a hierarchical model for evolution of ribosomal rna konstantin bokov and sergey steinberg...
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A hierarchical model for evolution of ribosomal RNA
Konstantin Bokov and Sergey Steinberg
Université de Montréal
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SMALLSUBUNIT
LARGESUBUNIT
The ribosome is a universal machine producing proteins
TRANSPORTRNA
MESSENGERRNA
- addition of new peptides to the growing protein chain (in PTC);
- correct decoding of the messenger RNA (in DR);
- precise movement along the messenger RNA;
- coordination of the work of all co-factors and ligands;
GROWINGPROTEIN
PTC
DR
225’
P A
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The evolution of Life on Earth directly depends on the emergence of the ribosome !
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Protein World
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The ribosome and LUCA
LastUniversalCommonAncestor
Bacteria Archaea Eukarya
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Functionality of the ribosome depends primarily on its RNA
Large subunit
RNA proteins++
Small subunit
++RNA proteins
RNA-bodyRNA-body
RNA+proteinsRNA+proteins
RNA-WORLD
Protein-WORLD
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MODERNRIBOSOME
F
Major periods in the evolution of the ribosomal RNA
PROTORIBOSOME
Unlimited reshuffling of RNA chains
F FRestricted step-wise increase of the ribosome size
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insertion gene sequence
5’ 3’ 5’3’
Preserve functional structure !
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Accommodation of an insertion
Broken Unstable Stable
insertion
gene sequence
gene sequence
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General principle of insertion:
Structural integrity of more ancient elements cannot be dependent on the presence of more recently acquired elements.
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Integrity of each strand of a double helix depends on the presence of the other strand
1010
5’
3’5’
3’
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The A-minor motif as an evolutionary determinant
A-minor motif
Nissen, P., Ippolito, J.A., Ban. N., Moore, P.B., Steitz, T.A. (2001) RNA tertiary interactions in the large ribosomal subunit: the A-minor motif. Proc Natl Acad Sci U S A. No 98(9), pp. 4899-4903.
1111
23S rRNA23S rRNA
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In a newly emerged element:
1. The 3’- and 5’-termini must be close to each other2. For each double helix, both strands must be present3. When such element forms an A-minor interaction with the other elements of the ribosome, it must provide the adenosine stack and not the double helix
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Dismantling the ribosomal RNA: removal of those elements that are qualified as the most recent acquisitions of the ribosomal structure
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MODERNRIBOSOME PROTO-
RIBOSOME
core
Last acquisitions 2-nd last acquisitions
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Dismantling the structure of the 23S rRNA
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Inter-domain A-minor interactions
double helix
stack of adenosines1515
A-minA-min
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Dismantling the structure of the 23S rRNA
1616
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The symmetrical structure in Domain V is the proto-ribosome
t-RNA
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A-site
P-site
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The network of dependencies does not contain cycles
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If the orientations of all A-minor interactions in the 23S rRNA were chosen randomly, the probability of a cycle-free arrangement would be P< 10-9.
The absence of cycles of dependency is a fundamental characteristic of the 23S rRNA, which is directly related to the particular trajectory of its emergence.1919
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Growing support for PTC
2020
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Appearance of the protuberances and of the small subunit
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What about 16S rRNA?
2121
LSUSSU
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The hypothetical structure of the primordial ribosome and two tRNAs
2525
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Small world...
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Acknowledgment
We appreciate the help ofNSERC and CIHR for financing this project.
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presentationpresentation
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Non-covalent dependency
Double helix is older than stack of A-s packing in its minor groove
H71
H68
H69
A-stack (in red)
H92
H93
H95
A-stack (in red) A-stack (in red)
H74
H69
H71
H93
H92H68
H95H74
E-coli, 23S E-coli, 23S E-coli, 23S
Chain of A-minor interactions
AA
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Pseudoknot
The loop of a stem-loop structure (A) forms a double-helix (B) with a region outside this stem-loop
A
B
C
for example with another stem-loop (C)BB
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Pseudoknots in the 23S rRNA
CC
- local- non-local
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Long-distance pseudoknots in the 23S rRNA
DD
40 40
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The approach is applicable
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H2
(G-C) H25
(G-U)
Along-groove packing” motif as a mean of structural fitting
H2 minor groove
H25 minor groove
G17-C523
G539-U554
Along-groove packing motif
E-coli, 23S
FF
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Along-groove packing motif
GG
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AGPM-s in 23S rRNA
HH
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What about evolutionary deletions ?
A
C=A-D
evolution
B
LL
X
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?
Accommodation must not provoke structure weakening
MM
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Notion of dependency
C
A
B
Additional
E-coli, 23S
A
B
C
Covalent dependency
The new RNA insertion covalently depends on the structure where it emerged
Core
Core
Non-covalent dependency (A-min)
D
E
E-coli, 23SB
A
yellowA-stacks
A
B
C
D
E
C
The element containing stack of adenosines is non-covalently dependent on its complimentary WC helix
In PCKWC helices
A A
NN
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Domain-V is the most ancient part of the ribosome
PP
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16S mitochondrial versus prokaryotes
Only prokaryotes
Mito and prokaryotesRR
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23S mitochondrial versus prokaryotes
Only prokaryotesMito and prokaryotesSS
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Dismantling versus evolution
TT
MODERNRIBOSOME PROTO-
RIBOSOME
PROTO-RIBOSOME
MODERNRIBOSOME
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19 54 26 26 11 11 25 47
36 27 45 57 40 51 20 40
AGPMs in the ribosome of E.coli
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The evolution of Life on Earth directly depends on the emergence of the ribosome !
22
Protein World