bis2c: lecture 24: opisthokonts

Slides by Jonathan Eisen for BIS2C at UC Davis Spring 2016

Lecture 24: Introduction to Opisthokonts

BIS 002C Biodiversity & the Tree of Life

Spring 2016

Prof. Jonathan Eisen

1


Where we are going and where we have been…

2

•Previous lecture: •23: Botanical Conservatory

•Current Lecture: •24: Intro to Opisthokonts

•Next Lecture: •25: Sponges


Key Topics

• Opisthokonts - major groups

• Shared traits of opisthokonts

• Derived traits of major opisthokont groups

• Evolution of multicellularity

• Choanoflagellates and their relevance to animals

3

Slides by Jonathan Eisen for BIS2C at UC Davis Spring 2016 44

Eukaryote Diversity


Opisthokonts

Opisthokonts

!6Slides by Jonathan Eisen for BIS2C at UC Davis Spring 2016

Opisthokonts

Fung

i

Ani

mal

s

Cho

anof

lage

llate

s

It is ALWAYS more complicated …


Opisthokonts

Fung

i

Ani

mal

s

Cho

anof

lage

llate

s

Icht

hyos

pore

a

Ich




Opisthokonts

Fung

i

Ani

mal

s

Cho

anof

lage

llate

sFila

ster

ea

Icht

hyos

pore

a

Filasterea examples


Ministeria

Capsaspora

It’s Always More Complicated II


Fila

ster

ea

Icht

hyos

pore

a

!12

Fila

ster

ea

Icht

hyos

pore

a

Mic

rosp

orid

i

Chy

trids

Zygo

spor

e

Arb

uscu

lar

Sac

fung

i

Clu

b fu

ngi

Dik

It’s Always More Complicated III


Opisthokonts


Opisthokonts

Fung

i

Ani

mal

s

Cho

anof

lage

llate

s

Opisthokonts


Opisthokonts

Fung

i

Ani

mal

s

Cho

anof

lage

llate

s

Shared derived traits of clade?

Opisthokonts


Opisthokonts

Fung

i

Ani

mal

s

Cho

anof

lage

llate

s

Flagellum, if presence, single and posterior,

Greek: opísthios = "rear" + (kontós) = "pole"

https://en.wikipedia.org/wiki/Greek_language

Opisthokonts


Opisthokonts

Fung

i

Ani

mal

s

Cho

anof

lage

llate

s

Multiple other features

Greek: opísthios = "rear" + (kontós) = "pole"

https://en.wikipedia.org/wiki/Greek_language

Opisthokonts


Opisthokonts

Fung

i

Ani

mal

s

Cho

anof

lage

llate

s

Why care about these?

Anti fungal drugs

!18Slides by Jonathan Eisen for BIS2C at UC Davis Spring 2016 http://www.slideshare.net/drjankiborkar/antifungals-14155209


The development of antifungal agents has lagged behind that of antibacterial agents. This is a predictable consequence of the cellular structure of the organisms involved. Bacteria are prokaryotic and hence offer numerous structural and metabolic targets that differ from those of the human host. Fungi, in contrast, are eukaryotes, and consequently most agents toxic to fungi are also toxic to the host.

http://www.ncbi.nlm.nih.gov/books/NBK8263/

Figure 30.2 Yeasts


Saccharomyces cerevisiae

5 µm


Human Disease Genes w/ Yeast Homologs I

21

Defect in adenylcyclase regulation; osteodystrophyAscorbic acid biosynthesis defectBiotin-responsive carboxylase deficiency; ataxiaLactic acidosis; neurodisordersWilliams syndrome; brain developmentLactic acidosis; "maple syrup" urine diseaseHomocystinuria; psychotic symptomsMevalonicaciduria; variety of symptomsMental retardation and keratocunjunctivisTumor metastatic processInsulin resistanceHyperornithinemia; atrophy of choroid and retinaHyperammonemia in malesPeroxisomal biogenesis disorder; neuropathyHemolytic blood disorder (venous thrombosis)Glycogen storage disease; muscle crampsMyopathyCholesterol esterification defects; cornea lipid depositsAcute intermittent porphyriaHyperglycinemia; intolerance to proteinsVariegate porphyria; light sensitive dermatisImmunodeficiency; neurodisordersLactic acidosis; deathLactic acidosis; ataxiaNon spherocytic anemiaRetinitis pigmentosaPeroxisomal biogenesis disorderHypertension-associated geneHyperoxaluria; urolithiase; nephrocalcinosisHereditary spherocytosisCerebral cholesterinosisFlavoprotein subunit defect; Leigh syndromeMental retardation and ataxiaSucrose intolerance

