Caballero B. (ed.) Encyclopaedia of Food Science, Food Technology and Nutrition. Ten-Volume Set

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Alternaria

0026 Species of Alternaria occur worldwide on many foods

and plant materials. They have septate hyphae and

appear to be dark, gray-green in color, and almost

black on the reverse side of colonies growing on agar.

They produce septate conidia which are also dark-

colored (Figure 4). The septa are both transverse and

longitudinal, and spores are oblong in shape, some-

times with an elongated apical cell. The spores are

produced in chains. Alternaria can cause spoilage of a

variety of foods, including tomatoes and fresh vege-

tables, such as bell peppers. Alternaria species have

been found in the core area of apples, in nuts, includ-

ing peanuts, hazelnuts, and pecans, in grains such as

wheat and sorghum, and in cold-stored meat and

spices. Alternaria are capable of growing at low tem-

peratures on refrigerated foods. Common species in-

clude A. alternata, which is considered synonymous

with A. tenuis,andA. tenuissima. Alternaria species

are capable of producing several mycotoxins and thus

present both food spoilage and potential safety

hazards.

Trichothecium

0027Trichothecium is a common genus of mold which

occurs throughout the world. A common species is

T. roseum, which is pink in color, and has been found

growing on various fruits and vegetables, as well as

cereal grains, such as barley, wheat, and corn, and

cereal products such as flour. It has also been found

on beans, pecans, filberts, and meat. Trichothecium

species produce clusters of two-celled or single-

septate conidia that are elliptical to pear-shaped.

Some strains of Trichothecium have been shown to

produce trichothecenes.

Trichoderma

0028Two of the most common species of Trichoderma are

T. viride and T. harzianum. Trichoderma colonies

are bright green. Trichoderma contaminate many

food products, including stored grains such as barley,

wheat, and oats, nuts such as peanuts and pecans, and

various fruits and vegetables, such as tomatoes, sweet

potatoes, and citrus fruit.

Cladosporium

0029Cladosporium has dark mycelia which may be brown

to blackish-brown or gray-green in color. The reverse

side of a colony of Cladosporium on agar is very dark

greenish-black or blue-black. Cladosporium species

produce many one-celled conidia, but two- and

three-celled forms are also common. Two common

species are C. cladosporioides and C. herbarum. Cla-

dosporium species, which can grow at low tempera-

tures, tend to be slow-growing and form black spots

on foods. Cladosporium species have been isolated

from cereal grains, peanuts, fruits, and refrigerated

meat, particularly beef. Cladosporium is very common

and can grow under refrigerated storage conditions.

The main consequence of Cladosporium species in

foods is spoilage and discoloration.

Geotrichum

0030Geotrichum has septate mycelia which readily frag-

ment into arthrospores (Figure 5), which are the

organism’s primary means of reproduction. The only

species that is significant in foods is G. candidum;

other names for this organism are Oidium lactis

and Oospora lactis; it produces ascospores, and the

fig0004 Figure 4 Multicelled conidia of Alternaria with transverse and

longitudinal septa. Reproduced from Spoilage: Fungi in Food –

An Overview. Encyclopaedia of Food Science, Food Technology and

Nutrition, Macrae R, Robinson RK and Sadler MJ (eds), 1993,

Academic Press.

SPOILAGE/Fungi in Food – An Overview 5517

telemorphic state is known as Endomyces geotri-

chum. G. candidum is referred to as a yeast-like

fungus because it exhibits a dimorphic form and

readily fragments into arthrospores, which appear to

be single-celled. In addition, colonies of this organism

can be white, soft, creamy, and yeast-like in appear-

ance. G. candidum is a problem on food-processing

equipment, particularly in vegetable-processing

plants, and is referred to as ‘machinery mold.’

Unclean equipment provides a favorable environment

for rapid growth of this organism. It attacks citrus

fruits, as well as other fruits. It is able to infect fruits

mainly through injuries to the skin, as well as growing

on overripe fruit. G. candidum has also been obtained

from cheese, meats, and frozen foods, particularly

vegetables.

Rhizopus

0031 Rhizopus differs from the molds previously described,

because it is nonseptate and produces sporangio-

spores rather than conidia. It is a very-fast-growing,

spreading type of mold which has white mycelia and

black sporangia. Rhizopus species form rhizoids at

the base of the sporangiophores, and columella in the

sporangium (Figure 6). Young sporangia are white

before turning black with age. Probably the most

common of the Rhizopus species is R. stolonifer, the

so-called bread mold. Besides bread, Rhizopus causes

spoilage of strawberries, other berries, fruits, and

vegetables. Rhizopus species have also been isolated

from cereal grains, nuts, and meat. R. oligosporus is

used in making tempeh and certain other mold-

fermented foods. Rhizopus is placed in the taxonomic

order Mucorales and is somewhat typical, and prob-

ably the most common genus of that order to contam-

inate foods. Other genera in the order Mucorales

which are nonseptate and produce sporangiospores

are Absidia, Mucor, Rhizomucor, Syncephalastrum,

and Thamnidium. All of the Mucorales genera

that contaminate food are found in the family

Mucoraceae. These genera are sometimes referred

to as mucoraceous fungi. They are a part of the

fig0005 Figure 5 Arthrospores typical of Geotrichum. Reproduced from

Spoilage: Fungi in Food – An Overview. Encyclopaedia of Food

Science, Food Technology and Nutrition, Macrae R, Robinson RK

and Sadler MJ (eds), 1993, Academic Press.

fig0006Figure 6 Sporangiospore typical of Rhizopus and other mucor-

aceous fungi. Reproduced from Spoilage: Fungi in Food – An

Overview. Encyclopaedia of Food Science, Food Technology and Nu-

trition, Macrae R, Robinson RK and Sadler MJ (eds), 1993, Aca-

demic Press.

