Download On the nature of the last common universal ancestor

On the nature of the last common
universal ancestor
David Moreira
[email protected]
CNRS - Université Paris-Sud
• A historical approach
• A robot portrait of the last common ancestor
"Phylogeny studies the relationships among
organisms to understand their evolution"
Two historical periods:
“before the evolutionary theory”
“after the evolutionary theory”
The ancestor of phylogeny: classification
Linné, 1707-1778
Hierarchical system with three
kingdoms: animals, plants,
and minerals.
Augier, 1801
The beginings of evolutionary theory
• Species can transform ("evolve")
• The different species are related
• They share a basic structural unit: the cell
Theodor Schwann (1810-1882) :
‘Cell theory’: all living beings are composed
of cells
Charles Darwin (1859) :
‘Probably all the organic
beings which have ever
lived on this earth have
descended from some
primordial form, into which
life was first breathed’
Ernst Haeckel (1834-1919) :
First ‘universal phylogeny’
La phylogénie moléculaire
Carl Woese (70’s) : la révolution ‘woesienne’
Eucarya
Archaea
Bacteria
Grec kainos, qui signifie récent et koinos, qui signifie commun)
La phylogénie moléculaire
Carl Woese (70’s) : la révolution ‘woesienne’
Eucarya
Archaea
Bacteria
Grec kainos, qui signifie récent et koinos, qui signifie commun)
LAST COMMON ANCESTOR
Molecular biology (1950…)
Molecular biology
All living beings share similar biochemical traits
‘What is true for Escherichia coli is true for elephants’
(Jacques Monod)
Molecular biology
Proteins
(ATPases, ribosomal, etc)
Membrane - Lipids
Last
common
Genetic
material
- DNA
Ribosomes
Polysaccharides
ancestor?
The last common ancestor and the origin of life
LCA
Prebiotic chemistry
Origin
of life
Present life
s
ge
u
ro s
a
s
ld o e b
e
u
u
m
o
lg
s
A e m n ta
b e s la sti de
E
i
m
m
A
i
p
Sl
éto
K in glena
s
i ne
Eu
n ad
o
ne s
m
n adi
ho
o
c
i
m
r
lo
T
Dip
ridie s
o sp o
r
c
i
M
St r
Champignons
am
én
op
il es
C
i
D lié
i
A no s
pi fl
co a g
m el
pl lé
èx s
es
Comparative genomics
Animaux
Plantes
lf
Su
Bacteria
Bacteria
Ch
le
ba
olo
la
ale s
rmo
to g
The
A qu
i fi ca
le s
cto
my
es
ce
(
s
n
so
o
n
uf r
du
e)
s
a
te
pro
le s
Archaea
Archaea
o
e rm
h
le s
T
s
ca
c
a le
co
m
o
s
a
erm mop l
es
Th
bal
er
lo
g
h
o
T
h ae
A rc
Halobactériaceae
Me
M
th
et
an
ha
om
no
i cr
ba
ob
ia
ct
le s
ér
ia
le
s
s
le
ra
Ve
rt
py
no
ha
Pl
an
et
M
my
Protéobactéries
di
ale
c hè
t es
s
Bac
te ro i
d
e
s
V e rte s
d u sou
fre
Cianobactéries
GC
L ow
GC
es
gh
siti v
o
i
p
H
m
G ra
/
us cus
m
er oc
Th noc
ei
D
Sp
i ro
Eucarya
UNIVERSAL GENES = ANCESTRAL GENES
ANCESTRAL GENES = THOSE FOUND
IN ARCHAEA AND BACTERIA
Comparative genomics: ancestral genes
Archaea and bacteria share many caracters
but...
only ~60 genes are shared by all species
• rRNAs
et ribosomal proteins : protein synthesis with a very
evolved molecular machinery
• RNA polymerase: RNA synthesis similar to that of contemporary
cells
• Membrane
ATPase: ATP synthesis using a H+ gradient
Ö presence of a cell membrane?
Comparative genomics: ancestral genes
~60 genes are not enough to assure a cell metabolism, even the
simplest one
Certain genes are lost in certain species (parasites…)
Less strict criteria are necessary
• Comparison of groups of species instead
of individual species
• Looking for gene families instead of
specific individual genes
500-600
ancestral
genes
Comparative genomics: ancestral genes
• >500 genes : genome size comparable to that of many
small prokaryotes
• Capacity to code for a complex metabolism
but many caracteristics of this ancestral metabolism
remain controversial…
Genomes may help to find the good answer
The lipid problem:
Had the last common ancestor a lipid membrane?
Phospholipid structure
phosphate
(PO43-)
Hydrocarbon chain
glycerol
(C3)
—
Hydrocarbon chain
(C14-C20)
Koga et al. 1998
Martin & Russell 2003
Had the last common ancestor a lipid membrane?
• G1PDH et G3PDH belong to two ancestral enzymatic superfamilies
• Most of the enzymes involved in synthesis and degradation of fatty
acids and isopreénoids are also ancestral
Pereto et al. 2003
Lombard et al. 2013
Had the last common ancestor a lipid membrane?
It had the enzymes to synthesize glycerol, fatty acids, and isoprenoids :
It had a lipid membrane
The ancestral genome : DNA or RNA?
• Many proteins involved in RNA metabolism
are universal
• Few proteins involved in DNA replication
and repair are conserved between bacteria
and archaea
The last common ancestor synthesized RNA but not DNA?
Had it a RNA genome?
