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Zygomycota and

Glomeromycota

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Article Contents
. Overview

Elizabeth Moore-Landecker, Rowan University, Glassboro, New Jersey, USA

. Morphogenesis (Zygomycetes)
. Sexual Reproduction (Zygomycetes)

The phylum Zygomycota is an ecologically diverse and economically important group


of fungi, containing two classes, the Zygomycetes and Trichomycetes. The phylum
Glomeromycota, a group of mycorrhizal fungi, is derived from the Zygomycota.

. Biodiversity (Zygomycetes and Trichomycetes)


. Ecology (Zygomycetes and Trichomycetes)
. Economic Importance of the Mucorales (Zygomycetes)
. Phylum Glomeromycota

Online posting date: 15th July 2008

Overview
The phylum Zygomycota consists of two classes, the
Zygomycetes and Trichomycetes. The Zygomycetes are
widely distributed and occur predominantly as saprotrophs. These fungi are readily isolated from soil, air, dung
or decaying plants. Some are parasites of other fungi,
plants or insects. Humans may experience fungal diseases
or allergic reactions to fungi. Economically important
chemicals, pharmaceuticals and foods are produced by
Zygomycetes. The other class within the Zygomycota, the
Trichomycetes, is a much smaller group whose members
occur within the guts of insects and other arthropods. The
phylum Glomeromycota contains a small number of mycorrhizal fungi that had previously been classied in the
Zygomycetes.
Molecular data conrm the importance of the Zygomycota in fungal evolution. It is likely that the ancestral fungi
diverged from the animals and plants about a billion years
ago (Bruns, 2006). These fungi were likely similar to
present-day chytrids which occur in freshwater as swimming single cells. These ancient fungi apparently lost their
agella multiple times, giving rise to nonmotile fungi that
occupied terrestrial habitats, the ancient Zygomycetes.
Even today, the Zygomycota fungi retain comparatively
primitive characteristics. Later the Zygomycete lineage
gave rise to the remaining more advanced fungi. The phylum Glomeromycota arose approximately 600 million
years ago in the Precambrian Era. The two remaining phyla
(the Ascomycota and Basidiomycota) emerged approximately 500 million years ago in the Paleozoic Era, before
the diversication of land plants (Berbee and Taylor, 2001).
Fossils of the reproductive structures of a zygomycete and

ELS subject area: Microbiology


How to cite:
Moore-Landecker, Elizabeth (July 2008) Zygomycota and
Glomeromycota. In: Encyclopedia of Life Sciences (ELS). John Wiley &
Sons, Ltd: Chichester.
DOI: 10.1002/9780470015902.a0000381.pub2

early members of the Glomeromycota have been recovered. See also: Ascomycota; Basidiomycota
A unique form of sexual reproduction characterizes
fungi in the Zygomycota. Fusion of multinucleate gametangia occurs, followed by formation of a thick-walled
zygospore. Asexual reproduction typically involves formation of nonmotile spores (sporangiospores) within a sac
(sporangium) (Benny et al., 2001; Moore-Landecker,
1996).

Morphogenesis (Zygomycetes)
Most fungi in the Zygomycota form hyphae, elongated
tubular structures. Typically, hyphae contain several haploid nuclei within a common protoplasm. Hyphae may be
divided into cellular compartments by the formation of
crosswalls (septa). Septa delimit old or damaged portions,
and reproductive structures. Septa are regularly formed
within the hyphae of some members. For many saprotrophic species, the hyphae branch extensively and rapid
growth in culture can be readily observed. See also: Hyphae
Asexual reproduction occurs after the hyphae have undergone extensive growth. Erect, aerial hyphae,
sporangiophores, arise from hyphae. The sporangiophores may be either branched or unbranched. The
sporangiophore tip enlarges to form a terminal swelling,
the sporangium. One or more sporangiospores develop
within the sporangial wall (Figure 1).
The multispored sporangium is typical for many common
and important zygomycetes such as those in the genera
Rhizopus and Mucor. In these fungi, the sporangium begins
its development as a balloon-like swelling at the
sporangiophore tip, and is later separated by a new septum.
This septum protrudes into the sporangium as a dome, the
columella. At rst, the sporangium is multinucleate. Uninucleate spores are delimited by the cleavage of the cytoplasm. They are released when the sporangial wall ruptures.
Although most of these fungi produce a large multispored sporangium, other types of sporangia occur in some
genera. Merosporangia are rodlike, containing several
sporangiospores in a row within the sporangium wall. In
others, the sporangia may contain only a few sporangiospores (these are known as sporangioles). Sporangioles are

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Zygomycota and Glomeromycota

Figure 1 Types of sporangia formed. (a) Blakeslea trispora. Multicelled sporangium with a columella. (b) Blakeslea trispora. Sporangioles with a few
sporangiospores borne on a swollen sporangiophore tip. (c) Syncephalis. Sporangiophore bearing merosporangia. (d) Detail of merosporangium. (a, b) Gaumann
EA and Dodge CW (1928) Comparative Morphology of Fungi. New York: McGraw-Hill (after Thaxter) and (c, d) Gwynne-Vaughan HCI (1937) The Structure and
Development of the Fungi. Cambridge: Cambridge University Press (after Thaxter).

much smaller than the multispored sporangia and lack a


columella. In some cases, only a single sporangiospore is
formed within the sporangium.

