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Supplementary Information S3 (Table)
Protein export through the bacterial Sec pathway
Authors: Alexandra Tsirigotaki, Jozefien De Geyter, Nikolina Šoštarić, Anastassios
Economou and Spyridoula Karamanou
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Table S3. Overview of protein structures mentioned/used throughout this review.
Structure
Section
Ref.
ID
MethodResolution
Thermotoga maritima SecYEG-SecA:ADP-BeFx (mimic for ATP-prehydrolysis) complex
3DIN
X-ray (4.5Å)
1
Methanocaldococcus jannaschii SecYE (resting closed state)
1RH5
X-ray (3.2Å)
2
Methanocaldococcus jannaschii SecE-30S, 50S ribosome complex
4V4N
EM (9.0Å)
3
Escherichia coli non-translocating SecYEG-50S ribosome complex
3J45
EM (9.5Å)
Escherichia coli active SecYEG-50S ribosome complex
3J46
EM (10.1Å)
NA
EM (8.0Å)
4
Escherichia coli SecYEG
3BO0
EM (9.6Å)
5
Geobacillus thermodenitrificans SecYE- Bacillus subtilis SecA complex with synthetic peptide
5EUL
X-ray (3.7Å)
6
Thermus thermophilus resting state of SecYEG
5AWW
X-ray (2.72Å)
7
Thermus thermophilus peptide-bound state of SecYEG
5CH4
X-ray (3.64Å)
Escherichia coli SecYE inserting the membrane protein proteorhodopsin
5ABB
EM (8.0Å)
8
Thermus thermophilus pre-open state of SecYE (with anti-SecY Fab fragment (mus musculus))
2ZJS
X-ray (3.2Å)
9
Escherichia coli 50S ribosome-SecYEG complex
5GAE
EM (3.33Å)
10
Escherichia coli 50S ribosome-Ffh-FtsY- PhoA signal peptide complex
5GAD
EM (3.7Å)
Escherichia coli 50S ribosome-SRP-PhoA signal peptide complex
5GAF
EM (4.3Å)
Escherichia coli 50S ribosome-Ffh-PhoA signal peptide complex
5GAG
EM (3.8Å)
Escherichia coli 50S ribosome-Ffh (detached NG domain)-PhoA signal peptide complex
5GAH
EM (3.8Å)
Escherichia coli 30S,50S ribosome-SecYE complex
4V6M
EM (7.1Å)
11
Escherichia coli SecYEG2
2AKH
EM (14.9Å)
12
Structure description
Protein
SecYEG
and
homologu
es
Introduction
Escherichia coli SecYEG (back-to-back dimer) unlocked with a signal peptide
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NA
EM (8.0Å)
13
Bacillus subtilis SecA - Geobacillus thermodenitrificans SecYE complex with synthetic peptide
5EUL
X-ray (3.7Å)
6
Bacillus subtilis SecA2
1M6N
X-ray (2.7Å)
15
Mg-ADP-bound SecA2
1M74
X-ray (3.0Å)
Escherichia coli SecA2
2FSF
X-ray (2.0Å)
Escherichia coli ATP-bound SecA2
2FSG
X-ray (2.2Å)
Escherichia coli AMP-PNP-bound SecA2
2FSH
X-ray (2.0Å)
Escherichia coli ADP-bound SecA2
2FSI
X-ray (2.11Å)
Thermotoga maritima SecYEG- SecA:ADP-BeFx (mimic for ATP-prehydrolysis) complex
3DIN
X-ray (4.5Å)
1
Mycobacterium tuberculosis SecA2
1NL3
X-ray (2.8Å)
17
Mycobacterium tuberculosis Mg-ADP-bound SecA2
1NKT
X-ray (2.6Å)
Thermus thermophilus SecA2 (head-to-head)
2IPC
X-ray (2.8Å)
18
Bacillus subtilis ADP-bound SecA
2IBM
X-ray (3.2Å)
19
Thermotoga maritima Mg-ADP-bound SecA
4YS0
X-ray (1.9Å)
20
Escherichia coli YidC
3WVF
X-ray (3.2Å)
21
Bacillus halodurans YidC
3WO7
X-ray (3.2Å)
22
Ribosome-bound YidC
4UTQ
EM (8.0Å)
23
Thermus thermophilus SecDF
3AQP
X-ray (3.3Å)
24
Staphylococcus aureus SPase I bound to maltose binding protein fragment (Escherichia coli)
