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1 Supplementary Information Structural analysis of leader peptide binding enables leaderfree cyanobactin processing Jesko Koehnke 1,2, Greg Mann 1,2, Andrew F Bent 1,2, Hannes Ludewig 1, Sally Shirran 1, Catherine Botting 1, Tomas Lebl 1, Wael Houssen 3,4,5, Marcel Jaspars 3 & James H Naismith 1,6* 1 BSRC, University of St Andrews, St Andrews, KY16 9RH 2 Equal contribution 3 Marine Biodiscovery Centre, Department of Chemistry, University of Aberdeen, Meston Walk, Aberdeen, AB24 3UE 4 Institute of Medical Sciences, University of Aberdeen, Aberdeen AB25 2ZD, Scotland, UK. 5 Pharmacognosy Department, Faculty of Pharmacy, Mansoura University, Mansoura 35116, Egypt. 6 State Key Laboratory of Biotherapy, Sichuan University, China * To whom correspondence should be addressed James Naismith, Naismith@st-andrews.ac.uk
2 Supplementary Results Supplementary Figures Supplementary Figure 1: Gel Filtration Chromatographs of LynD and LynDfusion. Gel filtration chromatographs of LynD (green) and LynDfusion (red). Comparing their retention times to commercially available gel filtration standards (Bio-Rad) (blue) both proteins elute with a retention time approximately consistent with a dimer.
3 Supplementary Figure 2: ITC of Nucleotide Binding. ITC data obtained for the injection of ATP and AMP injected into LynD and LynD mutant solutions. The top panel shows the raw data representing response to injections. The lower panel shows the integrated heats of injections ( ) and the best fit ( ) to the One-Site model (origin). Data for LynD R636A + ATP could not be fitted.
4 Supplementary Figure 3: MS/MS analysis of single heterocycle containing PatE species derived from LynD mutants. MS/MS analysis of the single heterocycle containing PatE species resulting from incubation with LynD mutants A) K409E, B) K427E, C) R636A and D) R636E. In each case, the heterocycle is at the C-terminus as expected. The ion masses for each mutant are listed in Supplementary Table 3.
5 Supplementary Figure 4: Relative Rates of LynD and LynD K409A with 500 µm ATP. Relative rates of heterocyclization reaction between LynD + PatE under standard conditions (blue), LynD + PatE µm ATP (red) and LynDK409A + PatE µm ATP (green). A) Time taken to complete 1 st heterocycle. B) Time taken to form 2 nd heterocycle. Experiments were set up in triplicate and each measurement was repeated three times; thus each time point represents an average of nine measurements. Errors are plotted as ± 1 s.d..
6 Supplementary Figure 5: A) Production of AMP, PPi and Pi During Turnover. B) Incorporation 18 O from Selectively Labelled 18 O-PatE Substrate into PPi. A) 31 P NMR measuring ATP turnover: i) ATP only; ii) ATP + LynD; iii) ATP + LynD + PatE. In both the absence and presence of substrate AMP, PPi and Pi were observed. B) i) MS of pyrophosphate purified from heterocyclization reaction with 18 O containing peptide. 16 O and 18 O PPi (m/z = and respectively) are observed in roughly equal amounts. The peak at m/z = is a contaminant (formula C 6 H 10 O 4 P, the 12 C/ 13 C isotope pattern is observed) and not related to pyrophosphate. It is observed when unlabeled ( 16 O) PPi is employed. ii) Accurate MSMS fragmentation of pyrophosphate showing the typical fragmentation fingerprint: loss of water ( m/z)) and fragmentation into PO - 3 ( m/z). iii) Accurate MSMS fragmentation of pyrophosphate purified from the 18 O-PatE heterocyclization reaction. Loss of H 2 O and H 18 2 O (m/z = and respectively) and fragmentation into PO 18 2 O - ( m/z) indicates 18 O is incorporated in pyrophosphate during heterocyclization.
7 Supplementary Figure 6: ITC of Substrate Binding. ITC data obtained for the injection of PatE (and mutants) injected into LynD (and mutants) solutions. The top panel shows the raw data representing response to injections. The lower panel shows the integrated heats of injections ( ) and the best fit ( ) to the One-Site model (origin). Data for LynD R636A + ATP could not be fitted.
8 Supplementary Figure 7: Time Course Experiments for Heterocyclization Reactions Time course experiments monitoring the ratios of 0, 1 and 2 heterocycle containing species as analyzed by MALDI TOF MS for various heterocyclization reactions. A) LynD + PatE B) LynD + core peptide C) LynD + minimal leader + core peptide D) LynDfusion + core peptide and E) LynD + full leader + core peptide. Experiments were set up in triplicate and each measurement was repeated three times; thus each time point represents an average of nine measurements. Errors are plotted as ± 1 s.d..
9 Supplementary Figure 8: MALDI TOF MS of core peptide (ITACITFCAYDG) incubated for 24 h with A) LynD and B) LynDfusion. In the absence of leader sequence, LynD does not efficiently process the core peptide, even after prolonged incubation at 37 C, yielding mixed products with either 0, 1 or 2 heterocycles. By comparison, LynDfusion restores WT-like activity, producing predominantly a peptide species containing 2 heterocycles.
