Lecture 05: The Success of Fungi

Introduction

There are around 70-100,000 species of fungi known to science and it is believed there are many species that are yet to be discovered and it is estimated that there may be as many as 1.0-1.5 millions species of fungi (Hawksworth and Rossman, 1997). 

Fungi are one of today's most successful group of organisms. They were even the dominant organisms on earth following mass extinctions at various periods of earth's geologic history. For example following the Permian extinction, about 252 million years ago (Rampino and Eshet, 2018) and at the end of the Cretaceous period (Vajda and McLoughlin, 2004), 90-97% and around 76% of all species became extinct, respectively, during these mass extinctions. With the demise of most organisms during these geologic periods, massive amounts of "food" became available for fungi as evidenced in the fossil records (Rampino and Eshet, 2018).  Today, fungi are still a force to be reckoned with. Some of the characteristics that have led to their sucess are:

• Their ability to exploit a variety of substrates, many not utilized by other organisms.

• The prolific number of spores that they produce, as well as the mechanisms by which the spores are dispersed.

• Most fungi have the ability to reproduce sexually and asexually. Together, both ensures the survival of the species.

Exploitation of Common and Unusual Substrates

Let us examine the above characteristics and see why they make fungi the successful organisms that they are. Many species are decomposers, some are pathogens of plants and less commonly humans (Figs. 1-3). 

A more exotic, but not uncommon substrate for fungi is dung (Figs. 4-6). A large variety of organisms can be found growing on dung.

Unusual substrates that some fungi are known to utilize for food, but usually not other organisms. These substrates include various petroleum products such as kerosene, car oil and even glass can be etched by fungi (Figs. 7-9). Other unusual substrates are CDs, paint and rubber (Figs. 10-12).

Only metals appear to be safe from fungal decomposition.

Reproductive Success of Fungi

In our seemingly infinite universe, Carl Sagan has often estimated that the number of stars and galaxies are in the order of billions. It is seldom that we use such large numbers in describing a characteristic of organisms. However, the number of spores that may be produced by an individual fungus, in some species are often time in the orders of billions and sometimes even trillions. A few examples are listed below (Figs. 13-xx) in which during reproduction, the number of spores produced by a single fungus reproductive unit will be in the orders of billions, if not trillions.

The spores of the above fungi are mostly dispersed to wherever the wind may carry them. However, only a small fraction of these spores will arrive to a favorable environment and land on a substrate that will enable them to germinate and reproduce themselves. Otherwise, we would be up to our ears in fungi. However, because fungi produce spores in such large numbers, there are more than enough spores that survive to make the world the "moldy" place that it is.

Dry vs Wet Spores

The production of large number of spores is only partly responsible for the abundance of fungi around us, but in order for them to become widespread, there must also be mechanisms by which they can disperse their spores. Some of the different mechanisms by which fungi disperse their spores are quite ingenious.

While there are many categories that we can recognize as to how spores are dispersed, Ingold (1953) suggested that one of the most fundamental biological distinctions is between wet and dry spores. Spores that are dry can readily be carried away from their point of origin and are dispersed by wind (Ingold 1953). Wet spores are held together en masse and are are not readily air borne, appear to be dispersed either by water or insect (Ingold 1953).  Dry spore dispersal is the more common of the two. 

Dry Spores Are Air Borne Spores

Dry spore dispersal occurs by riding air currents. These spores do not readily soak up water and when clusters of these spores are splattered by water, as may often occur in those fungi that produce their spores directly on their mycelium, rather than absorbing the water, the impact dislodges the spores and scatters them into the wind. Because these spores do not readily absorb water, they are said to be hydrophobic. Although this may seem counter intuitive, the initial resistance of these spores to water makes a great deal of sense. The absorption of water by spores would give them extra weight, making it more difficult for them to stay afloat. The majority of the known species of fungi disperse their spores by wind are dry spores.

