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Title: THE LAST 35 YEARS


1
THE LAST 35 YEARS OF PROTISTAN EVOLUTION
David J. Patterson University of Sydney
Adjunct Scientist, Astrobiology Institute,
Marine Biological Laboratory, Woods Hole
paddy_at_mbl.edu
2
This talk was published last year American
Naturalist, 154 S96-S124
3
EVOLUTIONARY PROTISTOLOGY IN THE LAST 35 YEARS
APPROACHES IMPACTS
Comprehensive tree
2000
Protein gene sequences
1995
Skeletal trees
1990
Reconstruction begins
16S rRNA sequence data
1985
Scenarios
Rejection of traditional taxonomy
1980
Endosymbiotic origins of organelles
1975
Integrated protistology
More diversity recognized
1970
Electron microscopy
Traditional taxonomy
1965
4
Traditionally ..
  • PROKARYOTES
  • EUKARYOTES
  • THE MACROBIAL TYPES
  • ANIMALS
  • PLANTS
  • FUNGI
  • AND THE MICROBIAL EUKARYOTES
  • ALGAE REDS, BROWNS, GREENS, DIATOMS, EUGLENIDS,
    DINOFLAGELLATES, HETEROKONTS, CRYPTOS
  • PROTOZOA CILIATES, AMOEBAE, FLAGELLATES,
    SPOROZOA
  • SLIME MOULDS MYCETOZOA, ACRASIDS,
    DICTYOSTELIDS LABYRINTHULIDS

5
Traditionally .. 4 types of protozoa
amoebae flagellates ciliates
sporozoa
6
Otto Bütschli his view, 1880
Protozoa Class Sarkodina Class
Mastigophora Class Sporozoa Class Infusoria
Sporozoa
Infusoria
Mastigophora
Sarkodina
Protsville
7
MICROSCOPES Royal Mail Mint Stamps
8
EVOLUTIONARY PROTISTOLOGY IN THE LAST 35 YEARS
APPROACHES IMPACTS
Comprehensive tree
2000
Protein gene sequences
1995
Skeletal trees
1990
Reconstruction begins
16S rRNA sequence data
1985
Scenarios
Rejection of traditional taxonomy
1980
Endosymbiotic origins of organelles
1975
Integrated protistology
More diversity recognized
1970
Electron microscopy
Traditional taxonomy
1965
9
The 1960s and the advent of good fixation
protocols for electron-microscopy
GLUTARALDEHYDE
10
Goniomonas
Electron microscopy provides more data
than light microscopy
11
Heliozoa
Centrohelids
Actinophryids
12
Ultrastructural features define robust groups of
protists
  • Flagellum - structure and associations
  • Flagellar rootlets
  • Mitotic spindle characters
  • Dividing nucleus
  • Mitochondrial cristae
  • Plastid structure bounding membranes
  • External spines, scales, etc.
  • Cytoskeletal materials
  • Extrusomes, contractile vacuoles, ingestion
    organelles
  • etc.

ultrastructural identity
13
How many groups have distinct ultrastructural
identities?
Algae 10 Amoebae 20 Slime Molds
6 Flagellates 39 Sporozoa 4 Ciliates
1 Animals 1 Plants 1 Fungi
1 TOTAL 82 RESIDUA - 320
genera
On this scale Animals 1, Plants 1 , Fungi
1 that is - the units are kingdoms. By the
1980s, there were about 80 kingdoms of protists
14
By the 1980s, the PROTISTS were ...
  • Acantharea Actinophryids Adriamonas
    Ancyromonas Apicomplexa Apusomonads
    Caecitellus Carpediemonas Centrohelida
    Cercomonads Chlorarachnion Choanoflagellates
    Chytrids Ciliophora Coelosporidium
    Colponema Copromyxids Cryothecomonas
    Cryptomonads Cyanophorids Desmothoracids
    Dimorphids Dinoflagellates Diphylleia
    Diplomonads Diplonema Discocelis Ebriids
    Ellobiopsiids Entamoebidae Euglenida
    Fonticula Glaucosphaera Gloeochaete
    Granuloreticulosa Gymnosphaerida Haplosporids
    Haptophytes Hedraiophrys Heterolobosea
    Histiona Hypermastigids Jakoba
    Kathablepharidae Kinetoplastida Komokiacea
    Leucodictyon Luffisphaera Microsporidia
    Ministeria Myxomycetes Nephridiophaga
    Nucleariidae Oxymonads Paramyxea Pelobionts
    Phaeodarea Phalansterium pkx
    Plasmodiophorids Polycystinea Protostelids
    Pseudodendromonads Pseudospora Ramicristates
    Reclinomonas Red algae Retortamonads
    Spironemidae Spongomonads Stephanopogon
    Sticholonche Stramenopiles Telonema
    Thaumatomonads Trichomonads Trimastix
    Vampyrellids Viridaeplantae Xenophyophores
  • PLUS 300 UNDERSTUDIED GENERA PLUS CRYPTIC TAXA