5518 SPOILAGE/Fungi in Food – An Overview

class Zygomycetes and form zygospores by sexual

processes and chlamydospores (Figure 7). They re-

quire high-moisture conditions for growth.

0032 For more detailed descriptions of these and other

genera of molds, refer to the references given in the

Further Reading Section at the end of this article.

Recognizing Molds

0033 Molds are recognized primarily as visible fuzzy, cot-

tony, or colored growth on the surfaces of substrates

such as foods or other organic materials. In grains,

seeds, and animal feeds, however, such growth may

not always be visible in this manner. Internal mold

contamination and growth in nuts, seeds, and grains

may not always be visible as filamentous growth.

However, mold growth in nuts, whole grains or

seeds often results in discoloration and altered ap-

pearance. In corn (including popcorn), for example,

invasion and growth of mold in the germ area

may produce darkened, greenish- or blueish-colored

germ areas in affected kernels. When this growth is

attributable to certain blue-colored Aspergillus or

Penicillium species, and a blueish line appears in

the germ area, the condition is known as ‘blue eye.’

In other grains, such as wheat, white to pinkish

discolored and shrivelled kernels may indicate mold

invasion. Likewise, with nuts, shrivelled or misshapen

kernels may be caused by mold, although that is not

the only cause of such problems.

Health Implications

0034Mold deterioration of foods and agricultural com-

modities is a serious problem worldwide. Besides

deterioration of food and feed products by causing

damage that reduces quality, grades, and prices,

resulting in economic loss, the presence of molds in

foods and commodities poses hazards to human and

animal health. A serious hazard associated with mold

growth in foods and feeds is the possible production

of mycotoxins – substances which are toxic and some

of which are carcinogenic. (See Aflatoxins; Myco-

toxins: Classifications.) Additional hazards arise

from the presence of the molds themselves. A wide

spectrum of human and animal diseases are attribut-

able to molds, ranging from mycotic abortion to afla-

toxin poisoning in animals, and from allergic

reactions to life-threatening systemic infections in

humans. In recent years, invasive mycoses have

become a more frequent and important cause of mor-

bidity and mortality in humans, particularly in indi-

viduals who are immunosuppressed as a result of

organ transplantation, underlying disease (acquired

immune deficiency syndrome or AIDS), chemother-

apy, radiation therapy, or age. The environment, in-

cluding foods, is the source of these molds. Certain

occupational niches, such as grain handling and stor-

age, pose additional hazards to agricultural workers

through exposure to high levels of mold spores and

endotoxins in grain dusts. These dusts may also be a

significant source of exposure to mycotoxins. Various

lung diseases in grain handlers, farmers, and food-

producing animals are associated with molds and

grain dust.

Yeasts

0035Yeasts are single-celled microscopic organisms that

are larger than bacteria, and are oval, elliptical, spher-

ical, or elongated into rod shapes. Most yeasts repro-

duce by a process called budding (Figure 8). Budding

is an asexual process in which a bulge (bud) develops

on the cell wall, and protoplasm, including replicated

nuclear material, fills the bulge. The bulge grows in

size and eventually a wall forms between the bulge

and the parent cell, forming a new cell. The new cell

then separates from the parent cell. Buds may form in

(a) (b)

fig0007 Figure 7 (a) Zygospore and (b) chlamydospores. Reproduced

from Spoilage: Fungi in Food – An Overview. Encyclopaedia of

Food Science, Food Technology and Nutrition, Macrae R, Robinson

RK and Sadler MJ (eds), 1993, Academic Press.

SPOILAGE/Fungi in Food – An Overview 5519

a polar position or multilaterally. Some yeasts repro-

duce by binary fission, similar to fission in bacteria,

but these are few in number. One yeast reproduces by

both fission and budding. So-called true yeasts also

reproduce by a sexual process involving conjugation

of two cells and the resultant formation of ascospores

within the cells. The cell containing ascospores is then

known as an ascus. A few yeasts produce ascospores

without conjugation, but the resulting ascospores

then undergo conjugation. True yeasts are referred

to as ascosporogenous yeasts and are classified in

the subdivision Ascomycotina, which used to be

called Ascomycetes. Asporogenous yeasts, also called

false yeasts, do not produce ascospores or other

sexual spores, and are placed in the subdivision Deu-

teromycotina, also called Fungi Imperfecti.

0036 Another type of spore formed by some yeasts is

called a chlamydospore. A chlamydospore forms

when a thick wall surrounds the yeast cell, and is

similar to chlamydospores formed by molds. These

appear to be resting or survival structures, and are

asexual. Yeasts that form pseudomycelia can also

produce by fragmentation spores known as arthro-

spores and blastospores.