The study of airborne reproductive propagules, which includes all spore producers, e.g., algae, fungi and plants, as well as pollen and other air borne organisms, is aerobiology. One of the significant aspect in this discipline that has been much studied is the cause of allergies by organisms in the air. Fungal spores are the cause of a significant number of allergies each year. Unlike pollen, however, it was not until Feinberg (1946) that fungal spores were discovered to cause respiratory allergies. Three Canadians, who were threshing wheat, were discovered to have allergies that were caused by mold spores of Cladosporium (Figs. 22-23) and Alternaria (Figs. 24-25). In 1937, in Minnesota and the Dakotas, it was estimated that thousands of tons of spores of Cladosporium and Penicillium (Figs. 17-18) were present in the air that blew eastward into the ocean and may possibly have blown across the Atlantic (Feinberg, 1946). Considering the size of spores and the fact that there was an estimated thousands of tons of spores, the number of spores present must have been astronomical.  It is not any wonder then that the above two genera of fungi are significant factors in the cause of allergies. The three, above genera are also the most commonly isolated fungal spores in the outdoor environment (Li and Kendrick 1995; Lee, et al. 2006; Oliverira, et al. 2010) 

Although airborne fungal spores are not visible to the naked eye, an air sample may contain as many as 200,000 spores/meter3. In order to give you an idea as to the number of spores that are in the air, let us make an indirect comparison with small air-borne objects that are visible to the naked eye. You have all probably already observed how small particles have the ability to stay afloat in the air, but just not have given it much thought. If we are sitting in a room, with the curtains mostly drawn shut and we look at sunlight coming through a window, in a room, where the air is still, numerous small particulate pieces of "lint" or dusts, in the light beam can be observed to be kept afloat by the convection of heat generated by the light beam as illustrated in the YouTube video link below.

So it should not be difficult to imagine that spores, which are far smaller and lighter, would and probably are also present in such a light beam. The extent that spores can travel indoors where the air is still was nicely demonstrated with an experiment carried out by Dr. Clyde Christensen (1975), at the University of Minnesota St. Paul Campus, in the plant pathology building.

The Amorphotheca resinae Parbery [=Cladosporium resinae (Lindau) G.A. de Vries] Experiment or "How Fungal Spores Stay Afloat"

About Amorphotheca resinae 

The experiment used Amorphotheca resinae as a "marker fungus" whose spores are not usually found in the air. In nature this fungus is found only in resin permeated soil, and in wood that has been impregnated with coal tar creosote in order to protect them from decay, such as telephone poles and railroad ties.  Because of its requirement for creosote, an agar medium containing this compound is not only required for growth of A. resinae, but at the same time, will prevent the growth of other common air-borne or soil fungi. For those of you unfamiliar with an agar medium, it is a solidified, gelatin medium with nutrient that enables fungi to grow. Examples of nutrient agar plates with molds growing were shown above in Figs 22, 24 and 26.

If a plate with the appropriate nutrient agar is exposed to the air that has fungal spores, it will enable the spores to germinate and grow.

Before beginning the experiment, Christensen wanted to ensure that the spores of this species were not already in the building, petri plates with creosote agar plates were exposed to ascertain if A. resinae was already established in the building or not. After exposing the plates throughout the building the A. resinae was not isolated. 

The Experiment

The four storied, plant pathology building, in which the experiment was carried out, has stairways at each end, with a hallway in the middle of each floor and does not have a central ventilating system. In testing the extent to which the A. resinae spores could remain afloat in the still air of the plant pathology building, agar plates with coal tar creosote were exposed throughout the building. A culture of A. resinae (Fig. 28) was then placed on the first floor hallway and the spores of the fungus were then brushed off the agar surface using a water color brush (Fig. 29), thereby dispersing the spores into the air of the building. 

Remember that Christensen had earlier exposed plates of the creosote agar prior to dispersing the spores and had not recover A. resinae. Thus, the presence of A. resinae was not present prior to the experiment. Therefore, any plates that were now discovered to have this fungus growing on it would be due to the brush dispersal of A. resinae, by Christensen, to that part of the building.  Two of the several tests that were carried out are summarized in Tables 1 and 2. Table 1 summarizes the number of colonies recovered on creosote plates exposed at successive five minute intervals. In Table 2, seven sets of plates were exposed at each location for intervals of 0-5, 5-10, 10-20, 20-30, 30-60, 60-120 and 120-240 minutes, at one minute intervals/plate. All plates were incubated and later examined for the number of colonies of the fungus formed on each plate. Colonies were recorded because it is assumed here that each colony was produced from a single spore. Plates with colonies of A. resinae were isolated throughout the buildings where the creosote plates were placed. As might be expected, there were generally more colonies on plates closest to the source, i.e. on the first floor, where the spores were dispersed and fewer occurred on those plates that were placed on the upper floors, more colonies were recovered in the hallway than in the rooms on the same floor and more colonies were recovered in those rooms with open doors than those with close doors.