ABC transporters; immunodeficiencyVitamin E deficiency; ataxiaChronic hemolytic anemia and neuromuscular disordersTyrosinemiaPorphyria, cutanea tardaPorphyria, congenital erythropoietic Mental/psychomotor retardationDNA helicase; TFIIH complex;subunit; photosensitivity; cancerDNA helicase; TFIIH complex subunit; photosensitivity; cancerStructure specific endonuclease; photosensitivity; cancerZinc finger damaged DNA binding protein; photosensitivity; cancer125 kDa ssDNA binding protein; photosensitivity; cancerDNA helicase; transcription-coupled repair;progressive neurological dysfunction;photosensitivityWD-repeat protein; same phenotype as above Membrane Ser/Thr protein kinaseABC transporter; neurodegenerative diseaseSuperoxide dismutasePhosphatidylinositol kinase-related proteinUnknown function; cardioskeletal myopathyRecQ DNA helicase-related protein; growth defect; predisposition to all types of cancerUnknown function; "Beige" protein; decreased pigmentation; immunodeficiencyComponent A of RAB geranylgeranyltransferaseABC transporter; impaired clearance in a variety of organs

Sulfate transporter; undersulfation of proteoglycansKidney chloride channel; nephrolithiasisDideadenosine tetraphosphate hydrolase; cancerUnknown function; neurodegenerative diseaseHyperglycerolemia; poor growth; mental retardationMismatch-repair ; hereditary nonpolyposis colon cancerMismatch repair ; hereditary nonpolyposis colon cancer


Subunit of platelet-activating factor acetylhydrolaseInositol polyphosphate 5 phosphatase-related protein; cataracts and glaucomaCopper-transporting ATPase; neurodegenerative disease and deathCalcium channel; familial hemiplegic migraine and episodic ataxiaAcetyltransferase; erythrophagocytosisRelated to transmembrane receptors with a cytoplasmic tyrosine kinase domainSer/thr protein kinase; neurodegenerative diseaseProbable tyrosine phosphatase; muscle specific diseaseHomologue of Drosophila patched; nevoid basal cell carcinoma syndromeGTPase-activating proteinFatal neurovisceral disorderDefect in development of multiple organ systemsRCC1-related protein; progressive retinal degenerationMuscle chloride channel; myotonic disordersDNA helicase Q-related protein; premature aging and strong predisposition to cancerZinc finger protein; nephroblastomaCopper transporting ATPase; toxic accumulation of copper in liver and brainEffector for CDC42H GTPase; immunodeficiency

Metabolic acidosisHemolytic blood disorder (venous thrombosis)UrolithiasisImmunodeficiencyPeroxisomal biogenesis disorder; neuropathyHemolytic anemiaHypermethioninemia; mental and motor retardation Purine nucleotide biosynthesis defect; autism featuresDelayed oxidation of acetaldehyde; acute alcohol intoxicationHepatic porphyriaSpherocytic anemiaNeonatal infantile chronic hyperammonemiaArgininemia; severe psychomotor retardationHypokalaemic alkalosis with hypercalciuraHyperammonemiaGalactosialidosisLipid metabolism defect; cardiomyopathyAcatalasiaCoproporphyria; psychiatric symptoms

HomocystinuriaLactic acidosis; "maple syrup" urine diseaseProtoporphyria, erythropoieticFumaric aciduria; encephalopathyHemolytic anemiaGlycogen storage disease; familial cirrhosisGlycogen storage disease; hepatomegalyLysosomal storage disease; cardiomyopathy; skeletal muscular hypotoniaHyperglycemia; diabetesGlutathionuriaHemolytic anemiaNon ketotic hyperglycinemia; lethargy; severe mental retardationGlycogen storage disease; skeletal muscle weakness

Human Disease Genes w/ Yeast Homologs II


Nobel Prizes for Fungal Work

Opisthokonts


Opisthokonts

Fung

i

Ani

mal

s

Cho

anof

lage

llate

s

Derived Features of Fungi

Opisthokonts


Opisthokonts

Fung

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Ani

mal

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Cho

anof

lage

llate

s

Absorptive heterotrophy

Clicker


Clicker

Which of the following best describes a heterotroph?