Sexual Reproduction (Zygomycetes)


Most species in the order Mucorales share a common,
characteristic pattern of development. With minor variations, this pattern exemplies sexual reproduction in other
Zygomycetes (Moore-Landecker, 1996).
Depending upon the species, sexual reproduction may or
may not require two genetically dierent hyphal strains.
Those fungi that can reproduce without a second genetic
strain are said to be homothallic, whereas those that require
two dierent, compatible strains for reproduction are heterothallic. Heterothallism is controlled by two alleles at a
single genetic locus controlling incompatibility. The mating types are designated as A and a, or (+) and (). A
compatible cross can occur only between two dierent
mating types (A and a, but not A and A or a and a).
2

In a heterothallic fungus such as Mucor or Rhizopus, the


hyphae of the (+) mating type grow towards the hyphae of
the () mating type. Attraction of hyphae towards each
other may occur as a result of volatile hormones. The plus
strains produce 4-hydroxymethyltrisporates, whereas the
minus strains produce trisporins. These volatiles induce
progametangia formation, the enlarged club-shaped ends of
the hyphae. Each progametangium is subsequently separated by a septum into a terminal multinucleated gametangium, and the subterminal suspensor. In most species, the
suspensor and gametangia are equal in size, but variations in
their morphology occur. Two gametangia (one from each
mating type) come into contact with each other and adhere
tightly together. The wall breaks down between the gametangia, allowing protoplasts to mingle to form a single cell,
the zygote. At rst, the zygote is surrounded by the thin wall
derived from fused gametangia. The zygote begins its development into the zygospore as a new thick wall forms
within the thin outer wall, which is eventually sloughed o
(Figure2). The mature zygospores are typically dark (black or
brown), and have thick walls roughened with warts or other

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Zygomycota and Glomeromycota

Biodiversity (Zygomycetes and


Trichomycetes)
Class Zygomycetes
The larger class, the Zygomycetes, contains approximately
1000 known species. These fungi are commonly collected
worldwide. Within this class, important dierences in asexual reproduction and ecological adaptations occur among
the orders. Orders in the class Zygomycetes are (White
et al., 2006):
Dimargaritales (14 species)
Endogonales (21 species)
Entomophthorales (185 species)
Kickxellales (21 species)
Mortierellales (100 species)
Mucorales (300 species)
Zoopagales (161 species)

Figure 2 Stages in development of a zygospore of Sporodinia grandis shown


in a median view. Nuclei are not shown. (a) Two swollen hyphal tips come into
contact. (b) Septa separate gametangia from the suspensors. The gametangia
fuse, and the intervening walls break down, allowing the cytoplasm to
mingle. (c) The zygote continues to enlarge. (d) A thick wall develops
surrounding the protoplast of the zygote. This wall lies to the inside of the
original walls of the zygote seen in the earlier stage. Gaumann EA and Dodge
CW (1928) Comparative Morphology of Fungi. New York: McGraw-Hill (after
Keene).

ornamentations. By the time the zygospore has undergone a


resting period and has begun to germinate, some nuclei may
have fused with each other to form diploid nuclei, which
subsequently undergo meiosis. As germination occurs, a
hypha or a sporangiophore terminated by a sporangium
emerges from the zygospore (Figure 3).
Some fungi routinely produce azygospores, which arise
from a single gametangium. Azygospores are thick-walled
spores that morphologically resemble zygospores, but are
apparently devoid of nuclear events characterizing a sexual
cycle. Both zygospores and azygospores are capable of
undergoing long periods of dormancy, enabling the fungus
to survive through the winter and perhaps other unfavourable conditions. They are often simply termed resting
spores. Massospora cicadina is apparently able to survive in
the soil as dormant resting spores for the 17-year period
before its host, the cicada, again becomes active.

A phylogenetic analysis of six genes was made of various


fungi in the Zygomycota (James et al., 2006). Apparently
there are four clades of related fungi, each representing an
early loss of the agellum in ancestral zygomycetes. The
largest clade is that consisting of the Mucorales, Mortierellales and Endogonales. Two additional clades are represented by the Entomophthorales and Zoopagales. The
fourth clade consists of the Kickxellales, Dimargitales and
the Trichomycetes. Mycolgoists are deliberating about appropriate taxonomic changes to incorporate this information (Hibbett et al., 2007).
Mucorales is the largest order (12 families, 300 species).
The majority are saprotrophs. Well-known and important
genera include Mucor, Rhizopus and Absidia. The hyphae
are nonseptate, except in old portions and at the base of
reproductive structures. Asexual reproduction most often
involves multispored sporangia, but can also involve fewto one-spored sporangioles or merosporangia. Species of
Pilobolus can eject the entire sporangium out into the open
and away from the dung heap where they live. The phototropic sporangiophore bends towards the light (an opening in the heap of dung), osmotic pressure builds up within
the sporangiophore which suddenly bursts, forcibly carrying the sporangium away on a minute jet stream of uid.
The sporangium can land on fresh grass where it can be
consumed by an herbivore.
A single genus, Endogone, belongs to the Endogonales.
These fungi occur widely in the temperate zone as saprotrophs in soil, sometimes forming ectomycorrhizae with
roots. Their multicellular sporocarps are elongated,
rounded or lobed. The largest sporocarps resemble peas,
giving these fungi their common name pea trues. They
occur chiey below the surface of the ground but also above
ground in the litter. Sporocarps contain zygospores, which
occur randomly inside, or in a basal row. Interwoven
hyphae surround the sporocarp contents. Sporocarp formation is otherwise unknown in the Zygomycetes, but is a

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Zygomycota and Glomeromycota

Figure 3 Zygospores of Mucor mucedo (Mucorales). (a) Mature zygospore supported by two suspensors. (b) A germinating zygospore forming a
sporangiophore and sporangium. Bessey EA (1961) Morphology and Taxonomy of Fungi. New York: Hafner (after Brefeld).

