FUNGI AND FOOD SPOILAGE

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FUNGIAND FOOD SPOILAGE Second edition

J.I. Pitt Chief Research Scientist CSIRO Division of Food Science and Technology North Ryde, New South Wales Australia

and

A.D. Hocking Principal Research Scientist CSIRO Division of Food Science and Technology North Ryde, New South Wales Australia

IUI'I SPRINGER-SCIENCE+BUSINESS MEDIA, B.V.

First edition 1985 published by Academic Press, Sydney

Second edition 1997

© 1997 J.I. Pitt and A.D. Hocking

ISBN 978-1-4613-7936-2 ISBN 978-1-4615-6391-4 (eBook) DOI 10.1007/978-1-4615-6391-4

Apart from any fair dealing for the purposes ofresearch or private study, or criticism or review, as permitted under the UK Copyright Designs and Patents Act, 1988, this publica­tion may not be reproduced, stored, or transmitted, in any form or by any means, without the prior permission in writing of the publishers, or in the case of reprographic reproduc­tion only in accordance with the terms of the licences issued by the Copyright Licensing Agency in the UK, or in accordance with the terms oflicences issued by the appropriate Reproduction Rights Organization outside the UK. Enquiries concerning reproduction outside the terms stated here should be sent to the publishers at the London address printed on this page.

The publisher makes no representation, express or implied, with regard to the accuracy of the information contained in this book and cannot accept any legal responsibility or liability for any errors or omissions that may be made.

A catalogue record for this book is available from the British Library

§ Printed on permanent acid-free text paper, manufactured in accordance with ANSIJNISO Z39.48-1992 and ANSIJNISO Z39.48-1984 (Permanence ofPaper).

Contents

Preface to the First Edition

Preface to the Second Edition

List of Keys for Identification

List of Tables

1. Introduction

2. The Ecology of Fungal Food Spoilage

2.1 Water Activity 2.2 Hydrogen Ion Concentration 2.3 Temperature 2.4 Gas Tension 2.5 Consistency 2.6 Nutrient Status 2.7 Specific Solute Effects 2.8 Preservatives 2.9 Conclusions: Food Preservation

3. Naming and Classifying Fungi

3.1 Taxonomy and Nomenclature: Biosystematics 3.2 Hierarchical Naming 3.3 Zygomycotina 3.4 Ascomycotina and Deuteromycotina 3.5 The Ascomycete-Deuteromycete Connection 3.6 Dual Nomenclature 3.7 Practical Classification of Fungi

4. Methods for Isolation, Enumeration and Identification

4.1 Sampling 4.2 Enumeration Techniques 4.3 Sampling Surfaces 4.4 Air Sampling 4.5 Isolation Techniques

v

ix

x

xi

xii

1

3

3 6 6 8 9

10 10 11 11

13

13 14 15 16 18 18 19

21

21 22 25 25 26

4.6 Choosing a Suitable Medium 28 4.7 Estimation of Fungal Biomass 38 4.8 Identification Media and Methods 44 4.9 Examination of Cultures 50 4.10 Preservation of Fungi 53 4.11 Housekeeping in the Mycological Laboratory 55

5. Primary Keys and Miscellaneous Fungi 59

5.1 The General Key 61 5.2 Miscellaneous Fungi 63 Acremonium Link 66 Alternaria Nees: Fr. 67 Arthrinium Kunze 74 Aureobasidium Viala & G. Boyer 76 Bipolaris Shoemaker 78 Botrytis P. Micheli: Fr. 80 Chaetomium Kunze 81 Chrysonilia Arx 86 Cladosporium Link 87 Colletotrichum Corda 96 Curvularia Boedijn 98 Drechslera S. Ito 101 Endomyces Reess 103 Epicoccum Link 105 Fusarium Link 107 Geotrichum Link: Fr. 144 Hyphopichia Arx & van der Walt 146 Lasiodiplodia Ellis & Everh. 147 Monascus Tiegh. 149 Moniliella Stolk & Dakin 152 Nigrospora Zimm. 155 Pestalotiopsis Steyeart 157 Phoma Sacco 159 Stemphylium Wallr. 161 Trichoconiella B.L. Jain 163 Trichoderma Pers. 165 Trichothecium Link 168 Ulocladium Preuss 170