Growth Requirements

0037 Individual yeasts vary in their growth requirements,

but some generalizations can be made. Yeasts are

aerobic and facultatively anaerobic. Some yeasts

are extremely aerobic and oxidative in their metabol-

ism. These oxidative yeasts grow on the surface of

liquids and are known as film yeasts. Yeasts that are

aerobic and facultatively anaerobic can grow both

ways. When growing aerobically, yeasts produce

mainly biomass, i.e., more yeast cells. When growing

anaerobically, yeasts have a fermentative metabolism

and produce carbon dioxide and ethanol. For the

most part, sugars are the best source of energy for

yeasts, but the film yeasts can oxidize organic acids

and alcohol for energy. Yeasts can utilize simple ni-

trogen compounds, such as ammonia, urea, and

amino acids. Some yeasts can also hydrolyze proteins

and polypeptides.

0038Yeasts require somewhat less available moisture

than bacteria, but more than molds. In terms of a

the lower limits for most yeasts are 0.88–0.94. Some

yeasts, known as osmophilic yeasts, can grow in the

presence of high concentrations of sugars or salt at a

as low as 0.62–0.65. Each yeast will have its own

characteristic optimal a

and a range of a

over

which it can grow. The minimum and optimum a

for a given yeast may change depending on outside

factors, such as nutrition, pH, temperature, oxygen,

and presence of inhibitors.

0039The optimum temperature for growth of yeasts is

in the mesophilic range of 25–30



C. Yeasts in general

can grow over a range of temperatures from 0



Cto



C. Yeasts grow well under acid conditions, at pH

4.0–4.5. They can grow at lower pH than most bac-

teria, but do not grow well under alkaline conditions.

Yeasts are widely distributed in nature and commonly

occur on grapes and other fruits. They are also found

in dust and water, and may be found on the skin and

in the intestinal tract of humans and animals.

Food Spoilage and Effects of Processing

on Yeasts

0040Some yeasts, mostly in the genus Saccharomyces, are

very important industrially for leavening of bread

and production of wine, beer, alcohol, glycerol,

and invertase. Other yeasts, referred to as wild yeasts,

can cause spoilage problems in foods. Film yeasts can

oxidize enough lactic acid to allow spoilage in sauer-

kraut and pickle fermentations by nonacid-tolerant

organisms. Yeasts can grow in vacuum-packaged

wieners and other cured meats, forming visible col-

onies or slime. Other salt-tolerant yeasts can grow in

curing brines, salted meats and fish, soya sauce,

tamari sauce, and miso. Osmophilic yeasts can grow

well in foods with high concentration of solutes, es-

pecially sugars and salts, and cause spoilage of salad

dressings, honey, syrups, concentrated fruit juices,

and even dried fruits. Certain other yeasts, known

as apiculate or lemon-shaped yeasts, can contaminate

wine fermentations, causing off-flavors, low yields of

alcohol, and production of volatile acids. Yeasts can

also reach high numbers in frozen vegetables prior to

freezing or after thawing, especially if the vegetables

are mishandled.

0041Yeasts are not heat-resistant and are readily des-

troyed in most heat processes. Other food processes,

such as freezing, refrigeration, vacuum packaging,

and acidification, will not necessarily destroy yeasts.

Vacuum packaging will prevent growth of highly

aerobic film yeasts, but not of fermentative types.

Lower pH will not necessarily prevent the growth

of yeasts, but organic acids may prevent growth of

fig0008 Figure 8 Diagrammatic representation of budding in a typical

yeast cell. Reproduced from Spoilage: Fungi in Food – An Over-

view. Encyclopaedia of Food Science, Food Technology and Nutrition,

Macrae R, Robinson RK and Sadler MJ (eds), 1993, Academic

Press.

5520 SPOILAGE/Fungi in Food – An Overview

some yeasts. Sorbic acid and sorbates are particularly

effective in preventing yeast growth. Sulfur dioxide

can be used to kill wild-type yeasts in dried fruits and

in grapes for wine-making. Heating of dried fruits in

the package can also be used to kill yeasts and pas-

teurize the fruit.

Specific Genera of Yeasts

0042 There are a number of genera of yeasts that are im-

portant in foods. These include both beneficial and

harmful types. The following is a synopsis of 10

genera of yeasts that include the most important in-

dustrial yeast, and various spoilage yeasts, including

osmophilic yeasts, film yeasts, and asporogeneous

yeasts.

Saccharomyces

0043 Saccharomyces is the most important genus from an

industrial standpoint. The main species is S. cerevisiae

and different strains of it are used in many food indus-

tries for leavening bread and making ales, beer, wine,

alcohol, and other products. It has also been used to

produce single-celled protein, and food ingredients

such as autolyzed yeast. It is probably the single

most important yeast known. S. cerevisiae cells are

elliptical to ovoid in shape, with some spherical and

elongated cells as well. They reproduce by budding,

and form ascospores. S. cerevisiae can also cause

spoilage under certain conditions where its fermenta-

tive activity is not desired.

Zygosaccharomyces

0044 Zygosaccharomyces is considered to be a subgenus of

Saccharomyces, and some authors have reclassified

this genus as Saccharomyces. The yeasts in this

genus are osmophilic and can grow in high concen-

trations of sugar. They are responsible for spoilage of

molasses, syrups, honey, salad dressing, soya sauce,

and wine. They reproduce by budding, and form

ascospores.

