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Biology of FUNgi

Lecture 3Fungi and the three domains

A look back

• What were the unique features of fungi?

• How would you briefly define fungi -exceptions?

• Which of the characters were shared withanimals, which with plants?

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Fungus of the day - Tubermelanosporum

Taxonomy: Phylum (subphylum) Ascomycota Order - Pezizales (Tuberales) Family - Tuberaceae Common names: Perigord Truffle

Characteristics: Peridium black, covered with wartsSporocarp solid and hardHymenium dark, with paler sterileveinsSpiny, with connecting ridges

Four ascospores in an ascus.The spores are notdischarged, but remain inthe asci until digested byfungivorous animals

Fungus of the day - Tubermelanosporum

Importance: T. melanosporum is a highly valuededible. The going price recently was $635.

Related organisms: Tuber gibbosum a North Americannative, equally edible truffle; Tuber magnatum theItalian white truffle

T. magnatum is equallyhighly priced, andpreferred by italians

T. gibbosum - Oregonwhite truffle

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A look ahead...

• We will continue to sum up the features shared byplants-animals-fungi.

• With all this information we will start arguingwhere do the fungi belong in the greaterevolutionary scheme.

• Then, we focus on the fungal life styles.

Fungi vs. animals vs. plants

The point: Fungi have similarities with Plantae and Animalia.Yet, they have distinct and unique features too. Based onthese characters it is hard to tell whether to put fungi next toplants or animals.

Fungi Plants AnimalsCell wall Yes Yes NoCell wall material Chitin Cellulose (Chitin)Central vacuole Yes Yes NoChloroplasts No Yes NoOrgan differentiation No (or poor) Yes YesStorage compounds Glycogen Starch GlycogenSterols Ergosterol Plant sterols Cholesterol

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To The Life Styles – Why focus on thefungal lifestyles?

• Heterotrophism is characterized byacquisition of energy and carbon from onesource or another without photosynthesis.

• The nutritional mode (the source of nutritionor the way of nutrient acquisition) allows usto characterize broad functional groups oforganisms beyond taxonomic boundaries.

Symbiotic vs. free-living fungiFree-living fungi are independent of aliving partner. In other words theyacquire their nutrition by utilizing deadtissues or organic material.

These fungi are often calledsaprotrophic. Saprotrophic fungi canderive their carbon and energy without aliving host.

In contrast, biotrophic (symbiotic) fungilive in a close association with a host.Symbioses in the broad sense includeamensalism, parasitism, mutualism andcommensalism. Competition may alsobe included.

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Different types symbioses (de Bary)Organism A

Org

anis

m B

+ 0 –+ Mutualism Commensalism Parasitism

(Predation)

0 Commensalism Neutralism Amensalism

– Parasitism Amensalism Competition(Predation)

Biotrophic fungi - examples

Biotrophs - organisms acquiring their energy andcarbon via biotrophism, i.e. from livingorganisms.In the past, the biotrophs were those organismswhich could not be cultured on artificial media(agar plates with mineral or organic nutrients).

Vesicular arbuscular mycorrhizaeare typical biotrops - incapable ofliving without their host plant

Cordyceps spp. arebiotrophs of different sort -they colonize living hosts.Here Cordycepsmyrmecophila parasitizedan ant finally killing it.

Trichophyton rubrum may parasitizehumans and cause lesions in thetissues. Here, on the foot.

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Facultative vs. obligatebiotrophy

The degree of the association may varyas well. Some fungi are obligatebiotrophs, some facultative. Facultativebiotrophs can have an alternativenutritional mode, i.e., they can utilizedead material if the living hosts are notavailable.Compare facultatively biotrophic root-inhabiting fungi and arbuscularmycorrhiza.

Vesicular arbuscular mycorrhizaeare typical biotrops - incapable ofliving without their host plant

Root endophytes (colonize space within the cell) inplant tissues. They grow also without their hosts andhave enzymatic systems to decay cellulose, pectinsand other complex organic molecules.

Saprotrophic fungi examples

Saprotrophs - organisms acquiring theirenergy and carbon via saprotrophism, i.e.from non-living substrates.Traditionally, these were the organisms thatmycologists could grow in pure culture(artificial medium) without the living host.

Serpula lacrymans is a typical saprotrophobtaining its energy and carbon by decayingtimber, i.e., attacking non-living carbonsource.

Pilobolus - a zygomycete - is among themost common coprophilic (poop-inhabiting) fungi

Pleospora - an ascomycete - is amost common saprophyte on deadherbaceous stems

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In summary,...

• Fungi have evolved different strategies to obtainthe energy and carbon.

• Some utilized dead organic materials, somecolonize living tissues living in a mutuallybeneficial association or causing damage and harmto the host. Some - pathogens - may even kill theirhosts in the process.

