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Differentiation and Pathogenicity Within the Saprolegniaceae

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Differentiation and Pathogenicity Within the Saprolegniaceae Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 680 _____________________________ _____________________________ Differentiation and Pathogenicity within the Saprolegniaceae Studies on Physiology and Gene Expression Patterns in Saprolegnia parasitica and Aphanomyces astaci BY GUNNAR ANDERSSON ACTA UNIVERSITATIS UPSALIENSIS UPPSALA 2001 Dissertation for the Degree of Doctor of Philosophy in Physiological Mycology presented at Uppsala University in 2002 Abstract Andersson, M. G. 2001. Differentiation and Pathogenicity within the Saprolegniaceae. Studies on Physiology and Gene Expression Patterns in Saprolegnia parasitica and Aphanomyces astaci. Acta Universitatis Upsaliensis. Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 680, 41 pp. Uppsala. ISBN 91-554-5203-5. Saprolegnia parasitica and Aphanomyces astaci are parasitic water moulds belonging to the Oomycetes. Despite their importance as parasites they are very little studied at the molecular level and the work described in this thesis was aimed at increasing the molecular knowledge of these organisms by cloning and characterising genes of potential importance for reproduction and pathogenicity. Stage-specific transcripts from Saprolegnia parasitica were isolated by differential display RT-PCR. One of the markers, puf1 encodes a putative mRNA binding protein which may be involved in post-transcriptional regulation of gene expression. S. parasitica puf1 is expressed exclusively in spore cysts that have not been determined for germination or repeated zoospore emergence indicating that the cyst stage has two phases, of about equal duration, which are physiologically and transcriptionally distinct. A similar expression pattern is observed in Aphanomyces spp. with different regulation of spore development and in the transcript is detected in both primary and secondary cysts. A putative chitinase AaChi1, was cloned from the crayfish plague fungus, Aphanomyces astaci. Analysis of chitinase activity and AaChi1 expression showed that chitinase in A. astaci is constitutively expressed in growing and sporulating mycelia, but absent in zoospores, a pattern which reflects the infectious life cycle of A. astaci. This expression pattern is conserved between the four known genotypes of A. astaci, in contrast to saprophytic and fish-pathogenic Aphanomyces spp. Genetic and physiological analysis were conducted on five strains of Aphanomyces, isolated from suspected outbreaks of crayfish plague in Spain and Italy. The strains are not virulent against freshwater crayfish, and RAPD PCR and ITS sequence analysis show that they are unrelated to the crayfish plague fungus, A. astaci. M. Gunnar Andersson, Department of Comparative Physiology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18A, SE-752 36, Uppsala, Sweden © 2001 M. Gunnar Andersson ISSN 1104-232X ISBN 91-554-5203-5 Printed in Sweden by Uppsala University, Tryck & Medier, Uppsala 2001 Till Mahsa Preface The thesis is based on the following papers, which will be referred to by their Roman numerals: I. Andersson, M. G. and Cerenius, L. (2002). Pumilio homologue from Saprolegnia parasitica specifically expressed in undifferentiated spore cysts. Eukaryotic Cell, in press. II. Andersson, M. G. and Cerenius, L. (2002). Comparison of pufI expression in Aphanomyces spp. with different regulation of germination. (in manuscript). III. Andersson, M. G. and Cerenius, L. (2002). Analysis of chitinase expression in the crayfish plague fungus, Aphanomyces astaci. (Submitted) IV. Royo, F., Andersson, G., Bangyeekhun, E., Cerenius, L., Múzquiz, J. L. and Söderhäll, K. (2002). Physiological and Genetic Characterisation of some Aphanomyces Strains Isolated from Freshwater Crayfish. (in manuscript) The manuscript I was reproduced with the permission from the American Society for Microbiology. © 2001 American Society for Microbiology 4 Contents Abstract 2 Preface 4 Table of contents 5 Abbreviations 6 Introduction 7 Background 8 Parasitic fungi 8 Oomycetes 9 Zoospores 10 Mechanisms of infection 12 Host response to fungi 15 Molecular mechanisms of parasitic adaptations 16 Results and discussion 18 Identification of stage specific transcripts (I). 18 A putative RNA binding protein (II) 21 puf1 is specific for undifferentiated cysts (I,II) 24 puf1 in species with other regulation of germination (II) 24 Chitinase in the crayfish plague fungus, A. astaci (III,IV). 25 New Aphanomyces strains from dead crayfish (IV). 