Schizosaccharomyces

0045 Schizosaccharomyces species are found in sugar, mo-

lasses, honey, tropical fruit, and soil. They reproduce

by fission, forming arthrospores, or by sexual means,

forming ascospores. There are either four or eight

ascospores per ascus. The spores are oval, spherical,

or kidney-shaped.

Debaryomyces

0046 Yeasts in the genus Debaryomyces are film yeasts,

and they form pellicles of surface growth on meat

brines. They also grow on cheese and sausage

products. The cells of Debaryomyces are round to

oval-shaped and they form ascospores. They may

also form pseudomycelia.

Hansenula

0047Yeasts in the genus Hansenula are also film yeasts.

They are common in olive brines, fruit juice concen-

trates, citrus fruits, and grapes. Although they are

film yeasts that form pellicles, they are somewhat

fermentative. They produce spherical to oval elong-

ated cells. They reproduce by budding and by forming

ascospores. The ascospores have a characteristic

shape, similar to a bowler hat. They may form

pseudomycelia.

Pichia

0048Yeasts in the genus Pichia are also film yeasts that

form a pellicle on liquids, such as beer and wines.

Cells are oval to cylindrical-shaped and form asco-

spores which are either round or hat-shaped.

Torulopsis

0049The Torulopsis genus may also be called Torula and it

consists of asporogenous yeasts that are round to oval

in shape. They reproduce by budding. These yeasts

are common in nature, and contaminate many foods,

including refrigerated foods. Species of this genus can

ferment lactose and can spoil milk products, such as

sweetened condensed milk, as well as fruit juice

concentrates and acid foods.

Candida

0050Candida species are asporogenous yeasts that form

pseudomycelia or true mycelia. They are sometimes

categorized as Fungi Imperfecti in the family Mon-

iliaceae with other yeast-like genera, particularly

Trichothecium and Geotrichum. They reproduce by

budding and fragmentation of the mycelia into

blastospores. Members of this genus are common

in foods and occur in fresh meat, such as ground

beef, cured meats, and butter and margarine. They

can spoil foods high in acid and salt, and the lipo-

lytic species C. lipolytica can cause rancidity of

butter and margarine. Other species have been

grown for food and feed. At least one species, C.

albicans, is responsible for infections in humans and

animals.

Trichosporon

0051Trichosporon species are asporogenous yeasts that

reproduce by budding and form arthrospores. They

grow at lower temperatures and can be found in

many foods, including chilled beef, beer, and maple

sap.

SPOILAGE/Fungi in Food – An Overview 5521

Rhodotorula

0052 Yeasts in the genus Rhodotorula are sporogenous and

reproduce by budding. They sometimes also from

pseudomycelia. These organisms are widespread in

nature, often found in air and dust, and contaminate

many foods. They produce red, yellow, and pink pig-

ments and often discolor foods with red and yellow

spots on meats, particularly cured meats, and pink

areas in sauerkraut.

Health Implications

0053 Yeasts are generally not associated with foodborne

illnesses, but certain yeasts can cause infections in

humans and animals. Probably the most common

infection caused by a yeast is candidiasis, caused by

C. albicans. This organism is a common inhabitant of

the mucous membranes of the mouth, vaginal canal,

and intestinal tract. Yeast infections can occur most

readily in persons receiving broad-spectrum antibi-

otic therapy and those who are immunocomprom-

ised. In the immunocompromised subjects, Candida

species and other yeasts can cause endocarditis, urin-

ary infections, kidney infections, esophageal infec-

tions, and septicemia or systemic candidiasis. As the

number of immunocompromised persons increases

from radiation and chemotherapy, AIDS, and simple

aging, it remains to be seen if foodborne yeasts may

become a problem for these individuals as opportun-

istic infectious agents.

See also: Aflatoxins; Antibiotics and Drugs: Uses in

Food Production; Cereals: Dietary Importance; Cheeses:

Chemistry and Microbiology of Maturation; Controlled-

atmosphere Storage: Applications for Bulk Storage of

Foodstuffs; Essential Oils: Properties and Uses;

Fungicides; Lactic Acid Bacteria; Mushrooms and

Truffles: Classification and Morphology; Mycotoxins:

Classifications; Occurrence and Determination;

Toxicology; Water Activity: Effect on Food Stability;

Yeasts

Further Reading

Bullerman LB (2000) Mold Growth in Bakery Products and

its Prevention. AIB Technical Bulletin, vol. XXII, issue 5.

Manhattan, KS: American Institute of Baking.

Doyle MP, Beuchat LR and Montville JT (2000) Food

Microbiology: Fundamentals and Frontiers, 2nd edn.

Washington, DC: ASM Press.

Klich MA and Pitt JI (1988) A Laboratory Guide to the

Common Aspergillus Species and Their Telemorphs.

North Ryde, Australia: Commonwealth Scientific and

Industrial Research Organization.

Nelson PE, Toussoun TA and Marasas WFO (1983) Fusar-

ium Species. An Illustrated Manual for Identification.

University Park, Pennsylvania: The Pennsylvania State

University Press.

