Title: THE LAST 35 YEARS
1THE 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
2This talk was published last year American
Naturalist, 154 S96-S124
3EVOLUTIONARY 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
4Traditionally ..
- 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
5Traditionally .. 4 types of protozoa
amoebae flagellates ciliates
sporozoa
6Otto Bütschli his view, 1880
Protozoa Class Sarkodina Class
Mastigophora Class Sporozoa Class Infusoria
Sporozoa
Infusoria
Mastigophora
Sarkodina
Protsville
7MICROSCOPES Royal Mail Mint Stamps
8EVOLUTIONARY 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
9The 1960s and the advent of good fixation
protocols for electron-microscopy
GLUTARALDEHYDE
10Goniomonas
Electron microscopy provides more data
than light microscopy
11Heliozoa
Centrohelids
Actinophryids
12Ultrastructural 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
13How 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
14By 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
15EVOLUTIONARY 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
16Endosymbiosis and the evolution of
eukaryotes from Merschkovsky 1910 .
17The Serial Endosymbiosis Theory is an easy idea
to test .
18EVOLUTIONARY 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
19A 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
20An example of creating bits of the tree
enigmatic opalines large (1 mm.) flat
flagellates living in amphibia
21Opalina
Karotomorpha
Proteromonas
22Hairs link proteromonads to the chrysophytes
23Identifying a lineage leading from algae
to protozoa grouping 3 ultrastructural
identities
24STRAMENOPILES
WITH STRAW HAIRS
Protsville
25The 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
26EVOLUTIONARY 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
27Small subunit (16S) rRNA 1250 - 2500 bases
Large subunit 28S, 5.8S and 5S rRNA
28AACUGGUUGAUCUUGCCAGUAGUCAUAUGCUUGUCUCAAAG AUUAGCCA
UGCAAGUGAAAUAUAUGCAUAUUUUAUAUGUAGAAACUGCGAACGGCUCA
UUAAAACAGUUAUAAUCUAXUUGACAUUUUAUUAUUAUAAGGAUAACUAC
GGAAAACGUGUAGCUAAUAACUUGCUUUAAGUGUUUUUACUUCUUGGAGU
AAUUAGCAUGUAUUGUUAAGCUUAUAAGAAAAAUUUUUAAUUAAAGCAAA
UUAUAACAAAGAAGUAACACAUAAUAUAUUUACUAUAUUUAGUGUGUACA
AUCGAGUUUCUGACCAUUCAGCUUUUCAUGUUAGGGUAUUGGCCUAACAU
GGCAUGACGGGUAACGGGGAAUUAGAGUUCGAUUCCGGAAGAGGGAGCCC
UGAGAAUAGCUACCACAUCUAAGGAAGGCAGCAGGCGGGUAAAUUACCCA
AUUCUAAAUAAGAGGGUAGUGACAAGAAUAACAAUAUAAGGCCAAAUUUU
GGUUUUAUAUAAUUGGAAUGAUGGGAAUUUAAAACCUUCCCAAAAUCAAU
UGGAGGGCAAGUCUGGUGCCAGCAGCAGCCGCGGUAAUUCCAGCUCCAAU
AGCUAUAUUAAAAUUGUUGCAGUUAAAGCGUCGUAGUUGAACUUCAAGGG
UAUUAUUAUUUUAAGUAACUCACUUGCAGAAUCUUGGCUCCGCCUCGAUA
UCUUCAUGCCUUGUUGUAGGUUCUUUUAAUUACACCCUUUGAGACCCCAA
UGAUUUAUCACUGGGUUUU...16SRIBOSOMALRNASEQUENCEFROMS
ARCOCYSTISMURIS ...
Protsville
29Giving universal trees of life
30A typical cell has endoplasmic
reticulum nuclei mitochondria dictyosomes micr
otubular cytoskeleton microfilamentous
cytoskeleton mitosis meiosis
secretory vesicles lysosomes
Wolfe
Protsville
31Microsporidia
32Leading 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?
33Thiobios The anoxic zone under the surface of
mud
34Free-living amitochondriate flagellates
retortamonads
Trimastix
trichomonads
Carpediemonas
pelobionts
diplomonads
35such as Mastigamoeba schizophrenia
pelobionts
Pelobionts Pelomyxa Mastigina
Mastigamoeba Mastigella Phreatamoeba
36Mastigamoeba schizophrenia Pelobionts have
flagella one microtubular root
endoplasmic reticulum nuclei no Golgi
apparatus no mitochondria no plastids no
fibrous cytoskeleton
37Flagellar idiosyncrasies in pelobionts might
indicate that they represent the first of the
flagellated eukaryotes
38But, when the first pelobionts were sequenced
...
39EVOLUTIONARY 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
40Molecular 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
41EVOLUTIONARY 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
42EVOLUTIONARY 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)
44A 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
45Focussing 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
46Focussing and (taxonomically) intensifying the
analysisthe sister group to the pelobionts are
entamoebaeleading to models of character
innovation
tubular mitochondrial cristae
47faster 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
48CONCLUSIONS
- 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)
50CONCLUSIONS
- 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