• In brief, there is substantial diversity in the styleswhich fungi utilize to go about their everydaybusiness.

To the classification: Threekingdoms, or five?

Until very recently, life has been viewed divided infive kingdoms. Whittaker (1969: Science163, 150-160) recognized the artificial three kingdomclassification; he proposed five.

Monera - unicellular prokaryotes, occasionally motileby flagellumProtista - unicellular eukaryotes, occasionally motileby flagellum or ciliaFungi - uni- or multicellular eukaryotes, motile(flagella) or non-motile, exception ChytridsPlantae - multicellular eukaryotes, non-motileAnimalia - multicellular eukaryotes, motile bycontractile fibers

AnimaliaFungiPlantaeProtistaMonera

Animalia

PlantaeProkarya

Where did fungi go in the threekingdom classification?

Whittaker, 1969

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Five kingdoms, or threedomains

Basically, the five kingdom system wasartificial and biased towards theeukaryotes. They are macroscopic, haveclear morphological characters toobserve, and can be observed withoutspecial high-fidelity tools.

Molecular tools caused a revolution inour view of the microbial world. It wasestimated that as little as 1% of microbescould be cultured (DNA reassociation orhybridization analysis).

AnimaliaFungiPlantaeProtistaMonera

From Pace 1997 Science 276: 734-740.

Finally, three domains

By comparison of ribosomal RNAsequence data, Carl Woese (1977; PNAS74:5088) realized that the genetic distancesamong Monera were far greater than thoseseen in the Eukaryotes.

Suddenly, most of the diversity of life wasin Monera, not Eukarya.

It also seemed that all respiratory andphotosynthetic capacity in Eukarya wasfrom bacterial symbiont - support for theendosymbiosis hypothesis.

AnimaliaFungiPlantaeProtistaMonera

From Pace 1997 Science 276: 734-740.

Chpl Mit

Root?

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Fungi in three domains

Looking at Fungi, Protista, Plantae andAnimalia, there seems to be a need foradditional eukaryotic groups.

Some organisms historically considered asfungi were among those groups that mightfall into phyla of their own - e.g.Dictyostelium - a cellular slime mold,Physarum - a true slime mold.

There is a need to recognize the “crowneukaryotes” and separate them from the restof the Eukarya.

AnimaliaFungiPlantaeProtistaMonera

From Pace 1997 Science 276: 734-740.

Fungi in three domains

Baldauf and Palmer used several proteincoding gene sequences (α-tubulin, β-tubulin,elongation factor [EF-1α] and actin).

In analyses using these sequence datacongruent results point out:

1) Fungi as known in five kingdoms waspolyphyletic. Slime molds (and oomycetes)were clearly protistan2) Animals and fungi (true fungi ) shared amore recent divergence event than plants andfungi did.

AnimaliaFungiPlantaeProtistaMonera

From Baldauf 1997 PNAS 97: 12007-12012.

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Three domains, summary

In other words, fungi and animals wereeach other’s closest relatives althoughfungi had historically been studied bybotanists.

Let’s look into the character evolution aswell:

StarchCelluloseSterolsCell wallChitinGlycogen

AnimaliaFungiPlantaeProtistaMonera

Animalia

Fungi

Plantae

Protista

Biosynthesis forStarchCellulosePlant sterolsCell wall

Biosynthesis forChitinGlycogen

Biosynthesis forCholesterolErgosterol

Look into the fungal cladeThe true fungi would include four fungalphyla.

The rest of the organisms previouslyconsidered as fungi would mainly beprotistan.

The position of Zygomycota andChytridiomycota seems uncertain.

However, character evolution maysupport a basal position ofChytridiomycota.

Chytridiomycota

Basidiomycota

Ascomycota

Zygomycota

Animalia

?

?

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Character evolution in the fungal clade

Ancestral traitsChitin GlycogenPosterior flagellum

Loss of phagotrophy

Spindle pole bodyLoss of flagellaLoss of centrioles

Dikaryotic stageSeptate mycelium

Ascospores

BasidiosporesDollipore septumClamp connections

Chytridiomycota

Basidiomycota

Ascomycota

Zygomycota

Animalia

?

?

Next time...

We will look into the groups that weretraditionally placed within fungi, but havebeen for long recognized as possibleoutliers.

We will first look into the slime molds,including true and cellular slime molds.

Then, we will proceed to the biflagellatesand see what they are all about.

AnimaliaFungiPlantaeProtistaMonera

From Pace 1997 Science 276: 734-740.

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To sum up for this time...

• Fungi are defined by their heterotrophy - wecan divide them into biotrophs andsaprotrophs.

• Biotrophy falls into several categories ofsymbiotic associations.

• Fungi are more related to animals thanplants.