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1 Biology of FUNgi Lecture 15 Happy together Fungus-animal symbioses Last time... Endophytes defined. Advantages of foliar endophytes. Advantages of root endophytes. How may endophytes control the composition of plant communities?

Biology of FUNgi - Kansas State Universitycourses.k-state.edu/fall2003/BIOL/BIOL604/Lectures/PDFs/...mushroom - being grown on concrete blocks with a thin layer of straw and manure

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Page 1: Biology of FUNgi - Kansas State Universitycourses.k-state.edu/fall2003/BIOL/BIOL604/Lectures/PDFs/...mushroom - being grown on concrete blocks with a thin layer of straw and manure

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Biology of FUNgi

Lecture 15Happy together

Fungus-animal symbioses

Last time...

• Endophytes defined.

• Advantages of foliar endophytes. Advantages ofroot endophytes.

• How may endophytes control the composition ofplant communities?

Page 2: Biology of FUNgi - Kansas State Universitycourses.k-state.edu/fall2003/BIOL/BIOL604/Lectures/PDFs/...mushroom - being grown on concrete blocks with a thin layer of straw and manure

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A great example of a mutualistic symbiosis betweenanimals and a fungus.

Tricholoma myomyces and leaf cutter ant generaAcromyces and Atta in the tribe Attini.

How does this mutualistic symbiosis work?

Tricholoma myomyces isassociated with leaf cutter ants(Acromyrmex and Atta) in tribeAttini

Fungus of the day -Tricholoma myomyces

Taxonomy: Phylum (subphylum) Basidiomycota Order - Agaricales Family - Tricholomataceae

Acromyrmex is an example offungus gardening attines

How does this mutualistic symbiosis work?

Leaf cutter ants (here, Atta)appropriately for their name,harvest leaves...

Fungus of the day -Tricholoma myomyces

...and drag them to their nests

Nests are usually belowground toprovide stable conditions for theresidents and their gardens.

Page 3: Biology of FUNgi - Kansas State Universitycourses.k-state.edu/fall2003/BIOL/BIOL604/Lectures/PDFs/...mushroom - being grown on concrete blocks with a thin layer of straw and manure

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How does this mutualistic symbiosis work?

Simple on the surface...

Fungus of the day -Tricholoma myomyces

…the nests are often monumentalin size indicating the success ofthe mutualistic association.

The nests may be impressive in sizebut they also have a beautifulinfrastructure including the queenchambers and the fungus gardens.

How does this mutualistic symbiosis work?

Some chambers are dedicatedto serve a special area wherethe Tricholoma myomyces isgrown.

Fungus of the day -Tricholoma myomyces

The special chambersare known as the fungusgardens, which...

…are meticulously tended by the leafcutter ants.

Page 4: Biology of FUNgi - Kansas State Universitycourses.k-state.edu/fall2003/BIOL/BIOL604/Lectures/PDFs/...mushroom - being grown on concrete blocks with a thin layer of straw and manure

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How does this mutualistic symbiosis work?

Ants bring the harvested leaves into the fungusgarden, which has fairly constant environmentalconditions (temperature and humidity) for thegrowth of a saprobic T. myomyces.

The ants then feed on the growing mycelium.

There is more to this story, the ants do not onlygrow the fungus but they groom and keep theirfungus farm clean.

Fungus of the day -Tricholoma myomyces

Special chambers arededicated as the fungusgardens.

How does this mutualistic symbiosis work?

The whole fungus-ant symbiosis is a complex webof interactions.

In addition to providing the fungus a niceenvironment, the ants lick the surfaces of the nestand the new leaf material they bring in forsubstrate; they decontaminate the new substrate.

When contaminations occur, great number ofworkers dedicate their time and attention to pickingcontaminant spores out of the culture.

If the contaminant spores germinate, the ants weedout the contaminated substrate.

Tricholoma myomyces isassociated with leaf cutter ants intribe Attini

Fungus of the day -Tricholoma myomyces

Page 5: Biology of FUNgi - Kansas State Universitycourses.k-state.edu/fall2003/BIOL/BIOL604/Lectures/PDFs/...mushroom - being grown on concrete blocks with a thin layer of straw and manure

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How does this mutualistic symbiosis work?

There is more to this story; it has been suggestedthat the ants have harnessed antibiotic bacteria tofight the contaminants.

The fungal gardens are the main habitat for aspecialized parasitic ascomycete, Escovopsis.

The attine ants carry about an actinomycete(Streptomyces) producing streptomycin-likeantibiotic in their cuticles.

The actinomycete is transmitted vertically (fromparent to offspring) and promotes the growth of thegarden fungus while suppressing the growth ofEscovopsis.

Tricholoma myomyces isassociated with leaf cutter ants intribe Attini

Fungus of the day -Tricholoma myomyces

This symbiosis seems tohave an ancient evolutionaryorigin. The ant and fungaltopologies follow each otherwith few transversionswhich may be due toacquisition of a superiorgarden strain

Page 6: Biology of FUNgi - Kansas State Universitycourses.k-state.edu/fall2003/BIOL/BIOL604/Lectures/PDFs/...mushroom - being grown on concrete blocks with a thin layer of straw and manure

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Thricholoma myomyces is not the only mutualismof this kind.

Termitomyces sp. is symbiotic with termites. Tricholoma myomyces

Termitomyces sp. is associatedwith termites.

Fungus of the day -Tricholoma myomyces

Termitomyces sp. emerging fromtermite gardens.

This time…

• Fungus animal symbioses.

• Human fungus symbioses?

• Remember that symbiosis is not alwaysmutualistic.