28 Conclusions 29 Acknowledgements 31 References 32 5 Abbreviations AaChi1 A. astaci chitinase 1 CSP Conserved sequence flanking Puf-repeats ddRT-PCR Differential display RT-PCR Ef-1 Elongation factor 1 EST Expressed sequence tag FBF fem-3 binding factor IpiO In planta induced "O" ITS Internal transcribed spacer LPS Lipopolysaccharide mst Mycelium specific transcript NAG N-acetylglucoseamine NRE Nanos responsive element PCR Polymerase chain reaction PkaC Protein kinase C PME Point mutation element ProPO Prophenoloxidase Puf-family/protein Pumilio and FBF family/protein. Puf1 Saprolegnia parasitica Puf like protein 1. RAPD Random amplification of polymorphic DNA RT-PCR Reverse trancription PCR. SAPS Secreted aspartyl proteases SAR Systemic aquired response sst Spore specific transcript UTR Untranslated region of mRNA 6 Introduction Saprolegnia parasitica and Aphanomyces astaci are pathogenic water molds, belonging to the oomycete family Saprolegniaceae. Despite their importance as pathogens on plants and animals Oomycetes have been little studied at the molecular level and the work presented in this thesis is aimed to increase the knowledge of the molecular biology of these organisms. The main, and often only, infectious stage of these organisms is the asexually formed zoospore, and by studying gene expression in the zoospore we hoped to identify transcripts of potential importance for reproduction and pathogenicity. We used differential display RT-PCR to identify transcripts specific for the zoospore and mycelium stages of S. parasitica. One of the identified transcripts, puf1, encodes a putative mRNA binding protein, and is specifically expressed in encysted zoospores. Another approach for studying pathogenesis is to study genes encoding enzymes of potential importance for the infection process. Using PCR with primers based on conserved chitinase domains a putative chitinase was cloned from the crayfish plague fungus, A. astaci, and the expression of this transcript was analysed under different growth condition and during different stages of the life cycle. This work also includes a genetical and physiological study of five strains of Aphanomyces, which had been isolated from freshwater crayfish in Spain and Italy. 7 Background Parasitic fungi The question what makes a fungus or another microorganism, a parasite or a pathogen is not simple, and there are multiple definitions of virulence and pathogenicity (Casadevall & Pirofski 1999). What adaptations will result in a successful parasitic life, why will a fungus be a pest on one host while it is harmless on another, often closely related host and how can a strain considered to be an opportunist, endophyte or saprophyte turn out to be a pathogen when brought into a new environment? Several attempts have been done to address these questions, in different host pathogen systems. In some cases mechanisms have been found that are unique to a particular host- parasite system, and maybe even attributed to a single gene. It may be the presence or absence of a gene product that is recognised by receptors in the host (Dangl & Holub 1997), the production of a potent toxin (Vilcinskas & Götz 1999a), or a gene product that inactivates the defence of the host (Vilcinskas & Götz 1999a). Adaptations to parasitism could also be more general treats that cannot easily be attributed to a single gene, such as adaptations in the regulation of life cycle or development or the formation of lytic enzymes. The interaction may often be a balance of offensive and defensive actions, so that a fungus producing the optimal mix of degrading enzymes, toxins etc may be virulent against one host because it is so optimised that it can successfully establish an infection, while it fails to infect a related species or cultivar. In such a case it will be almost impossible to correlate virulence with a particular gene (Schulz et al. 1999). 8 Oomycetes Not all classes of fungi-like pathogens belong to the kingdom fungi. One of these groups is the oomycetes. This group comprises severe pests, like Phytophthora infestans (Judelson 1997, Tyler 2001) causing the potatoe late blight, A. astaci (Cerenius et al. 1988), causing crayfish plague and several fish pathogens from genera Aphanomyces, Achlya, and Saprolegnia (Cerenius & Söderhäll 1996). There is also at least one species with the potential of infecting humans, namely Pythium insidiosum (de Cock et al.1987; Mendoza et al. 1993). Oomycetes are placed within the kingdom Chromista together with for example brown algae. The Oomycetes are subdivided in orders (Fuller 1987). One being the Peronosporales comprising for example Phytophthora spp which are parasites on among others potato and tomato, and Peronospora. The Peronosporales often infect land living plants. Another order is the Saprolegniales, a group of water molds that are common in aquatic environments both as saprophytes and parasites on fish and crustaceans (Cerenius & Söderhäll 1996). The Saprolegniales also comprise specialised
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