Northolt MD and Bullerman LB (1982) Prevention of mold

growth and toxin production through control of envir-

onmental conditions. Journal of Food Protection 45:

519–526.

Pitt JI (1988) A Laboratory Guide to Common Penicillium

Species, 2nd edn. North Ryde, Australia: Common-

wealth Scientific and Industrial Research Organization.

Pitt JI and Hocking AD (1999) Fungi and Food Spoilage,

2nd edn. Gaithersburg, MD: Aspen Publishers.

Rhodes M (ed.) (1979) Food Mycology. Boston: GK Hall.

Samson RA, van Reenen-Hoekstra ES, Frisvad JC and Fil-

tenborg O (1996) Introduction to Food-borne Fungi, 5th

edn. Baarn, The Netherlands: Centraalbureau voor

Schimmelcultures.

Molds in Spoilage

F Ottaviani, State University of Bologna, Italy

M G Ottaviani, CONSAL – Advising in Food

Microbiology, Sermide, Italy

Basic Biology of Molds

0001Molds are eukaryotic organisms widely distributed in

nature, and are common contaminants of agricultural

commodities, food, beverages, and feed.

0002In contrast to the simple (prokaryotic) bacteria,

molds are complex organisms whose mycelium is

composed of individual filaments termed hyphae.

The hypha is essentially a tube, consisting of a rigid

wall and containing a moving mass of protoplasm; its

interior is frequently divided into compartments by

cross-walls which, being incomplete or perforated, do

not separate the content into individual cells. This

coenocytic condition gives molds an advantage over

the single-celled bacteria, permitting both a more

efficient distribution of nutrients and a better dilution

of external stresses over a large number of cells. Or-

ganelles inside the hypha are of the eukaryotic type,

i.e., more sophisticated than those of the bacterial

cell. Nuclei and energy-yielding mitochondria are

present.

0003The hyphal wall is predominantly composed of

polysaccharides which give the molds a more defined

barrier against environmental stress.

0004Chitin, a polymer of N-acetyl-d-glucosamine, is

the more frequently occurring polymer in the walls

of fungal spores and mycelia and it does not exist in

bacteria or most uncontaminated food and feed prod-

ucts. Glycoproteins such as galactomannan are either

5522 SPOILAGE/Molds in Spoilage

extracellular or bound to the fungal cell wall. Ergos-

terol is considered the principal sterol of fungi and

plays an important role in cell membranes.

0005 All these specific components of fungi are used to

estimate fungal activity by rapid chemical, biochem-

ical, and immunological methods even when fungal

biomass may have been killed, given that chitin and

fungal polysaccharidic antigens are heat-resistant and

they can survive after the death of fungal species.

0006 Because of their peculiar structure, molds behave in

a different way from bacteria, with regard both to

food preservation technologies and to laboratory

analytical techniques – they have better control of

ionic homeostasis (with regard to pH and water ac-

tivity (a

)), and insensitivity to antibiotics commonly

used to repress bacterial growth.

0007 With generation times ranging between 2 and 5 h,

fungal hyphae extend at their apices with their oldest

parts producing branches which fuse between adja-

cent hyphae. Branched vegetative hyphae form a

vegetative mycelium which appears as a light, ill-

defined spot on the food or culture medium surface

at the beginning of the spoilage or during the initial

stage of the colony development. Later, specialized

cells emerge from the flat hyphal mass bearing at

their ends the staminal components of the molds.

These constitute the reproductive mycelium of the

mold, whose cells are usually called conidiophores

and staminal components either conidia, if asexually

formed, or spores, if sexually generated. Sexual for-

mation of spores, which involves genetic rearrange-

ments, greatly contributes to the mold’s survival in

nature, but it is seldom observed in food and culture

media where asexual conidia are more likely to

appear. Sexual spores are frequently thick-walled

and able to withstand severe environmental condi-

tions, including heat processing, as in the case of the

Byssochlamys sexual spores which may spoil fruit

juices. In common with conidia, which possess a thin-

ner wall, spores differ from vegetative cells in having

a thicker tegument, a poorly differentiated cytoplasm,

and a low water content, resulting in the ability to

survive when environmental conditions become

lethal to living cells.

0008 Resting cells, which can withstand many adverse

conditions such as drying or oxygen deprivation, may

later restore their normal metabolic pathways, even-

tually giving rise to the first hyphal cell and so com-

mencing the mold life cycle when availability of

water, or air, or any other condition suitable to

growth, occurs.

0009 Nutrient requirements for mold growth are very

simple. A suitable organic carbon source is necessary

(this can be simple, such as glucose, or very complex,

like cellulose and hemicellulose composing the plant

cell wall). Many molds grow on poor substrates

containing only inorganic nutrients, e.g., inorganic

nitrogen or phosphorus. This explains why molds

may actively grow where bacteria cannot proliferate,

such as on the apparently hostile substrates of walls,

wood, fabrics, etc.