Page 7: Biology of FUNgi - Kansas State Universitycourses.k-state.edu/fall2003/BIOL/BIOL604/Lectures/PDFs/...mushroom - being grown on concrete blocks with a thin layer of straw and manure

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The button mushrooms comprised 90% of theNorth American mushroom sales.

Agaricus bisporus would not be this widely spreadand doing this well unless humans had their fungusgardens.

Agaricus bisporus or A.brunnescens - the common buttonmushroom - being grown onconcrete blocks with a thin layerof straw and manure

Human symbiosis with Agaricus

Similarly to Agaricus bisporus, oyster mushroomand shiitake have gained global distribution andsecured substrate and habitat as a result of humanfungal gardening.

Lentinus was traditionally produced on oak and elmlogs. Nowadays, this practice is being replaced bysterile bags like those we are using in ourmushroom experiment.

Lentinus edodes or shiitake andwas traditionally produced onhardwood logs.

Human symbioses withother mushrooms

Page 8: Biology of FUNgi - Kansas State Universitycourses.k-state.edu/fall2003/BIOL/BIOL604/Lectures/PDFs/...mushroom - being grown on concrete blocks with a thin layer of straw and manure

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Log cultures have been given up and mostlignicolous fungi are now commercially producedin sterile bags filled with saw dust or straw.

Lentinus edodes or shiitake grownin spawn bags.

This is how well the oyster mushroom Pleurotusostreatus can produce when treated right and providedwith more appropriate substrates.

Human symbioses withother mushrooms

Other mammals can be more dependenton the fungi in their lives

Long-nosed potoroo (Potorous sp.)

Brown Bandicoot (Isoodon obesulus) Swamp wallaby (Wallabia sp.)

Page 9: Biology of FUNgi - Kansas State Universitycourses.k-state.edu/fall2003/BIOL/BIOL604/Lectures/PDFs/...mushroom - being grown on concrete blocks with a thin layer of straw and manure

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California red back vole (Clethrionomyscalifornicus) is exclusively dependent onfungi (truffles in particular) in its diet.

The vole’s dental structure does notallow it to eat anything but soft tissues,i.e. fungal tissues.

Other mammals were more dependent onthe fungi in their lives

Northern flying squirrel (Glaucomyssabrinius) is similarly dependent ontruffles for dietary supplement, but not tothe degree that California red back voledepends on them.

Animals feed on fungi.What do fungi get in return?

Most truffles emit odors that animals find attractive,this is necessary for the animals to find their food.Once ingested, the spores pass the digestive trackunharmed and are deposited in poop-capsulatedpropagules.

More rarely, the truffles mimic the food supply:Paurocystis pila and Weraroa erythrocephala mimicPodocarpus cones eaten by the kiwi-bird

Chamonixia vittatisporasmells like dog poop

Paurocystis pila andWeraroaerythrocephala looklike Podocarpus cones

Page 10: Biology of FUNgi - Kansas State Universitycourses.k-state.edu/fall2003/BIOL/BIOL604/Lectures/PDFs/...mushroom - being grown on concrete blocks with a thin layer of straw and manure

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Animals that consume the truffles unknowinglystratify the fungal spores in their gut anddisperse them with their feces.

Predators can increase the dispersal capacity ofthe fungi.

Some fungi do not pass the digestive track butare aerially dispersed once the outer layers of thesporocarps are eaten.

Elaphomyces sp.disperses aeriallyonce the sterileouter core is eaten

Mesophelliaceae are even moreclever than Elaphomyces spp.:animals need to get to the innersterile tissue through the sporemassPredators can

disperse spores evenlonger distances

Animals feed on fungi.What do fungi get in return?

Many of the fungi eaten by the animals are alsoassociated with the forest trees.

We can talk about an interconnected food web onan ecosystem scale.

There is more to the storythan that, though

NutrientsWaterProtectionfrom pathogens

CarbonEnergy Carbon

EnergyNutrientsProtection

Dispersal

Dispersal

CarbonEnergyNutrients

Page 11: Biology of FUNgi - Kansas State Universitycourses.k-state.edu/fall2003/BIOL/BIOL604/Lectures/PDFs/...mushroom - being grown on concrete blocks with a thin layer of straw and manure

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Recall, Laboulbeniales, the species-specific ascomycetes on the insectexosceleton with minuscule asci.

A social disease of most of the insects.

Laboulbenia is a socialdisease of insects colonizingthe chitinous exosceleton.

Other fungus animalsymbioses

Some insect symbionts (forming parasiticsymbioses) have been considered for biocontrol.

Entomophthorales (Zyg.) are omnipresentparasites of various insects.

Beauveria bassiana (Asc.), for example is acommon soilborne parasite of insects and severalstrains can level of peak insect populations.

Similarly, Metarhizium anisopliae (Asc.) has beenused against turf grass grubs.

Entomophthora is aspecialized parasite of insects,including flies.

Other fungus animalsymbioses

Wasps infected with the fungusBeauveria bassiana. Grass grubsinfected with the fungusMetarhizium anisopliae.

Page 12: Biology of FUNgi - Kansas State Universitycourses.k-state.edu/fall2003/BIOL/BIOL604/Lectures/PDFs/...mushroom - being grown on concrete blocks with a thin layer of straw and manure

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The specific parasitism a select insect resultedin great interest in Entomophthorales (Zyg.) asa potential biocontrol agent.

Entomophaga maimaiga and control of gypsymoths serves as an example.

Entomophaga maimaiga is aspecialized parasite of gypsymoth which may causeextensive tree defoliation whenpopulation densities are high.E. maimaiga allows

convenient dispersal. It hasboth resting diploid spores andhaploid conidia.

Other fungus animalsymbioses

Summary

• Leaf cutter ant - Tricholoma symbiosis.

• Human fungus symbioses

• Small mammal - fungus food web

• Entomopathogenic fungi