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
Fungi
Animals
Choanoflagellates

It is ALWAYS more complicated …
Opisthokonts
Fungi
Animals
Choanoflagellates
Ichthyosporea

Ich

Opisthokonts
Fungi
Animals
Choanoflagellates
Filasterea
Ichthyosporea

Filasterea examples
Ministeria
Capsaspora

It’s Always More Complicated II
Filasterea
Ichthyosporea

!12
Filasterea
Ichthyosporea
Microsporidi
Chytrids
Zygospore
Arbuscular
Sacfungi
Clubfungi
Dik
It’s Always More Complicated III

Opisthokonts
Opisthokonts
Fungi
Animals
Choanoflagellates

Opisthokonts
Opisthokonts
Fungi
Animals
Choanoflagellates
Shared derived traits of clade?

Opisthokonts
Opisthokonts
Fungi
Animals
Choanoflagellates
Flagellum, if presence, single
and posterior,
Greek:
opísthios =
"rear" +
(kontós) =
"pole"

Opisthokonts
Opisthokonts
Fungi
Animals
Choanoflagellates
Multiple other features
Greek:
opísthios =
"rear" +
(kontós) =
"pole"

Opisthokonts
Opisthokonts
Fungi
Animals
Choanoflagellates
Why care about these?

Anti fungal drugs
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; osteodystrophy
Ascorbic acid biosynthesis defect
Biotin-responsive carboxylase deficiency; ataxia
Lactic acidosis; neurodisorders
Williams syndrome; brain development
Lactic acidosis; "maple syrup" urine disease
Homocystinuria; psychotic symptoms
Mevalonicaciduria; variety of symptoms
Mental retardation and keratocunjunctivis
Tumor metastatic process
Insulin resistance
Hyperornithinemia; atrophy of choroid and retina
Hyperammonemia in males
Peroxisomal biogenesis disorder; neuropathy
Hemolytic blood disorder (venous thrombosis)
Glycogen storage disease; muscle cramps
Myopathy
Cholesterol esterification defects; cornea lipid deposits
Acute intermittent porphyria
Hyperglycinemia; intolerance to proteins
Variegate porphyria; light sensitive dermatis
Immunodeficiency; neurodisorders
Lactic acidosis; death
Lactic acidosis; ataxia
Non spherocytic anemia
Retinitis pigmentosa
Peroxisomal biogenesis disorder
Hypertension-associated gene
Hyperoxaluria; urolithiase; nephrocalcinosis
Hereditary spherocytosis
Cerebral cholesterinosis
Flavoprotein subunit defect; Leigh syndrome
Mental retardation and ataxia
Sucrose intolerance
ABC transporters; immunodeficiency
Vitamin E deficiency; ataxia
Chronic hemolytic anemia and neuromuscular disorders
Tyrosinemia
Porphyria, cutanea tarda
Porphyria, congenital erythropoietic
Mental/psychomotor retardation
DNA helicase; TFIIH complex;subunit; photosensitivity; cancer
DNA helicase; TFIIH complex subunit; photosensitivity; cancer
Structure specific endonuclease; photosensitivity; cancer
Zinc finger damaged DNA binding protein; photosensitivity; cancer
125 kDa ssDNA binding protein; photosensitivity; cancer
DNA helicase; transcription-coupled repair;progressive neurological dysfunction;photose
WD-repeat protein; same phenotype as above
Membrane Ser/Thr protein kinase
ABC transporter; neurodegenerative disease
Superoxide dismutase
Phosphatidylinositol kinase-related protein
Unknown function; cardioskeletal myopathy
RecQ DNA helicase-related protein; growth defect; predisposition to all types of cancer
Unknown function; "Beige" protein; decreased pigmentation; immunodeficiency
Component A of RAB geranylgeranyltransferase
ABC transporter; impaired clearance in a variety of organs
Sulfate transporter; undersulfation of proteoglycans
Kidney chloride channel; nephrolithiasis
Dideadenosine tetraphosphate hydrolase; cancer
Unknown function; neurodegenerative disease
Hyperglycerolemia; poor growth; mental retardation
Mismatch-repair ; hereditary nonpolyposis colon cancer
Mismatch repair ; hereditary nonpolyposis colon cancer