0010Many molds produce energy by reoxidation of

nicotinamide adenine dinucleotide/nicotinamide

adenine dinucleotide phosphate (NAD/NADP) co-

enzymes along an electron transport chain where an

inorganic compound serves as a terminal electron

acceptor (respiration); usually oxygen is the final ac-

ceptor, so molds need an aerobic environment for

their growth, but many common strains (e.g., asper-

gilli) use anaerobic respiration with nitrogen ions

as electron acceptors. Byssochlamys and a very few

other molds may break down sugars by fermentation,

in the complete absence of oxygen, initially producing

carbon dioxide, which can cause visible swelling of a

package. Growth of proteolytic and lipolytic strains

of molds is responsible for both the ripening and

distinctive flavor of the internally or surface mold-

ripened cheese and off-flavors and off-odors resulting

from fungal lipase activity, with an increase in the free

fatty acid (FFA) values.

0011Spoilage refers to any change that occurs in food

resulting in reduction in sensory quality, i.e., changes

in color, flavor, texture, or aroma brought about by

the growth of microorganisms in food and feed. De-

gradative enzymes, such as pectinases and cellulases,

are primarily responsible for degradation of the

main structural components of vegetables, fruits,

and legumes and related transformed commodities,

pectin, and cellulose.

0012Flavor-volatile metabolites produced by molds,

such as 3-methyl-butanol, 3-octanone, 3-octanol, and

many others, cause adverse changes in flavor and

aroma.

0013Besides the primary metabolic pathways supplying

the fungal cells with energy and cellular metabolites

necessary for growth, molds may show a range of

unusual metabolic processes (grouped as secondary

metabolism). These are not concerned with survival

and growth and take place when normal development

is restricted or the substrate composition is unbal-

anced (e.g., a very high carbon to nitrogen ratio, as

in the case of plant tissues). Some secondary metabol-

ites are of great commercial value (e.g., antibiotics

like penicillins) but others, such as mycotoxins, pose

a health risk to the consumer in crops and other plant

products. (See Mycotoxins: Occurrence and Deter-

mination.) Mold spoilage is so undesirable not solely

because of the resulting unesthetic changes, but also

because it may constitute a hazard to human and

animal health.

SPOILAGE/Molds in Spoilage 5523

Growth Requirements of Molds and

Effects of Processing

0014 The metabolism of molds, like that of other organ-

isms, is affected by environmental conditions which

may increase or decrease the rate of enzymatic reac-

tions. Physical and chemical conditions which play a

major role in controlling the mold’s metabolism and

growth are temperature, water availability, and ion

content.

0015 The nutritional, physical, and chemical attributes

of a given food substrate may select molds for pre-

dominant growth, these being the most highly

adapted organisms, e.g., to reduced water content in

high ionic strength (high acidity). Moreover, organ-

isms can survive to some degree in conditions that do

not allow growth. Spores and, to a lesser extent,

conidia may tolerate extreme conditions in food and

environment, retaining for extended times their abil-

ity to develop a mold when the substrate becomes

favorable again. Mold propagula held on a frozen

food may later undergo germination when mixed at

room temperature with other ingredients. Although

usually repressed by the high osmotic pressure (low

) in sugar-preserved or dried commodities, such as

in preserves in tanks for industrial use or in pasta in

its packaging, spores may give rise to a visible spoil-

age when water condenses at the mass surface.

0016 Most fungi are mesophilic, so they grow at moder-

ate temperatures, in the range 10–40



C. Lowering

the temperature decreases the rate of metabolism

and is often used to slow deterioration. A few fungi

grow at very low temperature. Cladosporium and

Thamnidium, sometimes colonizing animal hairs,

are important as spoilage agents of improperly

dressed meat that is held for long enough (usually

more than a month) at subzero temperatures above

10



0017 Important intrinsic factors which influence the

microflora that develops in food and feed include

pH and a

0018 Fungi show a wide range of behavior with respect

to water availability, generally being more tolerant of

water stress than other organisms, including the ma-

jority of yeasts. The lower limit for growth of molds,

expressed as a

, vary from 0.93 for destructive rots of

fruits and vegetables like Rhizopus and Mucor;to

0.87 for toxigenic fusaria; to 0.83 for agents of

surface discoloration in fresh cheese and sausage

like Penicillum expansum or P. viridicatum. Xerophi-

lic fungi are characterized as being capable of growth

below an a

of 0.85 and are most commonly associ-

ated with intermediate-moisture food such as dried

meats, seafood, fruit concentrates, jellies, jams, pre-

serves, and syrups, spices, nuts, and cereals, where

their effective growth range can be as low as 0.65.

Conditions of reduced a

lower the final fungal bio-

mass produced because of reduction of the growth

rate and of increase of the time required for spore

germination up to 3 months or more. Properly dried

and stored commodities are inherently resistant to

spoilage due to their low a

; however, temperature

differentials, such as in bulk-stored grains, may lead

to moisture condensation and possible growth of

xerophilic molds. The majority of xerotolerant fungi

belong to genera Penicillium and Aspergillus, includ-

ing its perfect forms such as Eurotium (Aspergillus

glaucus), Emericella, and Wallemia sebi.(See Water

Activity: Effect on Food Stability.)

0019Media and diluents with reduced a

are necessary

for enumerating xerophilic fungi, otherwise vegeta-

tive cells and spores may be lysed by osmotic shock or

remain dormant when exposed to the relatively high

associated with the conventional diluents and

media used in microbiological analysis. Addition of

humectants, such as 50% glucose to the diluent, and

18% glycerol or 50% glucose to traditional media,

especially malt extract agar, lowers a

levels to about

0.94 and 0.92 respectively. Extended incubation

periods, such as 4–6 weeks at room temperature

instead of the traditional 5 days time, are required

for recovery.