characteristic shared by a few fungi in the Glomeromycota,


and by the majority of the fungi in the Ascomycota, and
Basidiomycota.
The Entomopthorales are parasites of algae or ferns,
whereas the majority are parasites of insects or other animals.
Some are saprotrophs in soil or dung. The sparse hyphae
usually fragment into a number of multinucleate short segments, the hyphal bodies. Naked protoplasts may also be
formed. Asexual spores are conidia that develop exogenously
on their supporting conidiophores (this is in contrast to development within a sac-like sporangium). Conidiophores are
usually unbranched, and bear ovoid to spherical conidia that
are often forcibly discharged. Once discharged, a conidium
can germinate to form a secondary conidium. Sexual reproduction occurs by the fusion of hyphal bodies, or similar or
dissimilar gametangia to form a zygospore having a thick
two- or three-layered wall. The zygospores may be hyaline or
dark and smooth or ornamented. Not all species reproduce
sexually, and instead produce azygospores.
Zoopagales fungi can parasitize other fungi, or trap living nematodes, amoeba and small terrestrial animals. Life
4

as a predator is obligate for these fungi. They trap their prey


with sticky secretions produced by the hyphae or
sporangiospores that the host encounters. Subsequently,
the fungus produces a coiled thallus or hyphae within the
host, and feeds upon the host until its contents are exhausted. After the hosts death, the fungus reproduces
asexually by forming monosporous sporangioles that arise
from the exterior of the hosts carcass. Depending upon the
species, they may be borne singly or in chains. Spherical
zygospores, covered by hemispherical warts, are formed as
a result of sexual reproduction by some species. See also:
Fungal Pathogens of Nonhuman Animals; Nematophagous Fungi
The Kickxellales has one family, and a cosmopolitan
distribution with most organisms living as saprotrophs.
These fungi reproduce asexually by forming monosporous
sporangioles. Young as well as old hyphae are divided by
septa, each septum having a central plug. The smooth
zygospores are formed from hyphae that are not dierentiated as progametangia. The small order Dimargitales
bears many similarities to the Kickxellales, but diers

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Zygomycota and Glomeromycota

primarily by producing merosporangia containing two


spores. These fungi are obligate mycoparasites of members
of the Mucorales.

Class Trichomycetes
The second class, the Trichomycetes, has only approximately 200 species. These fungi produce a minute thallus
consisting of only a few cells (Lichtwardt, 1986). The
thallus is anchored to the host by a holdfast that may simply be a secretion, or a distinctive basal cell together with a
secretion. These fungi occur primarily in the midgut or
hindgut of insects and other arthropods, whereas a few
occur on the outside of the host. Distribution of the fungus
depends upon that of the hosts, and both have a cosmopolitan representation. There are two orders, the Asellariales (10 species) and Harpellales (103 species). Until
recently, the Trichomycetes was considered to have four
orders, but the orders Eccrinales and Amoebidales have
been transferred to the protozoa.
The Harpellales fungi occur in larvae of insects (such as
stoneies or mayies) that live in fresh water, especially
rapidly owing streams. The small thallus is either unbranched or branched. Branched thalli have septa that resemble those of the Kickxellales by having a central pore
and a plug. Asexual reproduction occurs by formation of
elongated monosporous sporangioles, which trail one or
more appendages after their release. The appendages become entangled in substrates at the streams bottom, where
the insect larvae often congregate and are likely to be infected by the fungus. Sexual reproduction occurs in some
species. Mating occurs between dierent thalli or between
cells of the same thallus. Enlarged cells (the gametes) fuse to
form an elongated conjugation tube within which their
protoplasts mingle. The conjugation tube gives rise to a
special branch, the zygosporophore, that bears a zygospore
at its apex. The zygospore is an elongated cell with conical
ends (Figure 4). Cytological events in the sexual cycle such as
nuclear fusion and meiosis have not been observed.
The remaining order, the Asellariales, contains only a
single family and three genera. They are widely distributed
and may occur in adult insects or isopods in streams, intertidal regions, or terrestrial habitats. These fungi produce
a branched, septate thallus that is attached to the hindgut
lining. Asexual reproduction occurs when parts of the
thallus break apart into uninucleate spores. Sexual reproduction is unknown.

Ecology (Zygomycetes and


Trichomycetes)
Zygomycetes as saprotrophs
Most members of the Mucorales and Kickxellales are
saprotrophs, feeding and living upon dead organic matter.
These zygomycetes are readily isolated from the soil, dung,
decaying plant debris and old mushrooms. There is some

Figure 4 A zygospore of a trichomycete borne on a zygosporophore. From


Moss ST and Lichtwardt RW (1977) Zygospores of the Harpellales: an
ultrastructural study. Canadian Journal of Botany 55: 30993110. Copyright
# 1977 NRC Research Press.

anity for particular substrates. Strict soil inhabitants include species of Zygorhynchus and many species of Mucor
and Absidia. Dung-inhabiting fungi include Pilobolus and
Phycomyces. Species of Spinellus occur exclusively on decaying mushrooms. Decaying grains, fruits and vegetables
are commonly invaded by species of Rhizopus and Absidia.
Some species of Mucor can grow at 258C and have been
found in the Arctic tundra. It is not unusual to nd coldtolerant strains of Mucor or Rhizopus growing on jam or
other refrigerated food. Species of Rhizomucor are thermophilic, growing at the temperatures above 408C that
occur in insuciently dried hay, moist stored grain and
compost where temperatures rise. Some zygomycetes can
also tolerate extremes in soil pH, being adapted to either

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Zygomycota and Glomeromycota

very alkaline or very acidic soils. Some play a benecial role


by degrading pesticides in soil, or by removing contaminating heavy metals from soil or water (particularly those
fertilized with sludge or contaminated with sewage).
Growth of saprotrophic fungi on organic debris is of
extreme importance because it provides a means to break
down natures garbage, returning the elements to the soil
and atmosphere in a form that can be used by other organisms. Zygomycetes are among the rst fungi to colonize
a fresh substrate such as plant remains or dung that has just
reached the ground. The spores germinate rapidly, and
their hyphae grow rapidly on the fresh substrate, giving
them an advantage over competing fungi. For a short time,
zygomycetes are the dominant fungi on the substrate. They
utilize the readily available sugars and other nutrients.
Later, their numbers decline because they are unable to
tolerate their own byproducts of metabolism (especially
carbon dioxide from respiration) and the competition from
other fungi. Along with some other soil fungi, species of
Rhizopus and Mucor can detoxify some pesticides in soil,
rendering them harmless. See also: Fungal Ecology; Fungi:
Ecological Importance and Impact on Humans

