[15]  G. Ziegler,et al.  Effect of 10-oxo-trans-8-decenoic acid on growth of Agaricus bisporus , 1992 .

[16]  G. Ziegler,et al.  1‐Octen‐3‐ol in the Cultivated Mushroom, Agaricus bisporus , 1992 .

[17]  R. C. French Volatile chemical germination stimulators of rust and other fungal spores , 1992 .

[18]  M. Veenhuis,et al.  Adhesive knob formation by conidia of the nematophagous fungusDrechmeria coniospora , 1992, Antonie van Leeuwenhoek.

[19]  R. Nicholson,et al.  Mycosporine-alanine: A self-inhibitor of germination from the conidial mucilage of , 1992 .

[20]  J. Schnürer,et al.  Volatile metabolites and other indicators of Penicillium aurantiogriseum growth on different substrates , 1990, Applied and environmental microbiology.

[21]  M. Raimbault,et al.  Germination of concentrated suspensions of spores from Aspergillus niger , 1989, Biotechnology Letters.

[22]  D. J. Weber,et al.  The Fungal Spore: Form and Function , 1976 .

[23]  E Kaminski,et al.  Volatile Flavor Compounds Produced by Molds of Aspergillus, Penicillium, and Fungi imperfecti. , 1974, Applied microbiology.

[24]  B. T. Lingappa,et al.  A self-inhibitor of protein synthesis in the conidia of Glomerella cingulata , 1973, Archiv für Mikrobiologie.

[25]  S. Steele Self-inhibition of arthrospore germination in Geotrichum candidum. , 1973, Canadian journal of microbiology.

[26]  A. Sussman,et al.  Effects of the self-inhibitor of Dictyostelium discoideum on spore metabolism. , 1973, Journal of general microbiology.

[27]  D. Cronin,et al.  The characterisation of some mushroom volatiles , 1971 .

[28]  R. Staples,et al.  Identification of the Germination Self-Inhibitor from Wheat Stem Rust Uredospores , 1971, Science.

[29]  R. Holtz,et al.  Lipid metabolism ofAgaricus bisporus (Lange) sing.: I. Analysis of sporophore and mycelial lipids , 1971, Lipids.

[30]  L. Vining,et al.  Coumarins and phenolic acids in the uredospores of wheat stem rust. , 1957, Canadian Journal of Microbiology (print).

[31]  M. Garrett,et al.  A stable inhibitor of spore germination produced by fungi , 2004, Archiv für Mikrobiologie.

[32]  K. Gull,et al.  The identification of a self-inhibitor from Syncephalastrum racemosum and its effect upon sporangiospore germination , 2004, Antonie van Leeuwenhoek.

[33]  J. Dijksterhuis,et al.  Food and Crop Spoilage on Storage , 2002 .

[34]  W. L. Meyer,et al.  Isolation, purification, and biological activity of a self-inhibitor from conidia of Colletotrichum gloesporioides , 1985 .

[35]  D. Gottlieb Endogenous Inhibitors of Spore Germination , 1973 .