While we can readily visualize fungal spores being wind dispersed outdoors, Christensen's experiment demonstrates what was previously illustrated above, in the YouTube video, showing how dust remains suspended in air due to convection of heat in the air. In this experiment, with no air movement, the spores of A. resinae were able to stay afloat to disperse themselves throughout a building, managing to even transport themselves to upper floors and inside rooms where doors have been closed, similar to how dust particles are able to stay afloat. 

The movement of spores indoors is of significance to the aerobiologist. Most of us may not suffer from any respiratory symptoms while outdoors, but once inside we may suffer from difficulty in breathing, have sniffles and perhaps even feel ill. This may occur at work in air-conditioned buildings or at home. Symptoms are more likely to occur at the latter when you are sweeping and vacuuming causing the dust in your house to shift around. It is commonly believed that it is the dust that is the sole cause of your misery, but instead it is more probable that the cause is due to fungal spores (more about this topic later).

Mechanism of Mushrooms & Puffballs Spore Dispersal

In the previous section, we have gone over experiments that demonstrate the ease with which many spores are able to stay afloat, which is an important feature if the spore is to be dispersed over long distances. There are several different mechanisms by which fungi release their spores into the air, which then allows them to be dispersed by wind. One that was mentioned, in the previous section, was the dispersal of basidiospores of mushrooms. This release is accomplished by the forcible ejection of the basidia from the basidiospores. The force that ejects the basidiospores comes about from the internal pressure that is built up in the basidia. When the basidiospores are mature, the pressure in the basidia literally shoots the basidiospores between the gills of the mushroom (Fig. 30). Although the actual distance that the basidiospores are ejected is very short, it is enough to  allow them to drop between the gills, without getting trapped (Fig. 31). Once free of the gills, they can be carried great distances by wind, away from the parent mycelium. The "cloud of spores" that drop from the gills can be seen in the YouTube video below:

 While this is a simple mechanism, it should not be underestimated. In one species of mushroom, Schizophyllum commune, research was carried out, by Raper, et al (1958) that genetically demonstrated that this dispersal mechanism has led to a world-wide distribution of this species. We will, however, not cover the details of this experiment since it is well beyond the scope of this course. There are other mechanisms that serve the same functions of initially ejecting the spores into the air so that they may be picked up by air currents.

 A similar means of dispersal occurs in the Ascomycota. In most species in this phylum, fruiting bodies (Figs. 32-33) are produced that bear ascospores, in asci. The ascospores are forcibly ejected through the top of the asci (Fig. 34) and are then carried away by wind . A YouTube video, below, shows the cloud of spores over the fruiting body after being ejected from their ascus. 

 An equally ingenious means by which spores are initially ejected into the air is the mechanism used by certain puffballs. Although, puffballs are also members of the Basidiomycota the basidium does not forcibly eject the basidiospores into the air to be carried away with the wind. Instead, several different mechanisms have evolved in "puffballs" to disperse the basidiospores.

The most familiar example is in those species in which the basidiospores mature within a hollow, elastic, globular sac called the peridium, which is entirely closed except for the terminal opening, called the ostiole, is where the spores will be ejected. The energy to eject the spores is entirely external and is usually provided by either the impact of raindrops and/or the inadvertent bumping of the peridium by small animals. The depression of the pliable peridium, usually by one of the two external force, causes the spores within to be ejected in a "puff" of smoke-like spores. Thus, the common name "puffballs". Geastrum fimbriatum and Lycoperdon pyriforme, Figs. 26, and 27, respectively are examples of puffballs. A YouTube video, below, shows both species demonstrating the described mechanism above by which spores are released.

