“One side of what?”
“…and the other side will make you grow shorter.”
“The other side of what?”
“The mushroom, of course!”
Alice in Wonderland by Lewis Carroll, 1865
|Modified original image from shockya.com|
In that manner, with a slender stem and elegantly radiating gills, this graceful beauty seemed to suddenly appear. Xerulae are members of phylum Basidiomycota whose constituents produce fruitbodies that include mushrooms, toadstools, puffballs, bracket fungi and the like. The phylum’s name is derived from the “basidium”, a region of microscopic, specialized club-shaped cells that both manufacture and release spores.
|A mirror allows the gills to be photographed while illuminating the cap’s shadowed undersurface.|
The gills are the spore-bearing structure of the mushroom.
Imperceptible to the naked eye, the lawn beneath the cap was being showered by spores.
|A deadly poisonous Omphalotus illudens fruiting just down the street|
MY MYSTICAL MYCO-MISSION
Every summer and early fall, my New England home hosts an enormous variety of these otherworldly “plants”. Their grotesque beauty, staggering diversity and fascinating biology inspired me to initiate this mycological journey. With an estimated 77,000 named species and a possible 1.2 million in existence according to mycologists who study them, what better place to start than in my own backyard and down the street.
IS A SPORE THE SAME AS A SEED?
The seeds of plants and the spores of fungi serve analogous functions, but differ in how they go about it. Seeds contain a small, multicellular, embryonic form of a plant, whereas most spores are single, unicellular reproductive cells. There’s no little fungus within the spore.
And unlike seeds, spores are capable of developing into a new individual without fusion with another reproductive cell. Spores are haploid (half the chromosomal number with a single set of chromosomes) and germinate into a haploid fungus; whereas, seeds are diploid (a full set of chromosomes, one from each parent) and form a diploid plant. We'll clarify that later.
|Mushrooms are a pizza topping and a kind of fungal reproductive structure|
FUNGI ARE MICROSCOPICALLY UNIQUE
Fungi lack xylem and phloem tubules, the vascular transport system of plants, yet the cytoplasm contained within its cells flows freely to provide nutrition. For rigidity, fungi have cell walls made of chitin (like a crab's exoskeleton), whereas plants have a cellulose cell wall. In contrast, animal cells possess a non-rigid, permeable cell membrane that facilitates motility of which fungi and plants are incapable. In common, the nuclei of all three are enclosed within nuclear membranes, and as we shall see, that has assisted in their classification.
|Modified from mrskingsbioweb.com|
IS FUNGUS A PLANT?
It seems like a simple question, but it’s tortured taxonomists for ages (biologists with a classification fetish). In 450 BC, the Greek philosopher Theophrastus viewed mushrooms as plants missing certain organs. Indeed, fungi resemble plants in that they lack mobility and grow from below ground, but beyond that the two have little in common. Most obvious, mushrooms are leafless and certainly not green. They differ from plants, which are capable of manufacturing nutrients by photosynthesis.
Instead, fungi obtain nutrients by enzymatically breaking down and absorbing materials from a decaying or dying host. Think of it as “external” digestion. Unlike animals that ingest and then digest, fungi digest and then ingest.
As we all know, plants thrive in sunlight, while mushrooms prefer darker, shaded environments that tend to be moist and less dehydrating, where spores are happiest to generate, disperse and germinate. Fungi are clearly different from plants at all levels of inspection.
IF FUNGI AREN’T PLANTS, WHAT ARE THEY?
In the scheme of things, the placement of fungi has been extremely problematic. In 1735, Carl von Linne (aka Carolus Linnaeus, the father of modern taxonomy and of binomial nomenclature fame) lumped all living things big and small into two large kingdoms: Regnum Vegetabile and Regnum Animale. In his own words, “God created, Linnaeus organized,” but he erroneously placed fungi in the plant kingdom.
Incidentally, Linnaeus had a third kingdom for minerals called Regnum Lapideum, which is the source of the phrase “animal, vegetable or mineral.” In time, the inadequacies of a two kingdom system became obvious. In 1836, Mycology developed as a branch of Botany in spite of taxonomic uncertainty and misconceptions.