0020Molds, like yeasts, tolerate a greater pH range than

bacteria do. Many fungi can grow over a wide pH

range of at least 3–8, while pH values below about 5

negatively affect the metabolism and growth of bac-

terial cells. Where the food substrate shows a high a

it is the acidic environment which plays a decisive role

in the competition between bacteria and filamentous

fungi. As fruits show pH values of 4.6 or lower, mold

growth is more likely. Spoilage thus arises from the

intense activity of pectic and proteolytic fungal

enzymes that have pH optima between 2 and 5. (See

pH – Principles and Measurement.)

0021Because of the the acido-tolerant behavior of

molds, originally food mycologists relied on low-pH

media, such as acidified potato dextrose, Sabouraud,

or similar agars to detect fungi in clinical and food

specimens. However, in food samples acid pH may

adversely affect mold spore germination and give rise

to protein coagulation with the formation of artifacts,

and, therefore, it is more effective to use media of

neutral pH in combination with antibiotics. Anti-

biotics, such as chloramphenicol, gentamicin, and

others, are well-known biomolecules perturbing the

cell wall of bacteria which is different from that of

fungi.

0022Molds may alter the pH of the environment in

which they grow, by producing ammonium ions

that neutralize the substrate acidity and thus allowing

5524 SPOILAGE/Molds in Spoilage

(re)growth of normally repressed, dangerous

organisms. Such an example of metabiotic associ-

ation is given by the persistence of Listeria in cheese

ripened by selected molds. (See Listeria: Properties

and Occurrence.)

0023 Molds are aerobic organisms in that they require

oxygen and/or a food substrate with a high oxidation-

reduction potential (E

) for growth. Oxidized foods,

such as fruits with E

values betwee0n þ300 and

þ400 mV, support the growth of molds well, while

reduced ones, like yogurt with its E

value of about

100 mV, do not. In the latter case, molds may de-

velop a mycelium only at the surface in contact with

the air. Some fungi (e.g., strains of Paecylomyces

and Penicillium) are microaerophilic, growing in an

atmosphere containing only 0.1–0.5% oxygen. A few

species, such as Fusarium oxysporum, may show a

very delayed growth in the complete absence of

oxygen. It would appear, therefore, that the degree

of anaerobiosis attained under commercial processing

conditions is not always adequate to prevent com-

pletely the growth of molds.

0024 There is evidence that raising the level of carbon

dioxide in the atmosphere above 70–80% greatly

reduces the growth rate of most molds, with some

notable exceptions, such as Penicillium roquefortii

or Byssochlamyis nivea.

0025 Growth of most molds is restricted – sometimes

inhibited – by the use of preservatives at the legally

permitted concentrations (between 0.1 and 0.2%)

The acids and salts commonly used are propionic,

sorbic, and benzoic. Propionates are added to bakery

products and to certain processed cheeses. Benzoic

acid and its sodium salt are most widely used in

highly acidic foods such as fruit products and carbon-

ated beverages. The undissociated acid is the active

molecule and therefore the effectiveness increases

with decrease in pH while the organic acids exhibit

little fungistatic activity in neutral conditions. Inhib-

ition of growth by weak acid preservatives is due to a

number of actions, including membrane disruption,

inhibition of essential metabolic reactions, stress on

intracellular pH homeostasis, and accumulation of

toxic anions. Natamycin (pymaricin), a natural anti-

mycotic compound produced by Streptomyces nata-

lensis, is commercially available for the surface

treatment of cheese. In recent years, strains of preser-

vative-resistant molds (particularly aspergilli) have

been reported which tolerate high (0.5–1.5%) con-

centrations of organic acids due the induction of

an active transport system that pumps undissociated

acid molecules out of cells. The enzymatic de-

gradation of sorbic acid to pentadien by certain

fungal species is well documented. (See Preservation

of Food.)

0026Most molds possess little heat resistance, and are

easily destroyed when food with a

values above 0.93

are heated at pasteurization temperatures. Vegetative

cells and asexual propagules behave in the same

manner. Heat resistance of molds is enhanced in the

presence of high levels of solutes such as salt and

sugar. The decimal reduction time for Aspergillus

niger conidia heated at 100



C increases from about

1 ms in a moist substrate (a

¼0.98) to about 1 s in

intermediate-moisture substrates (a

between 0.85

and 0.90, such as cakes and most oven-processed

sweet products), and to 10 s when a

falls below

0.85 because of the addition of sugar (e.g., in fruit

preserves). In the latter products, the low pH, usually

between 3.2 and 3.5, partially counteracts the pro-

tective effect of sugar, thus decreasing the resistance

of mold to heat.

0027The responses of molds to the presence of sodium

chloride (salt) is somewhat different from that ob-

served with sucrose. Protection against heat inactiva-

tion of molds is increased even at lower a

values,

usually below 0.97, i.e., a salt concentration of about

3%. This should be kept in mind when setting up

pasteurization procedures for brines used in cheese

and sausage manufacture.