A. Gets carbon from organic compounds

B. Gets electrons from organic compounds

C. Gets energy from organic compounds

D. Gets carbon and electrons from organic compounds

E. All of the above


Component Different FormsEnergy source Light

Photo

Chemical

Chemo

Electron source (reducing equivalent)

Inorganic

Litho

Organic

Organo

Carbon source Carbon from C1 compounds

Auto

Carbon from organics

Hetero

Forms of nutrition (trophy)

• Three main components to “trophy”


Opisthokonts


Opisthokonts

Fung

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Ani

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Cho

anof

lage

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Absorptive heterotrophy

Photo 30.3 Hardwood log being “recycled” by saprobic brown rot fungi; central Illinois.


Opisthokonts


Opisthokonts

Fung

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Ani

mal

s

Cho

anof

lage

llate

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Absorptive heterotrophy; Chitin in cell walls

Fungal Cell Walls


Figure 30.10 A Phylogeny of the Fungi


Mic

rosp

orid

ia

Chy

trids

Zygo

spor

e fu

ngi

(Zyg

omyc

ota)

Arb

uscu

lar m

ycor

rhiz

al fu

ngi

(Glo

mer

omyc

ota)

Sac

fung

i (A

scom

ycot

a)

Clu

b fu

ngi

(Bas

idio

myc

ota)

Dikarya

Opisthokonts


Opisthokonts

Fung

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Ani

mal

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Cho

anof

lage

llate

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Animal Shared Derived Traits


Opisthokonts

Fung

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Ani

mal

s

Cho

anof

lage

llate

s• Internal digestion

• Muscle & movement

• Extracellular matrix molecules such as collagen

• Unique cell junctions

• Multicellularity

Animal Shared Derived Traits


Opisthokonts

Fung

i

Ani

mal

s

Cho

anof

lage

llate

s• Internal digestion

• Muscle & movement

• Extracellular matrix molecules such as collagen

• Unique cell junctions

• Multicellularity

• More on this starting Friday

Opisthokonts


Opisthokonts

Fung

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Ani

mal

s

Cho

anof

lage

llate

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Choanoflagellate & Animal Derived Traits

Opisthokonts


Opisthokonts

Fung

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Ani

mal

s

Cho

anof

lage

llate

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Why Care About These?

Opisthokonts


Opisthokonts

Fung

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Ani

mal

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Cho

anof

lage

llate

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Multicellularity Origins?


Multicellularity vs. Colonial Aggregates

• Multicellular: having many cells of the same genotype, in which there is some level of morphological differentiation and division of labour among cell types

• Colonial: aggregates of morphologically identical cells of the same genotype

• There is a continuum of loosely integrated colonies to fully integrated multicellular organisms.

41

Opisthokonts


Opisthokonts

Fung

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Ani

mal

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Cho

anof

lage

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Multicellularity Origins?

M

M


Opisthokont Multicellularity

Figure 28.3 Red Algae



Red Algal Multicellularity

Figure 28.4 Chlorophytes



Chlorophyte Multicellularity

Figure 28.5 Charophytes



Charophyte Multicellularity

Land Plants



Land Plant Multicellularity

Figure 27.9 Brown Algae



Brown Algal Multicellularity

Figure 27.17 A Plasmodial Slime Mold



Plasmodial Slime Mold Multicellularity

Figure 27.18 A Cellular Slime Mold



Cellular Slime Mold Multicellularity


Convergent Evolution of Multicellularity


Clicker

60


Clicker

• The multiple origins of multicellularity is a form of

• A. Homology

• B. Heteroplasy

• C. Synapomorphy

• D. Homoplasy

• E. Homospory

61


Clicker

• The multiple origins of multicellularity is a form of

• A. Homology

• B. Heteroplasy

• C. Synapomorphy

• D. Homoplasy

• E. Homospory

62


History has often repeated itself: Multicellular organisms independently originated at least 25 times from unicellular ancestors