4WVG
X-ray (2.05Å)
25
Escherichia coli catalytically active fragment of signal peptidase I
1KN9
X-ray (2.4Å)
26
Escherichia coli closed state of SecYEG2
SecA14
YidC
SecDF
Signal
peptidase
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Oligomeric state
of SecA
SecA dynamics
Architecture of
SecYEG channel
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Pseudomonas aeruginosa signal peptidase II
5DIR
X-ray (2.8Å)
27
Monomeric
Thermotoga maritima SecYEG- SecA:ADP-BeFx (mimic for ATP-prehydrolysis) complex
3DIN
X-ray (4.5Å)
1
Methanocaldococcus jannaschii SecYE (closed)
1RH5
X-ray (3.2Å)
2
Oligomeric
Escherichia coli SecYEG2 (back-to-back dimer) unlocked with a signal peptide
NA
EM (8.0Å)
4
Escherichia coli closed state of SecYEG2
NA
EM (8.0Å)
13
Escherichia coli SecYEG2
2AKH
EM (14.9Å)
12
Mycobacterium tuberculosis SecA2 (apo-form)
1NL3
X-ray (2.8Å)
17
Mycobacterium tuberculosis Mg-ADP-bound SecA2
1NKT
X-ray (2.6Å)
Bacillus subtilis SecA2 (apo-form)
1M6N
X-ray (2.7Å)
Mg-ADP-bound SecA2
1M74
X-ray (3.0Å)
Bacillus subtilis SecA (apo-form)
1TF5
X-ray (2.18Å)
Bacillus subtilis Mg-ADP-bound SecA
1TF2
X-ray (2.9Å)
Escherichia coli SecA2 (apo-form)
2FSF
X-ray (2.0Å)
Escherichia coli ATP-bound SecA2
2FSG
X-ray (2.2Å)
Escherichia coli AMP-PNP-bound SecA2
2FSH
X-ray (2.0Å)
Escherichia coli ADP-bound SecA2
2FSI
X-ray (2.11Å)
Mycobacterium tuberculosis SecA2
1NL3
X-ray (2.8Å)
Mycobacterium tuberculosis Mg-ADP-bound SecA2
1NKT
X-ray (2.6Å)
Bacillus subtilis SecA2
1M6N
X-ray (2.7Å)
Mg-ADP-bound SecA2
1M74
X-ray (3.0Å)
Escherichia coli SecA2
2FSF
X-ray (2.0Å)
Nucleotid
e-states
Dimer
interface
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28
16
17
15
16
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Escherichia coli ATP-bound SecA2
2FSG
X-ray (2.2Å)
Escherichia coli AMP-PNP-bound SecA2
2FSH
X-ray (2.0Å)
Escherichia coli ADP-bound SecA2
2FSI
X-ray (2.11Å)
NA
EM (1.7nm)
29
Thermus thermophilus SecA2
2IPC
X-ray (2.8Å)
18
Bacillus subtilis ADP-bound SecA
2IBM
X-ray (3.2Å)
19
Thermotoga maritima SecYEG- SecA:ADP-BeFx (mimic for ATP-prehydrolysis) complex
3DIN
X-ray (4.5Å)
1
Escherichia coli 50S ribosome-SecYEG complex
5GAE
EM (3.33Å)
10
Methanocaldococcus jannaschii SecE-30S, 50S ribosome complex
4V4N
EM (9.0Å)
3
Escherichia coli non-translocating SecYEG-50S ribosome complex
3J45
EM (9.5Å)
Canis lupus non-translating ribosome-Sec61α,β,γ complex
4CG7
EM (6.9Å)
30
Saccharomyces cerevisiae idle Ssh1- 60S ribosome complex
2WWA
EM (8.9Å)
31
3J7Q
EM (3.4Å)
32
NA
EM (8.0Å)
4
Bacillus subtilis SecA - Geobacillus thermodenitrificans SecYE complex with synthetic peptide
5EUL
X-ray (3.7Å)
6
Canis lupus Sec61α,β,γ activated by prolactin signal peptide (Bos taurus)
3JC2
EM (3.6Å)
33
Escherichia coli active SecYEG-50S ribosome complex
3J46
EM (10.1Å)
3
Canis lupus Sec61α,β,γ activated by membrane-inserting substrate
4CG6
EM (7.8Å)
30
Escherichia coli 30S,50S translating ribosome-SecYE complex
4V6M
EM (7.1Å)
11
Escherichia coli SecA-maltoporin signal peptide complex
2VDA
NMR
34
Escherichia coli SecA2