10 Supplementary Figure 9 A: MALDI TOF MS of N-terminally cleaved PatE (ITACITFCAYDGELE-H 6 ) incubated for 24 h in the presence of LynDfusion. The product of the heterocyclization reaction is predominantly a species with 2 heterocycles, indicating a presence of a C-terminal His 6 -tag does not significantly alter LynDfusion activity (ITACITFCAYDG (Figure 3B) Vs ITACITFCAYDGELE- H 6 ). This allows a variety of core-peptide-like test substrates to be prepared by the same method.
11 Supplementary Figure 9 B: MALDI TOF MS of N-terminally cleaved PatE 7mer (IACITFCAYDGELE-H 6 ) incubated for 16 h in (i) the absence of enzyme, (ii) the presence of wild type LynD and (iii) the presence of LynDfusion. Wild-type LynD results in a mix of 1 and 0 heterocycles, whilst LynDfusion yields mainly 2 heterocycles.
12 Supplementary Figure 9 C: MALDI TOF MS of N-terminally cleaved PatE 9mer (IITACITFCAYDGELE-H 6 ) incubated for 16 h in (i) the absence of enzyme, (ii) the presence of wild type LynD and (iii) the presence of LynDfusion. Wild-type LynD results in a mix of 2, 1 and 0 heterocycles, but predominantly 1, whilst LynDfusion predominantly processes 2 heterocycles.
13 Supplementary Figure 9 D: MALDI TOF MS of N-terminally cleaved PatE 3Cys (ICACITFCAYDGELE-H 6 ) incubated for 24 h in (i) the absence of enzyme, (ii) the presence of wild type LynD and (iii) the presence of LynDfusion. Wild-type LynD predominantly processes 1 heterocycle whilst LynDfusion processes a mixture of 1, 2 and 3 heterocycles. Supplementary Figure 9 E: MALDI TOF MS PatE (core peptide: ITACITFC) incubated for 16 h with LynDfusion. The fusion enzyme processes full length PatE to completion of 2 heterocycles.
14 Supplementary Tables Supplementary Table 1: PatE and LynD mutations and their effect on heterocyclization. LynD PatE MS (No. of heterocycles) W.T PatE 2 W.T PatE -L26R 2 W.T PatE -L29R 1 and 2 W.T PatE -E31R 1 and 2 W.T PatE -E32R 2 Y67D PatE 2 Y67D PatE -L29R 2 R74E PatE 2 R74E PatE -E31R 1 and 2 R399E PatE 2 R399E PatE -E32R 2 K409A PatE 2 K409E PatE 1 E423R PatE 0 R427E PatE 1 and 2 R636A PatE 0, 1 and 2 R636E PatE 0, 1 and 2 I644V PatE 2 F740D PatE 2
15 Supplementary Table 2: Data collection and refinement statistics (molecular replacement) LynD/ATP/PatEC51A LynD/AMP/PatE LynD/β,γ-imido-ATP/PatEC51A Data collection Space group P P P Cell dimensions a, b, c (Å) 81.8, 116.2, , 152.8, , 152.9, α, β, γ ( ) 90.00, 90.00, , 90.00, , 90.00, Resolution (Å) 2.14 ( ) * 2.86 ( ) 3.01 ( ) R sym or R merge 4.4 (56.9) 12.4 (89.7) 12.1 (83.0) I / σi 19.5 (2.2) 11.1 (2.0) 11.4 (2.1) Completeness (%) 98.8 (98.3) 97.5 (98.5) 99.8 (100.0) Redundancy 3.7 (3.7) 4.0 (4.0) 5.4 (5.8) Refinement Resolution (Å) No. reflections 95,581 42,149 37,339 R work / R free / / / No. atoms 12,653 11,955 12,008 Protein 12,008 11,930 11,940 Ligand/ion Water B-factors Protein Ligand/ion Water R.m.s. deviations Bond lengths (Å) Bond angles ( ) *1 crystal per structure. *Values in parentheses are for highest-resolution shell.
16 Supplementary Table 3: Masses of ions highlighted in Supplementary Figure 3. A) K409E 1 heterocycle 815.4m/z, B) R427E 1 heterocycle 815.4m/z, C) R636A 1 heterocycle 815.4m/z, D) R636E 1 heterocycle 815.4m/z. 3A) K409E 1 heterocycle 815.4m/z b ion b ion - 18 side chain loss y ion Internal fragment - LE Internal fragment AhetC I T A C I T F Chet A Y D G E L E Immonium ion Y 3B) R427E 1 heterocycle 815.4m/z b ion b ion - 18 side chain loss y ion Internal fragment - LE Internal fragment AhetC I T A C I T F Chet A Y D G E L E Immonium ion Y * *
17 3C) R636A 1 heterocycle 815.4m/z b ion b ion - 18 side chain loss y ion Internal fragment - LE Internal fragment AhetC I T A C I T F Chet A Y D G E L E Immonium ion Y 3D) R636E 1 heterocycle 815.4m/z b ion b ion - 18 side chain loss y ion Internal fragment - LE Internal fragment AhetC I T A C I T F Chet A Y D G E L E Immonium ion Y * *
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