Is there a role for symbiosis at the origin of Eukaryotes

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Is there a role for symbiosis at the origin of
Eukaryotes ?

• François LALLIER

Université Pierre et Marie Curie Station
Biologique de Roscoff Adaptation et Diversité en
Milieu Marin
Ecole Thématique Endosymbioses - Octobre 2008
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Is there a role for symbiosis at the origin of
Eukaryotes ?

• Setting the time frame when did the first
  Eukaryotes appeared ?
• How did they appear multiple theories and a
  place for symbiogenesis ?
• Possible origin of the major components of the
  eukaryotic cell
• Why only mitochondria and plasts as primary
  endosymbionts ?

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A brief history of life on earth
Age 4,5 billion years (Gy)
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A brief history of life on earth
First atmosphere ?
First oceans ?
First continent ?
Prebiotic soup ?
pl
Iron-sulfur metab. ?
RNA world ?
EUKARYOTES
Lipid membranes ?
mt
DNA world ?
i
PROKARYOTES
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Hadean
4,5 3,8 Gy

• Earth formation 1st atmosphere and 1st ocean
  4.4 billion years ago
• Weather heavy meteorite falls !
• No land masses, and a reductive atmosphere made
  of NH3 H2 CH4 CO2
• Its hell (Hades) during 700 millions years...
• ... but thats when the bricks of life appeared

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Archean
3,8 2,5 Gy

• Age of anaerobic prokaryotes
• First continents
• Still a reducing atmosphere H2 CH4 CO2 N2
• First chemical biomarkers
• Large metabolic diversity in prokaryotes
• Cyanobacteria start to produce oxygen its a
  revolution !

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Proterozoic
2,5 0,6 Gy

• Age of aerobic organisms
• Present time continents but all mixed up
• Atmosphere slowly becomes oxydantO2 ? CO2 ??
  ??
• Aerobic prokaryotes
• First Eukaryotes
• Phototrophic Eukaryotes
• First multicellular organisms

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Phanerozoic
0,6 0 Gy

• Age of multicellular Eukaryotes
• cambrian explosion
• vertebrates
• terrestrial plants
• amphibians
• reptiles
• dinosaures
• birds
• mammals
• primates
• ...

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Oxygen, the major trigger
HADEAN
ARCHEAN
PROTEROZOIC
PHAN.
Atmospheric Oxygen ()
today
time (109 y)
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Oxygen, the major trigger
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Of fossils, biomarkers and molecular clocks

• How old are the Eukaryotes ?
• Biomarkers stable organic molecules that
  supposedly can only be synthesized by specific
  organisms,
• e.g eukaryotes sterols
• lanostane, most ancient, but some bacteria can
  make it too
• steranes, more recent, may be really diagnostic
  of Eukaryotes

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Of fossils, biomarkers and molecular clocks

• How old are the Eukaryotes ?
• Fossils preserved organisms whose morphological
  characteristics may be interpreted as eukaryotic
  features (cytoskeleton, internal membranes, ...)
• Often very hard to relate them to extant clades
• convincing most ancient microfossil evidence
  1.5 Gy in Lower Mesoproterozoic successions

e.g. Roper Group, Australia
Tappania plana
Valeria lophostriata
The vesicle size appendage diameter, number,
distribution and morphology (branching,
heteromorphic) and the presence of neck-like
extensions in Tappania indicate an early
eukaryotic cell with a cytoskeleton Javaux, 2007
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1.5 Gy
Paleovaucheria
Bangiomorpha
Proterocladus
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The composition and taxonomic richness of
non-metazoan eukaryotes in Proterozoic to Early
Cambrian fossil assemblages
Knoll et al, PTRSB, 2006, 361 1023
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Javaux, 2007
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Of fossils, biomarkers and molecular clocks

• How old are the Eukaryotes ?
• Phylogenetic trees and molecular clock
• Molecular estimates of divergence times are
  controversial and were generally much more
  ancient than suggested by the fossil record
• Larger, taxon- and gene-rich analyses, relaxed
  molecular clock, and progress in tree
  reconstruction methods the promises of
  phylogenomics
• Reconcile tree-like (vertical inheritance through
  common descent) and non-treelike (LGT and
  endosymbiosis) mechanisms of evolution

gt 2 Gy
1 to 1.3 Gy
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129 proteins 36 taxa Bayesian relaxed molecular
clock Fossil calibration (?) 95 credibility
intervals on node ages
Douzery, et al., Proc. Nat. Acad. Sc. USA 101
(43), 15386 (2004).
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• How did they appear multiple theories ......
  and a place for symbiogenesis ?