Distances That Spores are Dispersed by Wind

The distances that fungal spores are dispersed, outdoors, are equally phenomenal. Puccinia graminis (Wheat Rust) has been studied extensively because of its economic importance. The disease has probably been known since the beginning of agriculture and even today the occurrence of wheat rust results in billions of dollars in losses, annually. During the Spring, the urediospores from infected wheat plants are carried northward, from northern Mexico, into the United States, from southern Texas, over the Great Plains and into Canada. During the Fall, the urediospores are carried southward, back down into the wheat growing region where the young winter wheat is beginning to grow. Studies carried out over almost a thirty year period, have traced the path of wheat rust epidemics along this route.

Related to how far spores can travel is how high can spores be found. Not only are spores known to travel great distances, but have also are known to go up to high altitudes. In the early days of aerobiology, during the 1930s, planes flying at 10,000 feet commonly recovered fungal spores from that altitude. It is probable that they could have recovered spores at much higher altitudes, but because of the cold and the requirement of oxygen mask at higher altitudes, the scientists doing such studies were not quite as curious about fungal spores beyond 10,000 feet. Even at the altitudes in which studies were carried out, it was the graduate students that took the risk of actually going up in the planes to sample for fungus spores. However, it should be kept in mind that the 1930's such research was looked upon with more glamour since such flying involved a great deal more risk at that time and such "missions" were considered very daring and brave on the part of the graduate students. In the 1930's, even Charles Lindbergh, in collaboration with the United States Department of Agriculture, participated in surveying spores while he was flying over the Arctic Circle. Although he was flying lower, only 3,000 feet, compared to the 10,000 feet above, Lindbergh was able to catch what was described as a "considerable number of spores". This was of interest since Lindbergh was above the open ocean far from land, giving us an indication as to how far these spores must have traveled.

More sophisticated experiments utilized balloons to find spores in still higher elevations. In 1935, the balloon Explorer II, containing a spore trapping device was released at an altitude of 71,395 feet and was set to close once the balloon reached 36,000 feet. Although only five living spores were recovered, think of the conditions in which the spores faced at elevations between 36,000-71,000 feet. The air must have been very thin at that altitude and the temperatures must have been below freezing. Wind was also measured by the Explorer II. At the elevations in which the spores were trapped, winds were measured at 40-60 miles/hours. If winds remained constant at those elevations, it was calculated that fungal spores up in this jet stream could be carried 8,400 miles in a week.

The above experiments not only provided results that demonstrated that fungal spores are capable of traveling long distances, but whether they can survive these environmental conditions in doing so was not determined.

Although wind dispersal of dry spores is the means by which they travel all over the world, other means of spore dispersal are also found in other fungi. Although these other mechanisms are utilized by far fewer number of species, they are nevertheless interesting mechanisms that deserve a cursory coverage.

Wet Spore Dispersal

Where wind dispersed spores are hydrophobic, water dispersed readily absorb water and are said to be hydrophilic.  Water dispersed spores often produce their spores in "slime". Due to the weight of the slime, wind dispersal is impossible or at least impractical. What occurs in these spores is that when large amounts of water is present, during a rain or in area where there is water flowing freely, such as in a stream, the spores are carried away, passively. The spores are characteristically shaped, usually with long appendages or are coiled (Fig. 28). The spores stay afloat due to the surface tension of the spore or air pockets in the spores. The major source of food for these fungi are from leaf litter and other plant material that may fall into streams. 

Insect Dispersal of Wet Spores Borne in Slime

The most interesting dispersal mechanism can be found in the group of fungi that are commonly referred to as stinkhorns because of their unpleasant odor. These fungi produce their spores in a usually liver-brown slime, i.e. they are wet spores, which is on top of a colorful part of the fruitbody. See Figs. 29 and 30.  When the spores are mature and exposed to the external environment, the odor of the spores will attract flies that will eat up the slime and spores thereby dispersing the fungus. The number of spores produced in these fungi are far fewer than in the dry spores. This is likely that in this group the efficiency of its dispersal has a higher success rate than dry spores that are disseminated by wind. A YouTube video, below, show flies congregating and eating the slimy spores on the fruit body of a stinkhorn.

YouTube Video showing flies flies congregating and eating gleba of Phallus

Birds Nest Fungi Spore Dispersal

It is difficult to know where to put some mechanisms of dispersal. There are actually more than one mechanism involved in the group of fungi known as the bird's nest fungi (Fig. 31). The common name of this group of fungi is due to the strong resemblance that the fruiting body has with a birds nest. Prior to 1790, they were thought to be flowering plants and the eggs, which contains the spores of the fungus, were thought to be the seeds of the plant. The actual dispersal mechanism of this fungus was not discovered until the 1940's by Dr. Harold Brodie, a mycologist that devoted his career on studying this group of fungi.