Zygomycetes as necrotrophic plant parasites


Saprotrophic zygomycetes can invade weakened or
wounded plants, causing disease. These fungi are necrotorphic parasites that kill the plant tissues, and then feed on
them as saprotrophs.
The layperson is probably most familiar with postharvest rot because this can aect eshy plant parts in the
market or home. Strawberries and sweet potatoes are particularly susceptible to infection by species of Rhizopus and
Mucor. The fungi enter wounds, perhaps inicted by birds
or insects in the eld, or by harvesting and subsequent
processing for market. Within the plant, the hyphae grow
between cells, secreting pectinases that cause the tissues to
disintegrate and the cells to die. The fungus then feeds on
the dead cells. The aected plant tissue becomes watery and
soft, and the fungus sporulates on its surface. The infection
can be spread to adjacent fruits or vegetables in storage.
Choanephora cucurbitarum causes crop loss in the southeastern part of the United States where warm, humid conditions favour invasion of host plants. Hosts are primarily
squash and other curcubits, but a variety of vegetables and
ornamental plants are aected. On squash, the disease is
commonly known as wet rot, blossom blight or fruit rot,
names that describe the symptoms. The fungus overwinters
in the eld as resting spores. In the spring, sporangiospores
rst infect the blossom and then the infection extend into
the stem and developing fruit. Infected parts become soft
and wet as they rot. The fungus produces a visible mass of
black sporangiospores on the surface of the aected tissue,
producing a visible mass. An entire fruit can rot within 48 h.
Rhizopus stolonifer and other Rhizopus species can invade sunower plants, causing Rhizopus head rot. This
disease occurs in Israel and is becoming increasingly serious on sunower crops in California and other western
6

Figure 5 Rhizopus head rot on sunflower. Both watery soft rot and dried
shredded tissues are visible. Reproduced with permission from Harveson RH
(2007) Rhizopus head rot of sunflower in Nebraska. University of NebraskaLincoln Extension publications website.

states, sometimes resulting in loss of the entire crop. The


fungus enters through wounds that may result from injury
by insects, birds or hail. Infection of the plant rarely occurs
before owering. The rst symptoms are dark spots on the
back of ripening heads. A watery soft rot that later turns
brown follows. Eventually, the heads dry prematurely,
shrivel, and the tissues appear to shred (Figure 5). Fungal
growth and the dark sporangiophores become visible on
both sides of the head. The disease can result in underweight seed at harvest. If the peduncle is infected, the entire
head can fall o, resulting in even further loss of the seed.
The oil quality may be adversely aected as well. See also:
Fungal Pathogens of Plants

Zygomycetes as mycoparasites
Mycoparasites are fungi that parasitize other fungi.
Among the Zygomycetes, mycoparasites occur in the Mucorales, Dimargitales and Zoopagales (Jeries and Young,
1994).
Species of Syncephalis (order Zoopagales) are necrotrophic mycoparasites of members of the Mucorales, such as
Rhizopus. Hyphae of Syncephalis invade the host hyphae,
and nally grow within the host. The hosts protoplasm is
destroyed, and eventually the host is killed. Subsequently
the necrotrophic mycoparasite can live on the dead host as
a saprotroph.
Other Zygomycetes are biotrophic mycoparasites, parasites that do not cause the death of their host fungi. The
mycoparasite contacts its host, producing an infection peg
that rst binds to the wall, and then penetrates it by mechanical and/or enzymatic means. Each infection peg develops into a specialized hyphal ending, the haustorium,
that lies between the hosts protoplast and cell wall. Haustoria absorb nutrients from the host such as vitamins
(biotin and thiamin), a growth factor (mycotrophein) and a
fatty acid (g-linolenic acid). The hyphae of the mycoparasite, as well as its reproductive structures, develop outside

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of the host. The physiology of biotrophic parasites is nely


tuned to that of the host so that the host is not killed. This is
advantageous to the mycoparasite because it ensures a
continued source of nutrients for these fungi, which would
be unable to live as saprotrophs on the dead hosts. Obligate
biotrophic mycoparasites include fungi in the genera Dimargaris and Dispira (order Dimargitales) and Piptocephalis
virginiana (order Zoopagales). These fungi are almost exclusively restricted to host fungi in the Mucorales.

Zygomycetes as allergens
Workers in certain occupations are exposed to air that
carries an unusually large number of fungal spores, including those of saprotrophic zygomycetes. Examples include farmers who are exposed to grain, hay or silage;
woodworkers who are exposed to wood timber or pulp;
and workers in sewage disposal facilities. In these environments, the worker repeatedly inhales fungal spores that
may cause allergic reactions. Acute respiratory symptoms
such as wheezing and dry coughs, as well as fever occur.
Most cases are mild and of short duration, but in some
cases the condition may become chronic. Zygomycetes that
cause allergic reactions are Rhizopus microsporus that
grows on wood chips and timber in sawmills, and Rhizopus
stolonifer and Mucor racemosus that are encountered near
decaying vegetation or in damp interiors. Although these
zygomycetes can cause allergic reactions, they are not
among the most numerous or important of these troublesome fungi (Lacey and Crook, 1988). See also: Fungal
Spores

Zygomycetes as parasites of mammals


Sporangiospores of zygomycetes routinely occur in the air
breathed by mammals. The fungi rarely cause a problem,
but can become parasitic in individuals who are in a weakened condition. Zygomycetes cause diseases of a variety of
farm animals as well as humans. See also: Fungal
Pathogens of Humans; Fungal Pathogens of Nonhuman
Animals
A few Entomophthorales fungi can infect mammals such
as horses and humans, particularly in the tropics (Jong and
Dugan, 2003). One of these is Basidiobolus ranarum, which
can be isolated from the gut contents or dung of amphibians, or from decaying vegetation. The disease of humans is
known as basidiobolomycosis. The fungus is introduced
into the body by trauma. It is especially likely to aect
children in tropical regions, causing enlarged subcutaneous
masses, particularly in the buttocks or limbs. The second
fungus known to cause human disease is Conidiobolus coronatus, which also occurs as a saprotroph and occasional
insect pathogen. It rarely causes a disease, known as conidiobolomycosis, in immunosuppressed patients. The disease aects the nasal mucosa, causing nosebleeds, and
nodular growths of the nasal passages that can cause mechanical blockage.