0028A few molds produce heat-resistant ascospores or

sclerotia. Ascomycetous species are widely distrib-

uted in soil and cause spoilage in heat-processed

food products containing fruits which have been ex-

tensively contaminated with soil. Ascospores pro-

duced by the two species of Byssochlamys, B. fulva

and B. nivea, and by Neosartorya fischeri are the

most resistant of all and they are typically associated

with spoilage of thermally processed fruit products,

mainly canned, where the can center temperature is

raised up to 80–90



C. The decimal reduction time of

Byssochlamys nivea spores at 80



C increases from

about 35 min (a

¼0.95) to about 4 h in neutral

foods with a

values between 0.85 and 0.86. Neosar-

torya fischeri var fischeri has a D

(decimal reduc-

tion time at 85



C) value of 6–10 min with a Z value

(Thermal Death Time curve’s slope) of 5–7



C while

the spinosa variety is more heat-resistant (D

value of 10–96 min with a Z value of 5–7



C). Symp-

toms observed with spoiled canned fruits include

breakdown of fruit texture, off-odors, gas, and

visible mold growth. (See Heat Treatment: Chem-

ical and Microbiological Changes; Pasteurization:

Principles.)

Classification of Molds

0029Only a small proportion of the thousands of genera

and species of molds identified in nature are of any

significance in foods.

SPOILAGE/Molds in Spoilage 5525

0030 Ranked taxonomically in the separate kingdom of

Fungi, molds are subdivided into further taxonomic

categories on the basis of ecological behavior, and

gross colony and microscopic morphology.

0031 The most important diagnostic factor relies on the

morphology of the asexual reproduction system

(the so-called anamorphic stage of the mold), best

observed under the microscope in slide-mounted

cultures. Spores formed through sexual reproduction

(the so-called telemorphic stage) are rarely used in

identifying foodborne molds, given the difficulty of

inducing gametogenesis and sexual fusion in vitro.

0032 Molecular tools based on the polymerase chain

reaction (PCR) may be applied in food mycology for

diagnostic purposes. The noncoding ITS (Internal

Transcribed Spacer) region of the rDNA unit, and

other genes coding for metabolic and structural func-

tions (e.g., the b-tubulin gene), have been investigated

to clarify the genetic structure of some species.

0033 Three subkingdoms include genera of significance

in food spoilage: Zygomycotina, Ascomycotina, and

Deuteromycotina. Most fungi, within the subking-

dom Zygomycotina, belong to the class Zygomycetes,

which includes, in the order Mucorales, three phyto-

pathogenic genera frequently involved in the spoilage

of moist wheat, flour, and cereal products: Absidia,

Mucor, and Rhizopus. Distinctive features of these

molds are (1) rapid growth when water availability

is above the limiting value of 0.92–0.93, including

filling the whole Petri dish with fine white to greyish

to blackish aerial mycelium, and (2) asexual spore

formation by cytoplasmic cleavage within a large

globose cell termed sporangium, from where sporan-

giospores are liberated by breakage or deliquescence

of the wall. Sporangia are located at the end of a

supporting hypha (sporangiophore), from where

they are separated by a septum forming a protrusion

called columella (Figure 1).

0034 A distinctive feature of the subkingdom Ascomy-

cotina is the development of sexual spores in a cell

(sporangium), more specifically termed the ascus

(bag). Asexual spores, called conidia, develop in

various ways directly from reproductive hyphae.

Ascospores of Byssochlamys species show a very

distinctive heat resistance.

0035 The subkingdom Deuteromycotina is used mainly

for convenience to accommodate all those fungi that

seldom, if ever, produce sexual stages. In all other

respects, however, these fungi are similar to the Asco-

mycotina, and where sexual stages are discovered

they are usually found to belong to the Ascomycotina.

In Deuteromycotina systematics the teleomorph

(perfect, sexual stage) name should preferentially

be used to indicate the species. Unfortunately, the

anamorphic name is firmly rooted in the literature

and in common parlance. The teleomorphic stage

cannot usually be seen in routine examination

of fungi unless special cumbersome techniques are

used, so the anamorph name is commonly retained:

Aspergillus, instead of its teleomorphs Eurotium and

Emericella; Penicillium, not the teleomorphs Eupeni-

cillium and Talaromyces, and so on.

0036The morphology of the fertile hypha is again the

most important factor in taxonomic characterization.

During development of the mold, asexual propaga-

tion occurs which starts with conidiogenesis: asexual

propagula, named conidia, are produced from the

mother cell (conidiogenous cell). The system com-

posed of a conidiogenous cell and its conidia is

known as a conidiophore. Conidiogenous cells are

sometimes supported by mono- or pluricellular stipes

whose shape may help in mold identification. Differ-

entiation of the conidiophore and conidial arrange-

ments serve as diagnostic features, and we may

distinguish the following:

(a)

(b)

fig0001Figure 1 (a) Large, round sporangium of Rhizopus oryzae.

(b) After disintegration of the sporangial wall, small clusters of

sporangiospores are released, leaving a naked umbrella-shaped

columella. Reproduced from Spoilage, Encyclopaedia of Food Sci-

ence, Food Technology and Nutrition, Macrae R, Robinson RK and

Sadler MJ (eds) 1993, Academic Press.

5526 SPOILAGE/Molds in Spoilage