SecYEG-priming by
ribosome
SecYEG/
A copies
Sus scrofa ribosome- Sec61α,β,γ complex
Figure 1
SecYEG-activation by
preproteins
Escherichia coli SecYEG (back-to-back dimer) unlocked with a signal peptide
Opening
at various
degrees
panel d
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Figure 2
panel a
bottom
In format provided by Tsirigotaki et al. (doi:10.1038/nrmicro.2016.161)
Escherichia coli SRP-FtsY complex
6
2XXA
X-ray (3.94Å)
35
FtsY not shown.
panel a
middle
Escherichia coli 50S ribosome-SRP-PhoA signal peptide complex
5GAF
EM (4.3Å)
10
panel a
top
Escherichia coli 50S ribosome-Ffh-FtsY-PhoA signal peptide complex (early targeting complex)
5GAD
EM (3.7Å)
10
panel b
bottom
Vibrio cholerae trigger factor (TF2)
1T11
X-ray (2.5Å)
36
Escherichia coli TF-50S ribosome complex
Complete trigger factor structure as in file 2VRH was aligned to the structure of ribosome in
complex with a small part of trigger factor (residues 25-59; 1W2B)
2VRH
EM (19.0Å)
37
panel b
middle
1W2B
X-ray (3.5Å)
38
2MLX,
2MLY,
2MLZ
NMR
39
panel b
top
Escherichia coli trigger factor-unfolded proPhoA complex
The model was made by combining the respective structures, each containing a single trigger
factor molecule in complex with a different part of PhoA chain (its N-terminal, middle and Cterminal sequence, respectively)
Escherichia coli SecB4
1QYN
X-ray (2.35Å)
40
(5JTL)
Personal
communic
ation with
NMR
41
X-ray (2.8Å)
42
panel c
bottom
Escherichia coli SecB4 in complex with unstructured proPhoA
panel c
middle
41
panel c
top
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Haemophilus influenzae SecB4-SecA(C-tail) complex
1OZB
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bottom
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Bacillus subtilis SecA2 (one protomer was used)
1M6N
X-ray (2.7Å)
Escherichia coli SecA-maltoporin signal peptide complex (only SecA is shown)
2VDA
NMR
Escherichia coli SecA2 (only ATP is shown)
The structures were aligned with respect to Stem; in the final model represented, only Stem and
C-tail parts denoted in dark green originate from the structure 1M6N. For assignment of the ATPbinding site, SecA from the 2FSG structure was aligned to the structure 2VDA and only ATP is
shown.
2FSG
X-ray (2.2Å)
EMDB256
5
EM (10.3Å)
SecA1-70S ribosome electron density map
panel d
middle
7
Mg-ADP-bound SecA2
One SecA (1M74) protomer was modeled (Chimera) into the respective SecA-70S ribosome
electron density map.
15
34
X-ray (3.0Å)
16
43
15
1M74
Bacillus subtilis SecA-synthetic peptide complex
3JV2
X-ray (2.5Å)
44
panel d
top
Escherichia coli SecA-maltoporin signal peptide complex (only signal peptide is shown)
2VDA
NMR
34
panel a
Methanocaldococcus jannaschii SecYE (resting closed state of SecYEG homologue)
1RH5
X-ray (3.2Å)
2
Sus scrofa non-translating ribosome- Sec61α,β,γ complex
3J7Q
EM (3.4Å)
32
In d the primed Sec61 structure was aligned to the complete SecY sequence of the
Methanocaldococcus jannaschii SecYE closed state (1RH5) for comparison. The elements of
the closed state shown are: SecY TMHs 2b,3,7,10, loop 6/7, SecE.