TWO BEGETS THREE
With the advent of light microscopy that allowed observations of cellular detail, it became apparent that not all lifeforms fit neatly into one of two categories. In 1866, Ernst Haeckel abandoned the two kingdom system for a three kingdom one based on unicellularity (Kingdom Protista) and multicellularity (Kingdoms Plantae and Animale). Recognizing many differences between fungi and plants, he moved Fungi out of Plantae into Protista but later changed his mind.
THREE BEGETS FOUR
This time high-resolution electron microscopy led to a four kingdom classification by Herbert Copeland in 1938. His Monera (named after a Romanian village) included two groups of single-celled organisms that lacked a nucleus: bacteria and cyanobacteria. Prokaryotes (“before the kernel”) were also single-celled that had a nucleus (the kernel), but the nucleus lacked an enclosing membrane.
|The DNA of prokaryotic cells is located within a nucleoid region (left) and lacks a |
surrounding membrane. Eukaryotic cells have a nucleus that is membrane-bound (right).
The understanding of fungi was advancing, but they were still considered plants.
FOUR BEGETS FIVE AND FUNGI ACQUIRE THE RECOGNITION THEY DESERVE
In 1969, the five kingdom system of Robert Whittaker differentiated between prokaryotic cells (with a nucleus but without a nuclear membrane) and eukaryotic cells (with both nucleus and membrane). Finally, fungi was finally designated kingdom status, but, as we know, taxonomists are never content with the status quo.
FROM FIVE KINGDOMS TO THREE DOMAINS
In an attempt at simplification (and further confuse us all), Carl Woese in 1977, armed with tools of molecular genetic analysis based on ribosomal RNA, revised the classification from five kingdoms down to three domains: Archaea (a new superkingdom of ancient prokaryotes capable of survival in extreme environments); “true” Bacteria; and Eukaryota.
The previous Kingdoms Fungi, Plantae and Animalia became members of Eukaryota, since their nuclei are membrane-bound. Monera and Protista became obsolete, because their lifeforms were paraphyletic, not derived from the same ancestors and hence unrelated.
|Phylogenetic tree based on rRNA analysis|
IS THERE A COMMON ANCESTOR?
Recent molecular evidence strongly suggests that fungi are more closely related to animals than to plants in that they share a common, unicellular eukaryotic ancestor (a choanoflagellate). What a complete surprise this would have been to Linnaeus who placed fungi within the plant kingdom!
In addition, the thought that photosynthetic organisms were the first to evolve, since they were utilized by heterotrophs as food (an organism unable to obtain its carbon from carbon dioxide and instead feeding on organic material), is in question. That makes the evolutionary origin of fungi important in determining the phylogenetic relationships of the other members of Eukaryota.
WHAT DOES ALL THIS MEAN?
As we look increasingly deeper into the structure of the cell, the diversity of life has become far more complex than envisioned. Understanding the classification of fungi helps us to better appreciate their unique biological attributes, and once recognized, Kingdom Fungi has remained an independent group of organisms.
THE MANY PHYLA OF KINGDOM FUNGI
Fungi are further subdivided into phyla (at least four) and even subphyla, all ending with the suffix “-mycota.” Even at this level, fungi classification has plagued mycologists, who debate such erudite topics as "true" fungus versus "funguslike." Here's one version with three phyla but four groups.
Rising above the subtleties of fungal phylogenetics, the various phyla of fungi are distinguished and classified by their differing modes of reproduction and sexual reproductive structures. The majority of the fruiting bodies we see in nature such as mushrooms are produced by members of phylum Basidiomycota. That's what's sprouting all over my neighborhood! So let's investigate mushrooms further.
INSIDE THE MYSTICAL LIFE CYCLE OF A MUSHROOM
The fungi of Basidiomycota follow a reproductive cycle that involves the production of spores. Spores released by mature mushrooms begin forming a colony in moist soil when environmental conditions and a suitable substrate are favorable.
Spores are very picky as to where they germinate and the time of year. The development of fruitbodies (mushrooms) characteristically doesn't occur during intense cold or dry weather, but that doesn't mean that within the soil, the parent fungi are not reproducing. Also, of great importance is the soil's organic content, pH (which is modified by the presence of tree type), and the particular substate of the decaying host. Many fungus prefer certain trees under which and on which to thrive.