The disease muromycosis, caused by Mucorales members, is far more troublesome. It has been recognized in
farm animals such as pigs, horses and cattle for more than a
century. The principal fungus causing this disease in animals is Absidia corymbifera which occurs in grain and silage. Species of Rhizopus and Rhizomucor can also cause
the disease. Nodular lesions of subcutaneous tissue, lymph
nodes, or other organs such as the lungs or intestinal tract
may occur. The infection may be localized or become systemic as the fungus is spread throughout the body in the
blood, even infecting the brain. Some animals show no
symptoms, whereas others develop pneumonia. Animals
having a systemic infection can have dysfunctions of the
digestive system (anorexia and persistent diarrhoea) or
neurological disturbances if the brain is involved. Mucormycosis is a common cause of abortion in cattle and
pigs.
Species of Rhizopus (especially Rhizopus oryzae) and
Mucor cause muromycosis in humans. Infection of humans
is not common and occurs primarily in individuals with a
serious existing condition such as diabetes, leukaemia, organ transplantation or malnutrition. In patients with diabetes, mucormycosis originates in the sinus and nose.
Early symptoms include fever and dull sinus pain, followed
in a few days by double vision and increasing fever. Fungal
invasion of the ophthalmic artery leads to blindness and a
coma can result when the fungus invades the frontal lobe of
the brain. Without proper treatment, the diabetic patient
may die within a few days or weeks. Progression of muromycosis may be dierent for other patients, with the infection beginning in the lungs or gastrointestinal tract. In
all cases, there is the likelihood that the fungus will spread
rapidly through the blood to the brain, causing death
(Schipper and Stalpers, 2003). See also: Immunity to
Fungi; Infections in the Immunocompromised Host

Zygomycetes as insect parasites


Entomophthorales fungi can cause infection in most insects and sometimes can control populations of insect pests
in nature. Populations of the gypsy moth have been held in
check in the northeastern USA because this insect is parasitized by Entomophaga maimaiga that can occur in epidemic proportions. Fly populations can be reduced
considerably when cool, damp conditions favour infection
by species of Entomophthora (Figure 6).
Entomophthora muscae is probably most familiar to the
layperson because it attacks houseies in houses, barns and
poultry houses. Infection begins when a conidium contacts
a y, germinates and forms a germ tube. It penetrates the
insects integument, and multiplies within the body cavity
as short, thick hyphal bodies that grow by budding and
ssion. The fungus penetrates the insects brain, altering its
behaviour. As death approaches, the insect seeks a high
place such as a tall blade of grass in the eld, or window in a
house. The insect assumes a characteristic posture, stretching its legs outward and opening its wings. Both the elevation and the open posture aid spore dispersal after death,

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mosquito larvae that it invades. Another trichomycete,


Harpella melusinae, invades ovaries of blackies, forming
cysts in place of eggs. The female then deposits these cysts,
rather than eggs, in a suitable environment. The cysts germinate by forming one or two germ tubes that will produce
small sporangiospores. The blacky population is reduced,
while aiding dispersal of the fungus, perhaps from one body
of water to another (Lichtwardt, 1996).
Insect larvae often occur in dense populations where
they can infect each other. They may graze upon thalli that
emerge from the anus of their neighbours. Zygospores and
sporangiospores are shed into the environment with the
faeces, when the gut lining is shed as moulting occurs, or
when the host dies. The arthropod hosts feed upon debris
or algae. As they feed, they consume the fungal spores,
which then are stimulated to germinate within the gut.
Figure 6 A root maggot fly was attacked and killed by an Entomophthora
fungus. The fungus has emerged through the abdominal wall, and appears
white in the photograph. The fly is attached to a conifer needle by its
proboscis. Reproduced with permission from Barron GL (2006) Mycoalbum
compact disc. Mycographics, Guelph, Ontario.

which usually occurs in the late afternoon. Timing of death


is set by photoperiods and correlates this event with low
temperature and high humidity that favour spore germination. Conidiophores emerge through the exoskeleton
during the late afternoon and forcibly discharge their conidia at night. Discharged conidia can be visible as a ring
around a dead y. The conidia can germinate repeatedly,
forming smaller conidia. Other ies may be infected when
they contact conidia. Male ies often attempt to copulate
with the corpse of a dead female, which also helps spread
the infection. Resting spores sometimes develop within the
body cavity as winter approaches.

Trichomycetes as symbionts and parasites


Trichomycetes may be found when the midgut or hindgut
of an arthropod host (such as an insect or sowbug) is dissected (Lichtwardt, 1986, 1996). Within the gut, the thalli
are attached to the gut lining and lie within the gut lumen.
The thallus does not penetrate the gut tissue. Only the
largest of these fungi can be observed without a microscope. When clustered together, the longer thalli may make
the gut appear to be fuzzy or hairy, giving the name
Trichomycetes (hair fungi) to this group of fungi. In a few
species, the thalli may protrude from the anus of the host
and can therefore be detected without dissection.
The trichomycetes require a suitable host, but in contrast, having these fungi in the gut is not obligate for the
host. The fungi assimilate nutrients from materials within
the hosts gut. Typically, the host shows no response, either
favourable or unfavourable, to the presence of the fungi. It
is possible that the host may absorb some nutrients produced by the fungus. In culture, a few trichomycetes produce sterols and vitamin B that are normally required by
the hosts. The trichomycetes may be parasitic in some
cases. One species, Smittium morbosum, causes death of the
8

Economic Importance of the


Mucorales (Zygomycetes)
Some members of the Mucorales are economically important, either in a positive or negative way. Diseases of plants,
domestic animals and humans, discussed earlier, can cause
considerable economic loss. On the positive side, these
fungi can provide useful organic compounds, steroids and
foods. See also: Fungal Cells; Fungal Fermentation:
Industrial; Fungal Metabolites