63

Animal Multicellularity


Opisthokonts

Fung

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Ani

mal

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Cho

anof

lage

llate

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Key Point in Studying Animal Multicellularity & Biology

M

Choanoflagellates


Opisthokonts

Fung

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Ani

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Cho

anof

lage

llate

s

M

Choanoflagellates


Opisthokonts

Fung

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Ani

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Cho

anof

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M

From

Greek Khoanē = “funnel" (i.e collar)

And Latin “flagellum" (i.e., the flagella)

http://broom02.revolvy.com/main/index.php?s=Flagellum&item_type=topic&overlay=1

Figure 31.2 Choanoflagellate


Choanoflagellate protists

Stalk

Flagellum

Single cell

!68Slides by Jonathan Eisen for BIS2C at UC Davis Spring 2016 http://www.nytimes.com/2010/12/14/science/14creatures.html?_r=0

Figure 31.2 Choanocytes in Sponges Resemble Choanoflagellate Protists (Part 1)


Choanoflagellate protists

Stalk

Flagellum

Single cell

S. rosetta capture and phagocytosis


DIC timelapse movie of S. rosetta thecate cell showing capture and phagocytosis of bacteria.

http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0095577



Timelapse movie of S. rosetta thecate cell showing egestion of material, transported from the food vacuole to the inside base of the collar, exiting the cell between the collar and flagellum, and carried away by the current.


S. rosetta egestion



http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0095577Phase microscopy timelapse movie showing the arrival of an S. rosetta thecate cell and subsequent accumulation of bacteria on coverslip surface in the region surrounding the cell.

S. rosetta collecting food …


Sponges


Sponges

Bilaterians (protostomes and

deuterostomes)

Ctenophores

Cnidarians

Placozoans

Figure 31.15 Sponge Diversity


Euplectella aspergillum

Xestospongia testudinaria

Spicules

Sycon sp.

Figure 31.2 Choanocytes in Sponges


Choanocyte

Pore

Osculum

Water out via osculum

Atrium

Spicule

Water and food particles in via pores

Spicules

Flagellum

!77

Figure 31.2 Choanocytes in Sponges Resemble Choanoflagellate Protists


!78Slides by Jonathan Eisen for BIS2C at UC Davis Spring 2016 http://www.nytimes.com/2010/12/14/science/14creatures.html?_r=0



Opisthokonts

Fung

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Ani

mal

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Cho

anof

lage

llate

s

Colonial

M

FlagellumCollar

Choanoflagellate aggregation


Nicole King, Professor, UC Berkeley HHMI Professor MacArthur “Genius” Prize Winner

Many morphologies in cultures


Fig. 1. Five distinct cell morphologies observed in S. rosetta cultures. (A) Cells in rosette colonies orient in a sphere around a central focus, with their apical flagella and collars oriented radially outward. (B) Cells in chain colonies attach to one another laterally to form linear arrays of cells. (C,D) Thecate cells have long (~ 4 µm) collars surrounding apical flagella and attach to substrates via a goblet-shaped theca. (E,F) Slow swimmers have similar morphology to thecate cells, but lack thecae. (G,H) Fast swimmers have no theca and either no collar or a truncated collar (arrowheads), and are often covered in small filopodia . Key: f: flagellum, C: collar, T: theca, S: skirt, Fp: filopodia, B: bacteria. Scale bars = 5 µm. (A,B,C,E,G: DIC microscopy, D,F,H: Scanning Electron Microscopy).

http://topics.sciencedirect.com/topics/page/Differential_interference_contrast_microscopy

http://topics.sciencedirect.com/topics/page/Scanning_electron_microscope

Life history of a model Choanoflagellate Salpingoeca rosetta

!82Slides by Jonathan Eisen for BIS2C at UC Davis Spring 2016 http://www.sciencedirect.com/science/article/pii/S0012160611009924