15
EVOLUTIONARY PROTISTOLOGY IN THE LAST 35 YEARS
APPROACHES IMPACTS
Comprehensive tree
2000
Protein gene sequences
1995
Skeletal trees
1990
Reconstruction begins
16S rRNA sequence data
1985
Scenarios
Rejection of traditional taxonomy
1980
Endosymbiotic origins of organelles
1975
Integrated protistology
More diversity recognized
1970
Electron microscopy
Traditional taxonomy
1965
16
Endosymbiosis and the evolution of
eukaryotes from Merschkovsky 1910 .
17
The Serial Endosymbiosis Theory is an easy idea
to test .
18
EVOLUTIONARY PROTISTOLOGY IN THE LAST 35 YEARS
APPROACHES IMPACTS
Comprehensive tree
2000
Protein gene sequences
1995
Skeletal trees
1990
Reconstruction begins
16S rRNA sequence data
1985
Scenarios
Rejection of traditional taxonomy
1980
Endosymbiotic origins of organelles
1975
Integrated protistology
More diversity recognized
1970
Electron microscopy
Traditional taxonomy
1965
19
A phylogenetic problems - what is the
relationship of 1, 2 and 3. We have to find out
which pair of 1, 2 and 3 are more closely related
to each other than they are to the third
1 2 3
We depict ignorance as an unresolved polytomies
and understanding as dichotomies
20
An example of creating bits of the tree
enigmatic opalines large (1 mm.) flat
flagellates living in amphibia
21
Opalina
Karotomorpha
Proteromonas
22
Hairs link proteromonads to the chrysophytes
23
Identifying a lineage leading from algae
to protozoa grouping 3 ultrastructural
identities
24
STRAMENOPILES
WITH STRAW HAIRS
Protsville
25
The PROTISTS are getting fewer ...
  • Acantharea Adriamonas Ancyromonas
    Alveolates Apusomonads Centrohelida
    Cercomonads Chlorarachnion Coelosporidium
    Colponema Copromyxids Cryothecomonas
    Cryptomonads Desmothoracids Dimorphids
    Diphylleia Discocelis Ebriids
    Ellobiopsiids Euglenozoa Excavates
    Fonticula Glaucophytes Granuloreticulosa
    Gymnosphaerida Haplosporids Haptophytes
    Hedraiophrys Kathablepharids Komokiacea
    Leucodictyon Luffisphaera Ministeria
    Nephridiophaga Nucleariidae Opisthokonts
    Oxymonads Parabasalids Paramyxea
    Pelobionts Phaeodarea Phalansterium
    Plasmodiophorids Polycystinea Pseudospora
    Ramicristates Red algae Spironemidae
    Spongomonads Stephanopogon Sticholonche
    Stramenopiles Telonema Thaumatomonads
    Vampyrellids Viridaeplantae Xenophyophores
  • PLUS 300 UNDERSTUDIED GENERA PLUS CRYPTIC TAXA