6. Zygomycetes 173

Absidia Tiegh. 177 Cunninghamella Matr. 178 Mucor P. Micheli: Fr. 180 Rhizomucor (Lucet & Costantin) Yuill. 188 Rhizopus Ehrenb. 189 Syncephalastrum J. Schrot. 198 Thamnidium Link 200

vi

7. Penicillium and Related Genera 203

Byssochlamys Westling 205 Eupenicillium F. Ludw. 211 Geosmithia Pitt 219 Paecilomyces Bainier 220 Scopulariopsis Bainier 224 Talaromyces C.R. Benj. 226 Penicillium Link 234

Penicillium subgenus Aspergilloides Dierckx 237 Penicillium subgenus Furcatum Pitt 251 Penicillium subgenus Penicillium 272 Penicillium subgenus Biverticillum Dierckx 324

8. Aspergillus and Related Teleomorphs 339

Emericella Berk. 344 Eurotium Link: Fr. 347 Neosartorya Malloch & Cain 362 Aspergillus Fr.: Fr. 366

9. Xerophiles 417

Basipetospora G.T. Cole & W.E. Kendr. 419 Chrysosporium Corda 421 Eremascus Eidam 428 Polypaecilum G. Sm. 429 Wallemia Johan-Olsen 432 Xeromyces L.R. Fraser 435

10. Yeasts 439

Brettanomyces bruxellensis Kuff. & van Laer 445 Candida krusei (Castell.) Berkhout 447 Candida parapsilosis (Ashford) Langeron & Talice 448 Debaryomyces hansenii (Zop£) Lodder & Kreger 449 Kloeckera apiculata (Reess) Janke 451 Pichia membranaefaciens E.C. Hansen 453 Rhodotorula mucilaginosa (A. Jorg.) F.C. Harrison 455 Saccharomyces cerevisiae Meyen ex E.C. Hansen 457 Schizosaccharomyces pombe Lindner 459 Torulopsis holmii (A. Jorg.) Lodder 460 Zygosaccharomyces bailii (Lindner) Guillierm 462 Zygosaccharomyces rouxii (Boutroux) Yarrow 465

vii

11. Spoilage of Fresh and Perishable Foods

11.1 Spoilage of Living, Fresh Foods 11.2 Fruits 11.3 Vegetables 11.4 Dairy Foods 11.5 Meats 11.6 Cereals, Nuts and Oilseeds

12. Spoilage of Stored, Processed and Preserved Foods

12.1 Low Water Activity Foods: Dried Foods 12.2 Low Water Activity Foods: Concentrated Foods 12.3 Low Water Activity Foods: Salt Foods 12.4 Intermediate Moisture Foods: Processed Meats 12.5 Heat Processed Acid Foods 12.6 Preserved Foods 12.7 Cheese

Media Appendix

Glossary

References

Subject Index

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469

469 470 477 479 481 481

489

489 498 502 503 504 504 505

509

515

517

577

Preface to the First Edition

This book is designed as a laboratory guide for the food microbiologist, to assist in the isolation and identification of common food-borne fungi. We emphasise the fungi which cause food spoilage, but also devote space to the fungi commonly encountered in foods at harvest, and in the food factory. As far as possible, we have kept the text simple, although the need for clarity in the descriptions has necessitated the use of some specialised mycological terms.

The identification keys have been designed for use by microbiologists with little or no prior knowledge of mycology. For identification to genus level, they are based primarily on the cultural and physiological characteristics of fungi grown under a standardised set of conditions. The microscopic features of the various fungi become more important when identifying isolates at the species level. Nearly all of the species treated have been illustrated with colony photographs, together with photomicrographs or line drawings. The photomicrographs were taken using a Zeiss WL microscope fitted with Nomarski interference contrast optics. We are indebted to Mr W. Rushton and Ms L. Burton, who printed the many hundreds of photographs used to make up the figures in this book.