1RH5
X-ray (3.2Å)
2
Thermotoga maritima SecYEG-SecA:ADP-BeFx (mimic for ATP-prehydrolysis) complex
3DIN
X-ray (4.5Å)
1
In e the activated SecYEG structure was aligned to the SecY sequence 74-187 (TMH 2b-5) of
the Methanocaldococcus jannaschii SecYE closed state (1RH5) for comparison. The elements
of the closed state shown are: SecY TMHs 2b,7,8,9, loop 6/7, plug, SecE.
1RH5
X-ray (3.2Å)
Figure 3
panel b,d
panel c,e
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Escherichia coli SecA structure (2VDA) was aligned to the Bacillus subtilis SecA-tripeptide
(mature domain mimic) complex and only the signal peptide is shown from the 2VDA structure.
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Escherichia coli SecA2 models45 based on:
panel
Bacillus subtilis SecA2 (left)
1M6N
X-ray (2.7Å)
Mycobacterium tuberculosis SecA2 (right)
1NL3
X-ray (2.8Å)
Thermus thermophilus peptide-bound SecYEG
5CH4
X-ray (3.64Å)
7
The peptide mimic corresponds to the hydrophobic SecE N-terminal of a second SecYEG due to
crystal packing. For the cartoon representation, the peptide-mimic-bound SecYEG structure was
aligned to the complete SecY sequence of the resting Thermus thermophilus SecYEG state
(5AWW).
5AWW
X-ray (2.72Å)
7
Canis lupus Sec61α,β,γ activated by membrane-inserting substrate
4CG6
EM (7.8Å)
30
For the cartoon representation, the exported TM-bound Sec61 structure was aligned to the
Sec61α residues 81-191 of the Canis lupus non-translating ribosome-Sec61α,β,γ complex
(4CG7).
4CG7
EM (6.9Å)
30
Canis lupus Sec61α,β,γ activated by secretory substrate
4CG5
EM (7.4Å)
30
For the cartoon representation, the hydropholic peptide-bound Sec61 structure was aligned to
the Sec61α residues 81-191 of the Canis lupus non-translating ribosome-Sec61α,β,γ complex
(4CG7).
4CG7
EM (6.9Å)
30
Canis lupus Sec61α,β,γ activated by prolactin signal peptide (Bos taurus)
3JC2
EM (3.6Å)
33
For the cartoon representation, the preprotein-bound Sec61 structure was aligned to the Sec61α
residues 285-432 of the Sus scrofa non-translating ribosome-Sec61α,β,γ complex (3J7Q).
3J7Q
EM (3.4Å)
32
Escherichia coli SecYE inserting the membrane protein proteorhodopsin
5ABB
EM (8.0Å)
8
Bacillus subtilis SecA - Geobacillus thermodenitrificans SecYE complex with synthetic peptide
5EUL
X-ray (3.7Å)
6
f
panel
a
panel
Figure 4
b
panel c
panel d
15
17
panel e
panel f
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The synthetic peptide contains the signal sequence of OmpA and a 22 residue polypeptide,
inserted with a linker in the SecA sequence between residues 741-744 (IRA1).
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panel b
panel c
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Bacillus subtilis SecA2 (clamp wide open); left
1M6N
X-ray (2.7Å)
Bacillus subtilis SecA (clamp open); middle
1TF5
X-ray (2.18Å)
Thermotoga maritima SecA (clamp closed) from the SecYEG-SecA:ADP-BeFx (mimic for ATPprehydrolysis) complex; right
3DIN
X-ray (4.5Å)
Thermus thermophilus SecDF
3AQP
X-ray (3.3Å)
24
Escherichia coli signal peptidase I
3S04
X-ray (2.44Å)
46
Pseudomonas aeruginosa signal peptidase II
5DIR
X-ray (2.8Å)
27
Escherichia coli PpiD (parvulin domain)
2KGJ
NMR
47
NA: not available
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