26
EVOLUTIONARY PROTISTOLOGY IN THE LAST 35 YEARS
APPROACHES IMPACTS
Comprehensive tree
2000
Protein gene sequences
1995
Skeletal trees
1990
Reconstruction begins
16S rRNA sequence data
1985
Scenarios
Rejection of traditional taxonomy
1980
Endosymbiotic origins of organelles
1975
Integrated protistology
More diversity recognized
1970
Electron microscopy
Traditional taxonomy
1965
27
Small subunit (16S) rRNA 1250 - 2500 bases
Large subunit 28S, 5.8S and 5S rRNA
28
AACUGGUUGAUCUUGCCAGUAGUCAUAUGCUUGUCUCAAAG AUUAGCCA
UGCAAGUGAAAUAUAUGCAUAUUUUAUAUGUAGAAACUGCGAACGGCUCA
UUAAAACAGUUAUAAUCUAXUUGACAUUUUAUUAUUAUAAGGAUAACUAC
GGAAAACGUGUAGCUAAUAACUUGCUUUAAGUGUUUUUACUUCUUGGAGU
AAUUAGCAUGUAUUGUUAAGCUUAUAAGAAAAAUUUUUAAUUAAAGCAAA
UUAUAACAAAGAAGUAACACAUAAUAUAUUUACUAUAUUUAGUGUGUACA
AUCGAGUUUCUGACCAUUCAGCUUUUCAUGUUAGGGUAUUGGCCUAACAU
GGCAUGACGGGUAACGGGGAAUUAGAGUUCGAUUCCGGAAGAGGGAGCCC
UGAGAAUAGCUACCACAUCUAAGGAAGGCAGCAGGCGGGUAAAUUACCCA
AUUCUAAAUAAGAGGGUAGUGACAAGAAUAACAAUAUAAGGCCAAAUUUU
GGUUUUAUAUAAUUGGAAUGAUGGGAAUUUAAAACCUUCCCAAAAUCAAU
UGGAGGGCAAGUCUGGUGCCAGCAGCAGCCGCGGUAAUUCCAGCUCCAAU
AGCUAUAUUAAAAUUGUUGCAGUUAAAGCGUCGUAGUUGAACUUCAAGGG
UAUUAUUAUUUUAAGUAACUCACUUGCAGAAUCUUGGCUCCGCCUCGAUA
UCUUCAUGCCUUGUUGUAGGUUCUUUUAAUUACACCCUUUGAGACCCCAA
UGAUUUAUCACUGGGUUUU...16SRIBOSOMALRNASEQUENCEFROMS
ARCOCYSTISMURIS ...
Protsville
29
Giving universal trees of life
30
A typical cell has endoplasmic
reticulum nuclei mitochondria dictyosomes micr
otubular cytoskeleton microfilamentous
cytoskeleton mitosis meiosis
secretory vesicles lysosomes
Wolfe
Protsville
31
Microsporidia
32
Leading to 1990s models of the evolution of the
eukaryotic cell
Early evolution was of amitochondriate eukaryotes
At a time when there was little free
oxygen? Might more ancient amitochondriate
protists still exist? And where would we find
them?
33
Thiobios The anoxic zone under the surface of
mud
34
Free-living amitochondriate flagellates
retortamonads
Trimastix
trichomonads
Carpediemonas
pelobionts
diplomonads
35
such as Mastigamoeba schizophrenia
pelobionts
Pelobionts Pelomyxa Mastigina
Mastigamoeba Mastigella Phreatamoeba
36
Mastigamoeba schizophrenia Pelobionts have
flagella one microtubular root
endoplasmic reticulum nuclei no Golgi
apparatus no mitochondria no plastids no
fibrous cytoskeleton
37
Flagellar idiosyncrasies in pelobionts might
indicate that they represent the first of the
flagellated eukaryotes