Spores germinate by sending fast-growing, slender, branching filaments underground called hyphae, its feeding structures.
|Colored SEM of the fungal hyphae of Penicillium sp.|
Used with permission from psmicrographs.co.uk
Eventually, the hyphae form a web-like system called a mycelium (Greek for fungus) that permeates through the soil and into its food source. This matrix of intersecting membranes is virtually under every step we take on the ground. Sink a shovel into the soil, and it transects billions of unseen mycelia. More than 90% of plants have a fungus associated with their roots (a mycorrhizae symbiont). It’s the largest biological entity on the planet! Paul Stamets of Fungi Perfecti says “The world is a mycelial mass.”
In fact, the largest single organism on the planet consists of one massive mycelium confirmed by DNA fingerprinting. It's a 2,400 year old, 2,384 acre, conifer-killing, honey fungus called Armillaria that is growing beneath the surface in Oregon's Blue Mountains.
|Root-like, white mycelial strands called rhizomorphs are on this overturned rotting log.|
Mushroom emergence begins when the mycelium penetrates the surface as a knot of hyphae called a button. Some buttons germinate wrapped in tissue called a “universal veil” that remains as scales on the mushroom’s cap, while others possess a “partial veil” under the cap that later appears as a ring (annulus) on the stalk.
The body of the mushroom is filamentous like the buried mycelium, being composed of hyphae that cytoplasmically-communicates with the mycelial “root” structure. Hyphal cells are compartmentalized into segments by ladder-like rungs called septa that are perforated for nutritional conveyance (see inset below).
|Modified from flora-balance.com|
Eventually, a stalk and cap develops as the mushroom prepares for reproduction. Spores are produced on the underside of the cap within the basidium, as mentioned, the spore-producing organ that lends its name to phylum Basidiomycota. Spores cover the basidia of gilled mushrooms, the interior surface of tiny tubes in polypore mushrooms, and the spines of tooth fungi.
|A gilled mushroom of Phylum Basidiomycota. Other members have teeth and tiny tubes on the basidium.|
This one-inch Ganoderma lucidum, a bracket fungus, is just emerging through yard mulch. Notice the tiny holes on the basidium beneath the cap. Spores are produced within tubes that line the underside of the fruitbody and give it a perforated appearance. For this reason, this group of Basidiomycota are sometimes called "polypores."
|We’re looking upward (into a mirror) at the spectacular basidium of a mushroom of phylum Basidiomycota. |
Its radiating gills are the spore-producing structures.
In mushrooms of Basidiomycota, minute spherical basidiospores are attached to the basidium by a hilar appendage. Each spore contains one haploid nucleus with a single set of chromosomes. I'll attempt to make sense of that in a minute.
Mushrooms release spores into the flow of air beneath their caps with the intent of dispersal away from the parent. The basidium literally shoots the spores into the air using a hydraulic, spring mechanism. A tiny water droplet called a Buller’s drop (A) forms at the base of the spore in response to its release of a hydrophilic (water-loving) sugar. The sugar solution draws moisture from the air causing the drop to grow. As the surface tension lowers, the drop suddenly snaps onto the spore, akin to adjacent water droplets that snap together. The force catapults the spore away from the basidial tip (B) to populate the wind.
|A Buller's drop catapults the spore from the hilar appendage|
Modified from Carlile & Watkinson, (1994)
Most spores take advantage of the wind for dispersal, although some rely on insects and small animals as vectors of dissemination. Tiny spores (some no more than 10 µm) translates into travelling great distances. Once ejected, gentle breezes carry fungal spores aloft, millions per cubic meter, along with plant pollen, bacteria and viruses. The air is “full of invisible biology.” We’re bathed in it and consume it with every breath. They shower the earth and fall upon everything, as hayfever sufferers well know.
|A spore print is helpful in identifying mushrooms based on spore color, brown in this case.|
Notice the basidium lining the gills on the cap’s underside, the reproductive structure of the mushroom.
|Left overnight, the basidium showers the paper with billions of spores that mimic the structure |
of the mushroom's gills. This is an infinitesimally small fraction of what becomes airborne.