Mushegian & Koonin 1996
Leipe et al. 1999
Koonin & Martin 2005
Forterre 2006
Glansdorff, Xu & Labedan 2008
The origin of DNA and its replication
BACTERIA
Forterre, 1999
ARCHAEA
Forterre, 2006
RNA
EUCARYA
Villareal, 2003
Forterre, 2006
The origin of DNA and its replication
HOWEVER :
• No known virus has all the genes needed
for the synthesis and replication of DNA.
All viruses depend on the machineries
of the infected cells.
• Genes involved in DNA synthesis and replication
have been transferred from the host cells towards
the viruses that infect them.
No evidence to support that viruses
have "invented" DNA
The origin of DNA and its replication
• Some DNA replication and repair enzymes are ancestral:
Evidence for a DNA genome in the last common ancestor?
• RNA genomes have a maximum size of 35-50 kb, this is
the ‘Eigen limit’ which is due to:
• High error frequency during RNA replication
• High mutation rate
Incompatible with a genome of >500 genes inferred
for the last common ancestor
It likely had a DNA genome
The question of temperature :
Was the last common ancestor hyperthermophilic?
St r
am
én
op
il es
C
i
D lié
A in o s
pi fl
co a g
m el
pl lé
èx s
es
The question of temperature :
Was the last common ancestor hyperthermophilic?
Champignons
Animaux
Plantes
Bacteria
si ti
v
es
l es
myd ia
Ch l a
es
hè t
i roc
s
Sp
de re
f
ro i
cte sou
u
po
sd
am
ba
ct
é
Ba
Gr
no
r te
Ve
C
ia
ri e
s
Lo
w
GC
Hi g
h GC
le
ba
olo
f
l
Su
Th
s
g
o to
m
r
e
o
rm
a
te
pro
le s
Archaea
le s
s
c ca
o
a le
oc
sm
a
m
l
r
e
op
le s
Th
e rm
lo ba
g
o
Th
h ae
A rc
Halobactériaceae
Me
M
th
et
an
ha
om
no
i cr
ba
ob
ia
ct
le s
ér
ia
le
s
s
le
ra
Aq
le
i ca
u if
s
e
Th
py
no
ha
es
to myc
P la n c
u
nd
(n o
s
)
rt e
V e ou f re
s
ro
té
ob
ac
té
ri e
s
Eucarya
et
M
Thermus /
Deino coccus
P
s
ge
u
ro s
a
s
ld o e b
e
u
u
o m
lg
s
A e m n ta
b e s la sti de
E
A mi
il m
p
S
éto
K in glena
es
u
adi n
E
n
o
ne s
hom
n adi
Tric Diplo mo
ie s
p o rid
s
o
r
c
Mi
s
ale
Stetter 1996
am
én
op
il es
C
i
D lié
A in o s
pi fl
co a g
m el
pl lé
èx s
es
St r
Champignons
Animaux
Plantes
Bacteria
si ti
v
es
l es
myd ia
Ch l a
es
hè t
i roc
s
Sp
de re
f
ro i
cte sou
u
po
ri e
s
Lo
w
GC
Hi g
h GC
Th e rmo
to g ale s
s
a
te
pro
le s
Archaea
o
e rm
h
le s
T
ca
le s
c
c o a s ma
o
pl
es
e rm
bal
Th he rmo
lo
g
o
T
h ae
A rc
Halobactériaceae
Me
M
th
et
an
ha
om
no
i cr
ba
ob
ia
ct
le s
ér
ia
le
s
s
le
ra
es
?
py
no
ha
an
Pl
yc
m
o
t
c
ro
té
ob
ac
té
ri e
s
et
M
Th ermus /
De ino coccus
(n on du
les
V e rte s
fica
so u fre) A qui
P
Eucarya
a le
lo b
o
f
l
Su
sd
am
ba
ct
é
Ba
Gr
no
r te
Ve
C
ia
s
ge
u
ro s
ba
s
e u ld o e
u
m
g
o
l
s
A e m n ta
b e s la sti de
E
i
m
m
A
i
p
Sl
éto
K in glena
s
i ne
Eu
n ad
o
es
m
adi n
ho
Tric Diplo mo n
ridie s
o sp o
r
c
i
M
Brochier & Philippe 2002
Adaptations of bacteria and archaea to high temperatures are not
exactly the same, so probably they have not been inherited from a
hyperthermophilic last common ancestor.
However, it may have been mesophilic or thermophilic
A mesophilic last common ancestor?
Boussau et al., 2008
A thermophilic last common ancestor?
Nature, 2008
A thermophilic last common ancestor?
Earth was warmer during
the Archaean period
Age (Gyr)
Robert & Chaussidon, 2006
But… Hren et al. (2009) have found a
temperature ~40°C colder!
Metabolism (C et energy)
Very difficult to study : the genes involved have been
very frequently transferred between distant lineages
Metabolism (C et energy)
• A membrane ATPase was used
to synthesize ATP with a proton
gradient across the membrane
• Very likely a heterotrophic metabolism,
metabolism with simple
glycolysis and fermentation pathways
• Oxygen respiration?
respiration Very controversial, a possible
source of oxygen before the evolution of oxygenic
photosynthesis remains unknown
Conclusion: a very complex ancestor
Proteins
(ATPases, ribosomal, etc)
Membrane - Lipids
Genetic material - DNA
Ribosomes
Polysaccharides
Rapid evolution between the origin of life and the last
common ancestor
Conclusions
- Phylogeny and genomics allow the study of the caracteristics of
ancestral species
- The last common ancestor was a complex organism
- Several basic molecular functions of cells have not significantly
changed for billions of years (no permanent "complexification"
is observed)