Organic compounds
These fungi produce various useful enzymes and metabolites (Table 1).
Commercial production of proteases and lactic acid by
these fungi is especially signicant.
Rhizomucor miehei and Rhizomucor pusillus (along with
one other fungus) produce acid proteases that are used to
manufacture about half of the cheeses worldwide (Lowe,
1992). Cheese manufacturers had previously relied upon
suckling calves as a source of rennin (chymosin), a milkclotting enzyme produced in the fourth stomach. A worldwide shortage of calves rennin occurred because cheese
consumption increased while calves are usually slaughtered
at a later age. This shortage resulted in a search for an
alternative milk-clotting agent, and it was found that fungal proteases could substitute for calves rennin. Fungal
proteases can clot the milk, but the activity is not so intense
that the protein is completely hydrolysed. This is a desirable feature that is not shared by proteases from bacteria,
mature cows or pigs. Further, many vegetarians seek
cheese that was not manufactured with enzymes from animals. Fungal proteases have other uses (Table 1).
Rhizopus oryzae can produce signicant amounts of lactic acid from glucose.A high yielding strain originated as a
mutant, and further successive selection of six mutants led
to a strain of Rhizopus oryzae that can convert up to 90%
of glucose to lactic acid, representing a substantial

ENCYCLOPEDIA OF LIFE SCIENCES & 2008, John Wiley & Sons, Ltd. www.els.net

Zygomycota and Glomeromycota

Table 1 Useful organic compounds from mucoraceous fungi


Product

Producer

Use of product

Enzymes
Amylase

Rhizopus oryzae

Manufacture of beer, bread; sweetening of foods sizing


for textiles, paper
Rening of beet sugar
Fat removal from milk, meat, avour processed cheese;
enhance shelf life of baked goods; removal of fatty stains
from laundry
Increase yield of fruit juice; removes sediment from fruit
juice, wine; increases yield of vegetable oil from tissue
Cheese manufacture; tenderize meat, sausage casings;
preparation of animal skins for tanning; gum removal
from silk; relief of blood clots in humans

Galactosidase
Lipases

Pectinase
Proteases

Metabolites
b-carotene
Fumaric acid

Lactic acid
g-linolenic acid
Triglycerides

Mortierella vinaceae
Rhizomucor miehei
Rhizomucor pusillus
Rhizopus oryzae
Rhizopus oryzae
Rhizomucor miehi
Rhizomucor pusillus

Blakeslea trispora
Phycomyces blakesleeanus
Rhizopus delemar

Rhizopus oryzae
Mortierella spp.
Mucor spp.
Mortierella vinaceae

improvement over the 70% conversion by wild-type


strains. Although bacteria can also produce lactic acid,
Rhizopus oryze is favoured because it makes pure L(+)lactic acid, whereas bacteria make mixed isomers. This
isomer of lactic acid is preferred for use in the food industry
as a preservative, to enhance the avour of foods, and to
adjust the acidity. It is also the preferred form for manufacture of polylactic acid, a biodegradable plastic. Other
uses are listed in Table 1. The global market for lactic acid is
approximately 250 000 tons annually (Demain and Sanchez, 2007).

Steroid bioconversion
Steroids occur in humans as hormones produced by the
testes, ovaries, placenta and the adrenal cortex. They can be
useful as anti-inammatory agents, for the treatment of
sexual disorders or regulation of fertility.
Steroids may be obtained from natural sources such as
ox bile, urine or plants, or they may be synthesized. They
dier from each other in their side-chains, and their eectiveness as a drug depends upon a particular structure.
Chemists sometimes modify the steroid nucleus or the steroids isolated from natural sources. However, transformations or additions of side-chains may be dicult to
accomplish by chemical means, or may be too expensive
or time-consuming. Some bacteria, actinomycetes and
fungi can modify the steroid precursor if it is added to the
culture medium. An example is the hydroxylation of carbon-11, which can be accomplished by Rhizopus stolonifer
but is dicult for the chemist to accomplish. The particular

Colouring agent for food; precursor to vitamin A for


humans; dietary supplements
Flavour rye bread, fruit beverages, candies; control pH in
foods; leavening agent for baked goods; plastic
manufacture
Control pH in food; avour foods; plastic manufacture
Essential fatty acids for humans; dietary supplement;
lowers serum cholesterol
Alternatives for plant or animal fats in food

conversion is required to produce cortisone from progesterone. Species of Rhizopus and Mucor can also accomplish
other conversions such as hydroxylation of other carbons,
side-chain cleavage, epoxidation and hydrogenation. In the
commercial production of specic steroids, the steroid nucleus is often converted into the nal form by a combination of chemical procedures and conversion by specic
microbes.

Tempeh, an indigenous food


Eons ago, before the beginning of recorded history, our
ancestors doubtlessly found that various foods spoiled. In
other cases, rather than spoiling, the foods became converted to a new edible form. Fruit juices could become a
pleasant, tangy and slightly alcoholic beverage, wine,
which we continue to make with the aid of yeasts. The
texture, avour and nutritional properties of foods are often improved by microbial growth, whereas spoilage is delayed. Indigenous people worldwide have developed and
used fermented foods.
The Chinese made fermented foods approximately 2000
years ago when they also cultivated the soyabean, which is
used to produce several types of fermented foods with the
aid of Mucorales fungi. Indonesians probably learned to
make tempeh from the Chinese about that time. Temeph is
a particularly important food in Indonesia where it is used
as an economical meat substitute with distinctive avour
and texture. Approximately 64% of the soyabean crop is
made into tempeh in Indonesia. Other countries learned
about tempeh from Indonesian immigrants. Tempeh was