Mother Nature discharges gargantuan numbers of spores (2.7 billion daily per fruiting body at 31,000 per second), but most of them fall on dry, nutritionless hostile substrates. It’s the mathematics of survival. The plan is that a large number of “inoculating” spores will eventually alight on preferential food sources and begin to germinate. In her wisdom, she not only created spore-producing factories and spore-launching catapults but designed aerodynamic spores for optimum dispersal.
|A myriad of shapes of spores facilitate their catapultation through the air.|
From Ernst Haeckel’s "Kunstformen der Natur" and WikiMedia Commons
“MAKIN’ LOVE IN THE DIRT”
Fungi’s mode of reproduction differs significantly from other lifeforms and is a complex process. Depending on the species and the environmental conditions, fungi may reproduce sexually or asexually (or even both, about one-third), but the majority of species require sex between consenting colonies.
Asexual spores are produced by mitotic cell division. It occurs by budding or simply when a mycelium fragments apart. The mushroom produces genetically identical, DNA-copied, clonal spores. Asexual reproduction might seem to lack advantages since genetic exchange and diversity does not take place. But, it produces large number of spores quickly, a huge survival benefit.
Sexual reproduction, on the other hand, occurs by the process of meiosis. It requires two organisms and occurs with the fusion of hyphal nuclei within the basidium. Since DNA is exchanged, genetic diversity is ensured amongst the offspring. That provides “raw material” for natural selection to act upon and sets the stage for evolution to occur.
THE SEXUAL LIFE CYCLE OF A MUSHROOM (HOPEFULLY MADE REALLY SIMPLE)
The reproductive challenge for the parent fungus is to produce a spore on its mushroom for the next generation. The spore must be haploid (written as n), which contains a nucleus from each parent (that's why it's sexual reproduction) with a single set of unpaired chromosomes. In that regard, a spore is similar to a sperm and egg. But spores don't merge. There are no fungal males and females, and the spores actually form a new fungal organism BEFORE exchanging genetic information.
Here's what it looks like visually. It's easier to see the process.
|From the Diversity of Fungi by Mark Steinmetz and ca.bdol.glencoe.com|
STEP BY STEP GUIDE TO THE LIFE CYCLE OF A MUSHROOM
A – Haploid (n) spores are released from the basidium.
B - Once dispersed, spores germinate and form a haploid (n) mycelial network.
C - Suitable hyphal mating types (+ or -) attract, followed by cytoplasmic fusion but without nuclei fusion (called plasmogamy). The new dikaryotic (two kernels) mycelium (n + n) has two unfused nuclei per cell (called the heterokaryon stage).
D – The dikaryotic mycelium grows and forms a button below the surface.
E - As a mushroom forms, two nuclei in each cell fuse on the basidium forming a diploid (2n) nucleus (called karyogamy).
F– Each diploid nucleus undergoes meiosis (cell division halving the chromosomal number) and forms four haploid (n) nuclei, which develop into spores (zygotes). The spores are ready to be released to the environment, genetically “new” (sexually) rather than mitotically-cloned (asexually).
Please accompany me through my neighborhood on post Part II to see what sprouted overnight. Here’s a few samples. Can you identify them?
|This young mushroom, possibly a Pluteus, is just beginning to emerge.|
|These delicate bracket fungi Trichaptum abietinum are fruiting on a downed conifer.|
|This white, spherical puffball is precariously fruiting on a rotting branch.|
Its spores are produced within the fruitbody and are discharged when provoked.
|This common and highly recognizable red-capped mushroom of Genus Russula |
has skin that can be pulled off but is brittle when handled, a depressed cap and a striated margin.
With great appreciation, I thank professional mycologist Taylor Lockwood and amateur “mushroom expert” Michael Kuo for their expertise in identifying many of the more obscure mushrooms in my neighborhood. Their respective links are below.
VERY INFORMATIVE PUBLISHED RESOURCES
Kingdom Fungi by Steven L. Stephenson
Mushroom by Nicholas P. Money
Mushrooms Demystified by David Arora
Mushrooms of Northeast North America by George Barron
Mushrooms, Simon and Schuster’s Guide by Gary H. Lincoff
VERY INFORMATIVE LINKS
Tom Volk here
Michael Kuo here
Michael Wood here
Taylor Lockwood here
North American Mycological Association here