Timelapse microscopy of a fast swimmer building a new theca. Although fast swimmers normally attach to environmental substrates, an unusual case of attachment to an empty theca is presented here because the added elevation from the substrate affords a better view of the attachment process. A fast swimmer uses long filopodia to attach to an empty theca. Those filopodia in contact with the empty theca become more refractile and coalesce to form the base of a new stalk projecting from the base of the cell. The coalesced filopodia form a highly refractile stalk which extends from the cell base. The refractile material is replaced by a stable stalk, after which the cell becomes more spherical and secretes the theca cup from its sides, leaving a ~ 1 µm gap between the theca and cell base.

doi:10.1016/j.ydbio.2011.06.003


Top view of two fast swimmers attaching to substrate. Cells attach via long filopodia, and move several microns across substrates before building thecae.


Timecourse of three cells releasing from their thecae. As cells begin to leave thecae, multiple filopodia extend from sides of cell maintaining contact with edge of theca cup (clearest in middle cell at 1:02:10–1:30:00, and left cell at 1:01:30). Change in angle of filopodia as it releases from theca in left cell (from 01:01:20 to 01:01:30) shows that these are filopodia and not retraction fibers. As cells release, collar retracts (clearest in right cell at 0:12:30). Times shown in Hours:Minutes:Seconds

!88Slides by Jonathan Eisen for BIS2C at UC Davis Spring 2016 Thecate cell division showing that one daughter cell leaves while the other remains in the theca.

http://topics.sciencedirect.com/topics/page/Cell_division


Tilt series through an intercellular bridge shows that the cell membrane is continuous across the bridge.

http://topics.sciencedirect.com/topics/page/Cell_membrane

!91Slides by Jonathan Eisen for BIS2C at UC Davis Spring 2016 Rosette colony ejects minute cells that adhere to the coverslip.

!92Slides by Jonathan Eisen for BIS2C at UC Davis Spring 2016 S. rosetta rosette colonies reproduce by fission



A model of S. rosetta life history. S. rosetta cells can differentiate between at least five different forms. Arrows depict observed and inferred transitions that are described in the main text and in Fig. S9. Fast swimmers can settle to produce thecate cells that then produce swimming cells either through cell division or theca abandonment. Under rapid growth conditions, slow swimmer cells proliferate but remain attached via intercellular bridges and ECM to produce chain colonies, or, in the presence of A. machipongonensis bacteria (denoted by ‘⁎’), rosette colonies that have intercellular bridges, ECM and filopodia. caption

http://www.sciencedirect.com/science/article/pii/S0012160611009924

http://topics.sciencedirect.com/topics/page/Cell_division

http://topics.sciencedirect.com/topics/page/Extracellular_matrix

Choanoflagellate Genome


Nicole King Dan Rokhsar

Choanoflagellate Genome




Opisthokonts

Fung

i

Ani

mal

s

Cho

anof

lage

llate

s

• Colonial • Single flagellum • Collar • Cell adhesion

M

Nicole King



http://www.ibiology.org/ibioseminars/nicole-king-part-1.html

http://www.ibiology.org/ibioseminars/nicole-king-part-2.html


Single cell -> aggregation -> multicellular

100



Opisthokonts

Fung

i

Ani

mal

s

Cho

anof

lage

llate

sFila

ster

ea

Icht

hyos

pore

a

Filasterea also colonial

!102Slides by Jonathan Eisen for BIS2C at UC Davis Spring 2016 http://dx.doi.org/10.7554/eLife.01287

Filasterea aggregation

!103Slides by Jonathan Eisen for BIS2C at UC Davis Spring 2016 http://dx.doi.org/10.7554/eLife.01287


Filasterea aggregation

http://dx.doi.org/10.7554/eLife.01287

Animal (Metazoan) Diversity


Fungal Diversity


Mic

rosp

orid

ia

Chy

trids

Zygo

spor

e fu

ngi

(Zyg

omyc

ota)

Arb

uscu

lar m

ycor

rhiz

al fu

ngi

(Glo

mer

omyc

ota)

Sac

fung

i (A

scom

ycot

a)

Clu

b fu

ngi

(Bas

idio

myc

ota)

Dikarya

bis2c: lecture 24: opisthokonts

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