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Zygomycota and Glomeromycota

rst sold commercially in the United States in 1961, but is


now widely available in health, ethnic and grocery stores
(Kuswanto, 2004).
For traditional preparation of tempeh, soyabeans are
partially cooked and then inoculated with small amounts
of an earlier tempeh batch that had been dried. The inoculum contains spores of a Rhizopus species, particularly
Rhizopus oligosporus, which occurs on native vegetation.
Once inoculated, a small quantity (about a handful) of
soyabeans is wrapped in a large leaf to form a packet. The
tempeh is ready to eat approximately 24 h later when the
soyabeans are bound together by the hyphae into a solid
cake.
The Rhizopus fungi are prolic producers of proteases
and lipase. Proteases hydrolyse large amounts of the soyabean protein to peptides and amino acids, whereas the lipases free unsaturated fatty acids. There is an increase in
soluble carbohydrates, riboavin, niacin and vitamin B12.
When compared with cooked soyabeans, tempeh is softer,
more easily digested, and provides enhanced nutritional
value. In addition to being a good food, tempeh apparently
has some useful health properties. It was discovered during
World War II that prisoners of war could not digest soyabeans, but even prisoners with dysentery could eat tempeh.
An antibiotic eective against bacteria that could cause
gastrointestinal distress was later discovered in tempeh.
Tempeh also contains isoavones and fat-soluble vitamins,
antioxidants that provide protection against cancer and
ergosterol which helps lower blood cholesterol levels.

The Glomeromycota is a small phylum, containing only


approximately 200 species and 10 genera. Taxonomists
have increasingly relied upon molecular data to clarify their
relationships. Traditionally families and genera were delimited by the manner in which spores are formed, whereas
spore morphology is used to delimit species. However,
morphologically similar fungi can be shown to belong to
dierent clades on the basis of molecular data, immunological reactions and types of fatty acids produced. Using
molecular data in combination with morphology, Schuler
et al. (2001) divide the phylum into four orders. The Archaeosporales and Paraglomerales are the closest to the ancestral type, and each order has only one genus and a few
species.
The majority of these fungi occur in the Glomerales and
Diversisporales. Glomus is the only genus in the Glomerales, and with about 70 species, is the largest genus in the
phylum. These fungi produce chlamydospores from a
swollen hyphal tip. The wall becomes thicker, and either
one or two wall layers are evident. Finally, the chlamydospore is separated from the supporting hypha by a septum,
but remains attached to the parent hypha. The chlamydospores are usually ovoid to globose, have dense oily cytoplasm, and are yellow to brown in colour. Spores are
produced singly, in loose or tight clusters, or in sporocarps
that have a surrounding membraneous covering. Glomuslike fungi have been reassigned to all other orders on the
basis of molecular data. The order Diversisporales contains three families with dierent spore types, including the
Glomus-type.

Phylum Glomeromycota

Vesicular arbuscular mycorrhizae

Before 2001, these fungi were classied in a single order in


the Zygomycota. They were thought to be closely allied to
the Endogonales because their morphology is sometimes
similar and they are found in comparable habitats. Molecular data established that they diverged early from the
zygomycetes, and supported their removal from the
Zygomycota as a new phylum (Schuler et al., 2001). They
are obligate symbionts with photosynthetic organisms.

These fungi coevolved as symbionts with photosynthetic


hosts. One fungus harbours cells of a bluegreen alga
(Cyanobacteria) within bladderlike sacs. Others may be
symbiotic with primitive plants such as the liverworts and
hornworts. The vast majority of these fungi occur as vesicular arbuscular mycorrhizae (VAM) in association with
vascular plants. VAM occur worldwide, in most ecosystems, and in approximately 80% of the vascular plant species. The symbiotic relationship is especially important for
grasslands, or on herbaceous plants cultivated as crops.
The relationship is mutualistic, favouring both fungal and
plant partners.
Spores are stimulated to germinate by exudates from
nearby roots. The fungus penetrates the young root, behind
the root tip, with a combination of mechanical pressures
and enzymatic breakdown. Hyphae grow within and between cells in the cortex, forming coils and dichotomously
branched, bush-like arbuscules. They lie between the plant
cell walls and their plasma membranes, greatly increasing
the membrane surface adjacent to plant protoplasts. Bidirectional transport of nutrients occurs between the
arbuscles and plant protoplasts, as well as through the
intercellular hyphae and coils. The fungus is nourished with
soluble carbohydrates from the plant. Hyphae absorb
minerals (especially phosphate ions) from the soil and

Morphogenesis and diversity


Sexual reproduction is unknown in these fungi. Their asexual spores are usually borne singly on hyphae within the
soil. Two major types of spores may be distinguished. One
type is the chlamydospore, which originates as a swollen
hyphal tip. A thick wall is layed down within the enlarged
hyphal tip. The second type, azygospores, are formed below globose hyphal tips, or from hyphal tips having some
other distinct form. A few species form sporocarps that
contain asexual spores. The spores are quite large (up to
800 microns in diameter), and they have dense oily contents
and a thick multilayered wall. They are often some shade of
yellow or brown. Each spore can contain thousands of nuclei, perhaps genetically dierent and providing for genetic
diversity within the hyphal system.
10

ENCYCLOPEDIA OF LIFE SCIENCES & 2008, John Wiley & Sons, Ltd. www.els.net

Zygomycota and Glomeromycota

transport these minerals into the root. The uptake of phosphorous and other minerals enhances plant growth, particularly in phosphorous-decient soils. VAM roots also
have a greater capacity to take up water, and are better able
to withstand drought conditions than plants lacking VAM
fungi. The ability of these fungi to increase mineral and
water uptake is related to the increased absorptive surface.
Very narrow hyphae grow into smaller spaces in the soil
where the larger roots and root hairs cannot penetrate, as
well as to grow away from the root and into new zones
where minerals are available. Hyphae may grow from one
plant to another, forming a nutritional network. Later,
some species form terminal swellings on hyphae within the
root. These are vesicles, which are similar to spores as they
have thick walls and a high lipid content. Vesicles may serve
as storage organs or survival units under adverse conditions (Linderman, 1997). See also: Mycorrhiza