How Brodie determined the mechanism is an interesting story. However, before telling his story, let's look at the composition of the a fruiting body of a birds nest fungus (Fig. 32). The 'eggs' that contain the spores are called peridioles. There are usually several peridioles per nest  attached to the inside by means of a slender connection that is folded up called a funiculus. If we moisten a peridiole and pull the funiculus out, it may stretch up to 6 to 8 inches and at its base is a stick area, the hapteron that will adhere to any surface that it touches.

Before Dr. Brodie determined the mechanism, mycologists believed that the peridioles must have been shot into the air by some explosive force generated by the fungus itself since such of mechanisms are known to occur in some groups of fungi. However, long observations failed to detect any such explosive mechanism. Brodie determined that the nest was so constructed that when a raindrop splashes into the nest, the force will eject the peridiole out of the nest up to a distance of 3-4 feet. The force of ejection causes the funiculus to unwind and if the now wet and sticky hapteron comes in contact with any object as it flies through the air, it will stick to that object. Once attached the cord stretches and winds around the object. This all takes place very quickly. The peridiole is now in contact with a substrate where it can grow. This mechanism is illustrated in Fig.32 and on a YouTube Video below:.

Active Mechanisms of Spore Release

Active mechanism of spore release refer to those fungi that are able to eject their spores using energy from within their mycelium or fruitbody. These can be divided into subcategories:

Explosive Mechanisms: A common means of forcible spore discharge is that in which a cell contains a large vacuole through which greater and greater pressure is applied as water comes into the cell. Eventually, the vacuole will explode releasing the spores in a jet stream of water and the fruiting structure collapses. You saw an example of such a fungus in the video, The Moldy World About Us.

The genus Pilobolus (Figs. 33-34) forcibly ejects an entire Sporangium (Zygomycota) approximately 4 feet away and the swollen portion of the sporangium also serves as a light receptor that curves the stalk of the sporangium so that it shoots the spores in the direction of the light. The spores of the sporangium are in a slime layer so that the entire mass of spores are dispersed as a unit. As you recall the distance here is important because Pilobolus is a dung inhabiting species and the spores must be dispersed beyond the dung heap that it is growing on because the cow will not graze within a certain distance of their dung heaps. And it is important that the cow eat the spores, in order that they will go through their digestive system, and come out with the dung to start the next generation. A YouTube video below shows the ejection of the entire sporangium from the top of the sporangiophore.

Animal Dispersal

By examining the fruitbodies of some puffballs, there do not always appear an obvious means of dispersal. In some genera, it is believed that such puffballs are adapted for dispersal by animals. Foraging animals often consume these fruiting bodies. The spores of these fungi are able to pass through their digestive systems unharmed and will be dispersed in their fecal material. Rhizopogon (Figure 35) and Tuber melanosporum (Figure 36) are two common examples.

I hope that you can now appreciate the means by which fungi are able to get around. There are more interesting mechanisms and we do not have time to cover these others. The mechanisms mechanisms covered represent the most common I have included a few of the more interesting ones.

Some Fungi Do Not Disperse Their Spores

The majority of fungal spores are dispersed, away from the parent mycelium, where they are more likely to have a fresh food supply thereby increasing their chances for survival. However, some fungi may produce resting spores that are not dispersed, but instead become dormant, waiting for favorable conditions to return before germinating . Some common examples of thick walled resting spores are below (Figures 37-39):

Sexual vs Asexual Reproduction

Most organisms with which we are familiar reproduced by sexual reproduction. That is there are two parents, each contributing characteristics to the progeny that they will produce, making each progeny genetically different. Being genetically different is of selective advantage for the survival of species. For example, if a a species come in contact with a fatal disease, genetic differences for each individual of a species will make it more likely that some of the members of the disease may carry genetic information that will allow it to survive or be immune to the disease. However, if members of a species is genetically identical to one another, and one member should contract a disease that proves to be fatal, then all members of the species will die from the disease since all members are genetically identical. But this does not mean that asexual reproduction does not have its advantages. Many fungi have both asexual and sexual reproduction and utilize both types of reproduction to their advantage. Lets look at one example, Black Stem Rust, a disease of wheat and other grains.