38
But, when the first pelobionts were sequenced
...
39
EVOLUTIONARY PROTISTOLOGY IN THE LAST 35 YEARS
APPROACHES IMPACTS
Comprehensive tree
2000
Protein gene sequences
1995
Skeletal trees
1990
Reconstruction begins
16S rRNA sequence data
1985
Scenarios
Rejection of traditional taxonomy
1980
Endosymbiotic origins of organelles
1975
Integrated protistology
More diversity recognized
1970
Electron microscopy
Traditional taxonomy
1965
40
Molecular trees do not agree with each other
in the tubulin trees microsporidia go with
fungi amitochondriate organisms are dispersed
trichomonads
Suggesting that our earlier confidence in the 16S
trees was not justified
41
EVOLUTIONARY PROTISTOLOGY IN THE LAST 35 YEARS
APPROACHES IMPACTS
Comprehensive tree
2000
Protein gene sequences
1995
Skeletal trees
1990
Reconstruction begins
16S rRNA sequence data
1985
Scenarios
Rejection of traditional taxonomy
1980
Endosymbiotic origins of organelles
1975
Integrated protistology
More diversity recognized
1970
Electron microscopy
Traditional taxonomy
1965
42
EVOLUTIONARY PROTISTOLOGY IN THE LAST 35 YEARS
APPROACHES IMPACTS
Comprehensive tree
Protein gene sequences
1995
Skeletal trees
1990
Reconstruction begins
16S rRNA sequence data
1985
Scenarios
Rejection of traditional taxonomy
1980
Endosymbiotic origins of organelles
1975
Integrated protistology
More diversity recognized
1970
Electron microscopy
Traditional taxonomy
1965
43
(No Transcript)
44
A more extensive analysis of 16S ribosomal RNA
genes confirms that pelobionts are not primitive
but related to slime moulds and entamoebae
Saccharomyces
opisthokonts - animals and fungi
Pneumocystis
Diaphanoeca
Euglypha
Apusomonas
Acanthamoeba
Chlamydomonas
green algae and land plants
Zea
Porphyra umbilicalis
red algae
Porphyra minia
Labyrinthuloides
stramenopiles
Thalassonema
Paramecium
Oxytricha
alveolates - ciliates dinoflagellates and
apicomplexa
Prorocentrum
Toxoplasma
Trimastix

Mastigamoeba invertens
Hartmannella
Bodo
Naegleria
Dictyostelium
mycetozoan slime moulds
Physarum
Mastigamoeba balamuthi
Mastigella commutans
pelobionts - well almost all of them
Mastigamoeba sp.
Mastigamoeba simplex
Endolimax nana
Entamoeba gingivalis
entamoebae
Entamoeba histolytica
Entamoeba coli
Trepomonas
Trichomonas
45
Focussing and (taxonomically) intensifying the
analysis - the sister group of the
pelobionts are the entamoebae
Hyperamoeba
slime moulds
Physarum
Entamoeba gingivalus
Entamoeba histolytica
Entamoeba coli
entamoebae
Endolimax nana
Mastigamoeba simplex
Mastigamoeba sp.
pelobionts
Mastigamoeba balamuthi
Mastigella commutans
ramicristate amoebae
Hartmannella vermiformis

Mastigamoeba invertens
Oxytricha
46
Focussing and (taxonomically) intensifying the
analysisthe sister group to the pelobionts are
entamoebaeleading to models of character
innovation
tubular mitochondrial cristae
47
faster technologies more taxa genomics
Comprehensive tree
200?
2000
Protein gene sequences
1995
Skeletal trees
1990
Reconstruction begins
16S rRNA sequence data
1985
Scenarios
Rejection of traditional taxonomy
1980
Endosymbiotic origins of organelles
1975
Integrated protistology
More diversity recognized
1970
Electron microscopy
Traditional taxonomy
1965
48
CONCLUSIONS
  • A tree will be assembled with ultrastructural and
    molecular data
  • Early confidence was misplaced

STATUS Structural insights seem robust, but
there are conflicts between molecular trees to be
resolved.
  • Disputes among molecular trees will be resolved
    in part by better taxonomic sampling, and by the
    benefits of accelerated technologies
  • PROSPECT The universal tree will probably be
    assembled from the tips of the branches in, and
    probably within the next decade

49
(No Transcript)
50
CONCLUSIONS
  • A tree will be assembled with ultrastructural and
    molecular data
  • Early confidence was misplaced
  • STATUS Structural insights seem robust, but
    there are conflicts between molecular trees to be
    resolved.
  • Disputes among molecular trees will be resolved
    in part by better taxonomic sampling, and by the
    benefits of accelerated technologies
  • PROSPECT The universal tree will probably be
    assembled from the tips of the branches in, and
    probably within the next decade
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