Linderman RG (1997) Vesicular-arbuscular mycorrhizal (VAM)


fungi. In: Carroll GC and Tudzynski P (eds) The Mycota: A
Comprehensive Treatment on Fungi as Experimental Systems for
Basic and Applied Research, vol. 5B, pp. 119128. Berlin: Springer.
Lowe DA (1992) Fungal enzymes. In: Arora DK, Elander RP and
Mukerji KG (eds) Handbook of Applied Mycology. Fungal Biotechnology, vol. 4, pp. 681706. New York: Marcel Dekker, Inc.
Moore-Landecker E (1996) Fundamentals of the Fungi, 4th edn,
674 pp. Upper Saddle River, NJ: Prentice-Hall.
Schipper MAA and Stalpers JA (2003) Zygomycetes: the order
Mucorales. In: Howard DH (ed.) Pathogenic Fungi in Humans and
Animals, 2nd edn, pp. 67125. New York: Marcel Dekker, Inc.
Schuler A, Schwartzott D and Walker C (2001) A new fungal
phylum, the Glomeromycota: phylogeny and evolution. Mycological Research 105: 14131421.
White MM, James TY and ODonnell K (2006) Phylogeny of the
Zygomycota based on nuclear ribosomal sequence data. Mycologia 98: 872884.

References

Further Reading

Benny GL, Humber RA and Morton JB (2001) Zygomycota:


Zygomycetes. In: Esser K and Lemke PA (eds) The Mycota: A
Comprehensive Treatise on Fungi as Experimental Systems for
Basic and Applied Research, vol. 7(A), pp. 113146.
Berbee ML and Taylor JW (2001) Fungal Molecular evolution:
gene trees and geologic time. In: Esser K and Lemke PA (eds) The
Mycota: A Comprehensive Treatise on Fungi as Experimental
Systems for Basic and Applied Research, vol. 7(B), pp. 229245.
Bruns T (2006) A kingdom revised. Nature 443: 758761.
Demain AL and Sanchez SS (2007) Microbial synthesis of
primary metabolites: current advances and future prospects.
In: El-Mansi EMT, Bryce CFA, Demain AL and Allman AR
(eds) Fermentation Microbiology and Biotechnology, 2nd edn,
pp. 99130. Boca Raton, Florida: CRC Press.
Hibbett DS, Binder M, Bischo JF et al. (2007) A higher-level
phylogenetic classication of the Fungi. Mycological Research
111: 509547.
James TY, Kau F, Schoch C et al. (2006) Reconstructing the
early evolution of fungi using a six-gene phylogeny. Nature 443:
818822.
Jeries P and Young TWK (1994) Interfungal Parasitic Relationships. Wallingford: CAB International. 296pp.
Jong SC and Dugan FM (2003) Zygomycetes: the order Entomophthorales. In: Howard DH (ed.) Pathogenic Fungi in Humans and Animals, 2nd edn, pp. 127139. New York: Marcel
Dekker, Inc.
Kuswanto KR (2004) Industrialization of tempe fermentation. In:
Steinkraus KH (ed.) Industrialization of Indigenous Fermented
Foods, Second Edition, Revised and Expanded, pp. 587635.
New York: Marcel Dekker, Inc.
Lacey J and Crook B (1988) Fungal and actinomycete spores as
pollutants of the workplace and occupational allergens. Annals
of Occupational Hygiene 32: 515533.
Lichtwardt RW (1986) The Trichomycetes: Fungal Associates of
Arthropods. New York: Springer.
Lichtwardt RW (1996) Trichomycetes and the arthropod gut. In:
Howard DH and Miller JD (eds) The Mycota: A Comprehensive
Treatment on Fungi as Experimental Systems for Basic and Applied Research, vol. 6, pp. 315330. Berlin: Springer.

Bigelis R (1991) Fungal enzymes in food processing. In: Arora DJ,


Mukerji KG and Marth EH (eds) Handbook of Applied Mycology: Foods and Feeds, vol. 3, pp. 445498. New York: Marcel
Dekker, Inc.
Day JH (1996) Allergic respiratory responses to fungi. In: Howard
DH and Miller JD (eds) The Mycota: A Comprehensive Treatment on Fungi as Experimental Systems for Basic and Applied
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Dix NJ and Webster J (1995) Fungal Ecology, 549 pp. London:
Chapman & Hall.
Frankland JC, Magan N and Gadd GM (eds) (1996) Fungi and
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using amylolytic Rhizopus in Guyana. Mycologia 97: 111.
Isaac S (1992) Fungal-plant Interactions, 418 pp. London: Chapman & Hall.
Johri BN, Satyranarayana T and Olsen J (eds) (1999) Thermophilic Moulds in Biotechnology, 354 pp. Dordrecht: Kluwer
Academic Publishers.
Magnuson JK and Lasure LL (2004) Organic acid production by
lamentous fungi. In: Tkacz JS and Lange L (eds) Advances in
Fungal Biotechnology for Industry, Agriculture, and Medicine,
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Redecker D and Raab P (2006) Phylogeny of the Glomeromycota
(arbuscular mycorrhizal fungi): recent developments and new
gene markers. Mycologia 98: 885895.
Steinkraus KH (ed.) (1996) Handbook of Indigenous Fermented
Foods Second Edition, Revised, and Expanded, 776 pp. New
York: Marcell Dekker, Inc.
Taylor TN, Krings M, Klavins SD and Taylor ED (2005) Protoascon missouriensis, a complex fossil microfungus revisited.
Mycologia 97: 725729.
Taylor TN, Remy W, Hass H and Kerp H (1995) Fossil arbuscular
mycorrhizae from the early Devonian. Mycologia 87: 560573.
Washburn RG (1996) Opportunistic mold infections. In: Howard
DH and Miller JD (eds) The Mycota: A Comprehensive Treatment on Fungi as Experimental Systems for Basic and Applied
Research, vol. 6, pp. 147158. Berlin: Springer.

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