Two of the spore stages that are produced by the Black Stem Rust fungus are the rusty colored, urediospores and the black teliospores (Figs. 40-41). The latter will reproduce itself asexually during the spring and late summer, spreading rapidly through an entire wheat field because asexual reproduction rate is more rapid than sexual reproduction. through out the spring and into late summer because of the rapid rate in which reproduction can occur, asexually, the disease will spread rapidly throughout the wheat field. and the former has thick cell walls that allow it to withstand the cold winter, and when spring returns, will produce sexual spores that are genetically different, the following spring. 

Literature Cited

Arora, D. 1986. Mushrooms demystified: a comprehensive guide to the fleshy fungi. Berkeley: Ten Speed Press.

Christensen, C.M. 1975. Molds, Mushrooms, and Mycotoxins. University of Minnesota Press, St. Paul.

Feinberg, S.M.  1946. Allergy in Practice. 2nd. Ed. Chicago. The Yearbook Publisher, Chicago.

Hawksworth, David L. and Amy Y. Rossman. 1997. Where are all the undescribed fungi? Phytopathology 87: 888-891

Ingold, C. T. 1965. Spore liberation. Clarendon Press, Oxford. 210 pp.

Lee, T., S. A. Grinshpun, D. Martuzevicius, A. Adhikari, C. M. Crawford and T. Reponen. 2006. Culturability and concentration of indoor and outdoor airborne fungi in six single-family homes. Atmos. Environ. 40: 2902-2910.

Li, D. W., B. Kendrick. 1995. A year-round comparison of fungal spores in indoor and outdoor air. Mycologia 87: 190-195.

Oliveira, M. H. Ribeiro, L. Delgado, J. Fonseca, M. G. Castel-Branco and L. Abreu. 2010. Outdoor Allergenic Fungal Spores: Comparison Between an Urban and a Rural Area in Northern Portugal. J. Investig. Allergol. Clin. Immunol. 20: 117-128.

Rampino, M.R. and Yoram Eshet. 2018. The fungal and acritarch events as time markers for the latest Permian mass extinction: An update. Geoscience Frontiers 9: 147-154

Raper, J. R., Krongelb, G. S. & Baxter, M. G. 1958. The number and distribution of incompatibility factors in Schizophyllum commune. American Nat. 92, 221-232.

Vajda, V. and Stephen McLoughlin. 2004. Proliferation at the Cretaceous-Tertiary Boundary.Science 303: 1489

Important Terms and Concepts 

Dry spores: Referring to air-borne spores that are hydrophilic. Their ability to not take up water enhances their ability to remain air-borne. These spores are normally wind dispersed.

Hydrophilic: Have an affinity for water; readily absorbing water.  Hydrophobic: Having an aversion to water and tending to repel water.

Dormancy: Stage in which an organism is metabolically inactive, waiting for favorable conditions to return, at which time growth will resume. Stage is often referred to as a resting stage.

Wet spores: Spores that are borne en masse and not readily air-borne. These spores are hydrophilic and are normally water or insect dispersed.

Learning Goals

1.  What reasons can you give as to why fungi are successful organisms?

2.  What are some unusual substrates that fungi can utilize for food?

3.  What is the only type of substrates that are probabaly safe from decomposing fungi?

4.  What are hydrophobic vs hydrophilic spores?

5.  What is the most likely mechanism of dispersal for fungi that have “dry” spores?

6.  What are some examples of dispersal mechanisms of fungi that have wet spores?

7.  How do stinkhorns disperse their spores?

8.  How do fungi that produced fruitbodies usually disperse their spores?

9.  What are some specific mechanisms by which some puffballs disperse their spores?

10. What is thought to be the reason that Pilobolus spore masses disperse away from their point of origin?

11.  Why do dry spores stay afloat, as seen in the experiment by Christensen?

12.  How are spores from fruiting bodies that are buried underground dispersed?

13. Resting spores do not disperse. What is believed to be the reason for the lack of dispersal in these Fungi?

14.  What are the advantages/disadvantages of sexual and asexual reproduction?