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Prokaryotes ? Eukaryotes
membrane
cytoplasm
DNA
ribosomes
NUCLEUS
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Eukaryotes genome is chimeric
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Theories forEukaryotes origin

• In 2008 nothing is certain !
• The story of LUCA (Last Universal Common
  Ancestor) and of LECA (Last Eukaryotic Common
  Ancestor)
• Many hypotheses in 3 main families
• 1. LUCA was a (proto)Eukaryote LECA was close
  Archaea Bacteria could even be derived and
  simplified
• 2. LECA originates from a fusion/syntrophy/symbio
  sis between Archaea Bacteria
• 3. LUCA is a bacteria and LECA is close to
  Archaea, having a common ancestor within the
  Bacteria, the Neomura

E
B
A

E
B
A

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LUCA was already a complex organism

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Symbiosis
B ? A
A ? B
SET
syntrophy
eocyte
hydrogen
oxygen
sulfide
Moreira Lopez-Garcia
Margulis
Lake Rivera
Martin Müller
Vellai Vida
Searcy
From Embley Martin, Nature 2006, 440623
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Serial Endosymbiosis Theory
Margulis et al. Paleobiology, 2005, 31 175
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Syntrophy hypothesis

• Methanogenic Archaea
• d proteobacteria
• a proteobacteria
• d-proteobacteria
• CHOn -gt CO2 H2
• methanogen
• H2CO2 -gt CH4
• a-proteobacteria
• CH4O2 -gt CO2H20

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Hydrogen hypothesis

• Methanogenic Archaea
• a proteobacteria
• a proteobacteria CHOn -gt CO2 H2
• methanogen
• H2CO2 -gt CH4

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E
B
A

Cavalier-Smith, BioDirect 2006, 119
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Major components of the eukaryotic cell
About 1500 million years ago, in a world
inhabited by prokaryotes, a novel type of
cellular organization appeared, characterized by
a complex network of endomembranes, and a dynamic
internal skeleton able to protrude, constrict and
move these membranes. Gáspár Jékely
Membranes and nucleus - compartmentalization and
exchanges - exo- and endocytosis - phagotrophy a
prerequisite for endosymbiosis ? - nucleus a
consequence of endosymbiosis ? Cytoskeleton -
motility and regulation of intracellular
traffic - cilium autogenous formation possible
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Membranes
Hypothetical steps in the development of the
eukaryotic cytomembrane system
enzyme secretion
reversible vesiculation
proto-LY
proto-ER
proto-Golgi
exocytosis
from extracelular digestion to phagocytosis
From De Duve Nat Rev Genet 2007,8395
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Membranes
Hypothetical steps in the development of the
eukaryotic cytomembrane system
From Jékely 2007
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Nucleus
massive gene transfer from symbiont multiplication
of introns necessity to process RNA gt
spliceosome slow maturation vs fast
translation gt physical separation of the 2
processes with import/export capacities gt
nuclear enveloppe with nuclear pore
complexes transcription and splicing in the
nucleus translation in the cytoplasm
From Martin Koonin Nature 2006,44041
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CytoskeletonActin Tubulim
Actin and tubulin, major actors of the
cytoskeleton Both have ( distant) homologs in
Prokaryotes Actin ltgt MreB
Tubulin ltgt FtsZ
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Cytoskeleton - Cilium
Today, a highly complex structure, gt 250
proteins involved Acquired from endosymbiosis
(spirochetes) ? Autogenous formation possible
From Mitchell 2007
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Subcellular proteomes
Eukaryote Specific Protein
Cellular Signature Structure
Kurland et al. Science 2006, 312 1011
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Is there a place for symbiosis at the origin of
Eukaryotes ?

• in 1998, YES !
• the syntrophy or hydrogen hypotheses were
  prevalent
• in 2008, probably not
• autogenous evolution of a phagotrophic
  proto-eukaryotic lineage from a bacterial
  ancestor...
• ...but expansion of Eukaryotes follows
  endosymbiotic acquisition of mitochondria
• tomorrow ?

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Why only mitochondria and plasts as primary
endosymbionts ?
A limited use by Eukaryotes of the metabolic
diversity of Prokaryotes
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Symbiosis and Eukaryotes origins
0 ?
1

• Symbiogenesis the chimeric nature of Eukaryotes
  is partly due to endosymbiosis events
• mitochondria and plasts have bacterial origins
• a phagotrophic protoeukaryote may have evolved
  autogenously
• recent endosymbioses allow acquisition of new
  metabolic capacities

?
2
3 ?
F. H. Lallier, Cahiers de Biologie Marine (2006).
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