We also wish to express out appreciation to Dr D.L. Hawksworth, Dr A.H.S. Onions and Dr B. C. Sutton of the Commonwealth Mycological Institute, Kew, Surrey, u.K., Professor P.E. Nelson and the staff of the Fusarium Research Center, University of Pennsylvania, U.S.A., and Dr L.W. Burgess of The University of Sydney, who generously provided facilities, cultures and advice on some of the genera studied.

ix

Preface to the Second Edition

In planning for a second edition of "Fungi and Food Spoilage", we decided that the book would benefit from a larger format, which would permit improved illustrations, and from some expansion of the text, in both numbers of species treated and overall scope. These aims have been realised. The Crown Quarto size has allowed us to include substantially larger, clearer illustrations. Many new photographs and photomicrographs have been added, the latter taken using a Zeiss Axioscop microscope fitted with Nomarski differential interference contrast optics. We have taken the opportunity to include more than 40 additional species descriptions, to add a new section on mycotoxin production for each species, and to update and upgrade all of the text.

Since the first edition, changes in the climate for stabilising fungal nomenclature have resulted in development of a list of "Names in Current Use" for some important genera, including Aspergillus and Penicillium. Names of species used in the second edition are taken from that list, which was given special status by the International Botanical Congress, Tokyo, 1994. Names used in this edition have priority over any other names for a particular species. Publication of a list of "Authors of Fungal Names" (P.M. Kirk and A.E. Ansell, Index of Fungi, Supplement: 1-95, 1992), has also stabilised names of authorities for all fungal species. Abbreviations of authors' names used in this edition conform to those recommended by Kirk and Ansell. Some progress in standardi­sation of methods and media has also been made, primarily through the efforts of the International Commission on Food Mycology.

The first edition included some 400 references. When we began revisionary work, we felt that the number of references in the area of food mycology had probably doubled or increased by perhaps 150% during the intervening years. In fact this second edition includes over 1900 references, almost a 5 fold increase over the 1985 edition! This provides a clear indication that interest in, and study of, food mycology has greatly increased in recent years. Modern referencing systems have enabled us to expand information from tropical sources, especially Asia and Africa, but we are conscious of the fact that treatment of fungi found in foods on a world wide basis remains rather incomplete.

We gratefully acknowledge support and assistance from colleagues who have contributed to this new edition. Ms J.C. Eyles formatted and printed the camera ready copy, Ms C. Heenan collated, arranged and formatted the illustrations, and Mr N.J. Charley looked after the culture collection, culture growth and colony photography. Without this level of support the book could not have been completed.

x

List of keys for identification

General key to food spoilage fungi Key to miscellaneous genera

Key to Alternaria species included here Key to Chaetomium species included here Key to Cladosporium species included here Key to Curvularia species included here. Key to Fusarium species included here Key to Moniliella species included here

Key to genera of Mucorales included here Key to Mucor species included here Key to Rhizopus species included here

Key to genera producing penicilli Key to teleomorph genera producing anamorphs with penicilli

Key to Byssochlamys species included here Key to Eupenicillium species included here Key to Geosmithia species included here Key to Paecilomyces species included here Key to Talaromyces species included here

Key to subgenera of Penicillium Key to Penicillium sub gen. Aspergilloides species included here Key to Penicillium subgen. Furcatum species included here Key to Penicillium sub gen. Penicillium species included here Key to Penicillium subgen. Biverticillium species included here

Key to Aspergillus species and teleomorphs included here Key to Eurotium species included here

Key to Xerophilic fungi Key to xerophilic Chrysosporium species Key to spoilage yeasts

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61 64 69 82 88 98

110 152 176 181 190 204 204 205 212 220 222 228 237 238 252 276 325 342 348 418 422 444

List of Tables

2.1 Water activity and microbial water relations in perspective 2.2 Comparative heat resistances of ascospores and conidia 4.1 Recommended media for fungal detection, enumeration

and isolation 7.1 Characteristics distinguishing subgenus Furcatum from

subgenus Biverticillium 7.2 Responses of common species of Penicillium subgenus Penicillium

to Neutral Creatine Sucrose agar (CSN) after incubation for 7 days at 25°C

8.1 Colony diameters expected for Aspergillus species and teleomorphs 10.1 Spoilage yeasts 10.2 Media and conditions for identification of spoilage yeasts 10.3 Salient properties of yeasts

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5 8

30

236

274 343 441 442 443