Subunit of platelet-activating factor
acetylhydrolase
Inositol polyphosphate 5 phosphatase-related
protein; cataracts and glaucoma
Copper-transporting ATPase; neurodegenerative
disease and death
Calcium channel; familial hemiplegic migraine
and episodic ataxia
Acetyltransferase; erythrophagocytosis
Related to transmembrane receptors with a
cytoplasmic tyrosine kinase domain
Ser/thr protein kinase; neurodegenerative disease
Probable tyrosine phosphatase; muscle specific
disease
Homologue of Drosophila patched; nevoid basal
cell carcinoma syndrome
GTPase-activating protein
Fatal neurovisceral disorder
Defect in development of multiple organ systems
RCC1-related protein; progressive retinal
degeneration
Muscle chloride channel; myotonic disorders
DNA helicase Q-related protein; premature aging
and strong predisposition to cancer
Zinc finger protein; nephroblastoma
Copper transporting ATPase; toxic accumulation
of copper in liver and brain
Effector for CDC42H GTPase; immunodeficiency
Metabolic acidosis
Hemolytic blood disorder (venous thrombosis)
Urolithiasis
Immunodeficiency
Peroxisomal biogenesis disorder; neuropathy
Hemolytic anemia
Hypermethioninemia; mental and motor retardation
Purine nucleotide biosynthesis defect; autism features
Delayed oxidation of acetaldehyde; acute alcohol intoxication
Hepatic porphyria
Spherocytic anemia
Neonatal infantile chronic hyperammonemia
Argininemia; severe psychomotor retardation
Hypokalaemic alkalosis with hypercalciura
Hyperammonemia
Galactosialidosis
Lipid metabolism defect; cardiomyopathy
Acatalasia
Coproporphyria; psychiatric symptoms
Homocystinuria
Lactic acidosis; "maple syrup" urine disease
Protoporphyria, erythropoietic
Fumaric aciduria; encephalopathy
Hemolytic anemia
Glycogen storage disease; familial cirrhosis
Glycogen storage disease; hepatomegaly
Lysosomal storage disease; cardiomyopathy; skeletal muscular hypotonia
Hyperglycemia; diabetes
Glutathionuria
Hemolytic anemia
Non ketotic hyperglycinemia; lethargy; severe mental retardation
Glycogen storage disease; skeletal muscle weakness
Human Disease Genes w/ Yeast Homologs II

Nobel Prizes for Fungal Work

Opisthokonts
Opisthokonts
Fungi
Animals
Choanoflagellates
Derived Features of Fungi

Opisthokonts
Opisthokonts
Fungi
Animals
Choanoflagellates
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 Forms
Energy 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
Fungi
Animals
Choanoflagellates
Absorptive heterotrophy

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

Opisthokonts
Opisthokonts
Fungi
Animals
Choanoflagellates
Absorptive heterotrophy;
Chitin in cell walls

Fungal Cell Walls

Figure 30.10 A Phylogeny of the Fungi
Microsporidia
Chytrids
Zygosporefungi
(Zygomycota)
Arbuscularmycorrhizalfungi
(Glomeromycota)
Sacfungi
(Ascomycota)
Clubfungi
(Basidiomycota)
Dikarya

Opisthokonts
Opisthokonts
Fungi
Animals
Choanoflagellates

Animal Shared Derived Traits
Opisthokonts
Fungi
Animals
Choanoflagellates
• Internal digestion
• Muscle & movement
• Extracellular matrix
molecules such as
collagen
• Unique cell junctions
• Multicellularity

Animal Shared Derived Traits
Opisthokonts
Fungi
Animals
Choanoflagellates
• Internal digestion
• Muscle & movement
• Extracellular matrix
molecules such as
collagen
• Unique cell junctions
• Multicellularity
• More on this starting
Friday

Opisthokonts
Opisthokonts
Fungi
Animals
Choanoflagellates
Choanoflagellate
& Animal Derived Traits

Opisthokonts
Opisthokonts
Fungi
Animals
Choanoflagellates
Why Care About These?

Opisthokonts
Opisthokonts
Fungi
Animals
Choanoflagellates
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
Fungi
Animals
Choanoflagellates
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
Fungi
Animals
Choanoflagellates
Key Point in Studying Animal
Multicellularity & Biology
M

Choanoflagellates
Opisthokonts
Fungi
Animals
Choanoflagellates
M

Choanoflagellates
Opisthokonts
Fungi
Animals
Choanoflagellates
M
From
Greek Khoanē
= “funnel" (i.e
collar)
And Latin
“ﬂagellum" (i.e.
, the ﬂagella)

Figure 31.2 Choanoflagellate
Choanoflagellate protists
Stalk
Flagellum
Single cell

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

Phase 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

http://www.nytimes.com/2010/12/14/science/14creatures.html?_r=0

Opisthokonts
Fungi
Animals
Choanoflagellates
Colonial
M
Flagellum
Collar

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).

Life history of a model Choanoflagellate Salpingoeca rosetta
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

Thecate cell division showing that one daughter cell leaves while the other remains in the theca.

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

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

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

Choanoflagellate Genome
Nicole King Dan Rokhsar

Choanoflagellate Genome

Opisthokonts
Fungi
Animals
Choanoflagellates
• 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
Fungi
Animals
Choanoflagellates
Filasterea
Ichthyosporea

Filasterea also colonial
http://dx.doi.org/10.7554/eLife.01287

Filasterea aggregation

Animal (Metazoan) Diversity

Fungal Diversity
Microsporidia
Chytrids
Zygosporefungi
(Zygomycota)
Arbuscularmycorrhizalfungi
(Glomeromycota)
Sacfungi
(Ascomycota)
Clubfungi
(Basidiomycota)
Dikarya

BIS2C: Lecture 24: Opisthokonts

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