CoChat
Sign Up
Cited by 28Enzyme Structure and FunctionInsect Resistance and GeneticsEntomopathogenic Microorganisms in Pest Control

The DOI matches its Crossref record; 6 of the 6 references it cites were found in a registry or an index.

De novo determination of mosquitocidal Cry11Aa and Cry11Ba structures from naturally-occurring nanocrystals

Open access
Tetreau, Guillaume, Sawaya, Michael R., De Zitter, Elke, Andreeva, Elena A., Banneville, Anne-Sophie, Schibrowsky, Natalie A., Coquelle, Nicolas, Brewster, Aaron S., Grünbein, Marie Luise, Kovacs, Gabriela Nass, Hunter, Mark S., Kloos, Marco, Sierra, Raymond G., Schiro, Giorgio, Qiao, Pei, Stricker, Myriam, Bideshi, Dennis, Young, Iris D., Zala, Ninon, Engilberge, Sylvain, Gorel, Alexander, Signor, Luca, Teulon, Jean-Marie, Hilpert, Mario, Foucar, Lutz, Bielecki, Johan, Bean, Richard, de Wijn, Raphael, Sato, Tokushi, Kirkwood, Henry, Letrun, Romain, Batyuk, Alexander, Snigireva, Irina, Fenel, Daphna, Schubert, Robin, Canfield, Ethan J., Alba, Mario M., Laporte, Frédéric, Després, Laurence, Bacia, Maria, Roux, Amandine, Chapelle, Christian, Riobé, François, Maury, Olivier, Ling, Wai Li, Boutet, Sébastien, Mancuso, Adrian, Gutsche, Irina, Girard, Eric, Barends, Thomas R. M., Pellequer, Jean-Luc, Park, Hyun-Woo, Laganowsky, Arthur D., Rodriguez, Jose, Burghammer, Manfred, Shoeman, Robert L., Doak, R. Bruce, Weik, Martin, Sauter, Nicholas K., Federici, Brian, Cascio, Duilio, Schlichting, Ilme, Colletier, Jacques-Philippe·2022·Nature Communications
DOI 10.1038/s41467-022-31746-xPMC PMC9334358

Published version of a preprint

Open this paper in CoChat — free accountOpen PDF

Abstract

Cry11Aa and Cry11Ba are the two most potent toxins produced by mosquitocidal Bacillus thuringiensis subsp. israelensis and jegathesan , respectively. The toxins naturally crystallize within the host; however, the crystals are too small for structure determination at synchrotron sources. Therefore, we applied serial femtosecond crystallography at X-ray free electron lasers to in vivo-grown nanocrystals of these toxins. The structure of Cry11Aa was determined de novo using the single-wavelength anomalous dispersion method, which in turn enabled the determination of the Cry11Ba structure by molecular replacement. The two structures reveal a new pattern for in vivo crystallization of Cry toxins, whereby each of their three domains packs with a symmetrically identical domain, and a cleavable crystal packing motif is located within the protoxin rather than at the termini. The diversity of in vivo crystallization patterns suggests explanations for their varied levels of toxicity and rational approaches to improve these toxins for mosquito control.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41467-022-31746-x

Cites

6 of 6 references verified0 citation errors · 0 not checkable

Statistics

Figures

Fig. 1 Phylogentic tree of delta-endotoxins. Tree plot showing structural relatedness of Cry11Aa and Cry11Ba to the family of 13 delta-endotoxins reported in the PDB. Structural similarity is represented on a phylogenetic tree plot. Shorter connecting lines signify closer structural similarity. Cry11Aa and Cry11Ba are structurally similar to each other, but distant from the other 13 delta-endotoxins. The closest structural homolog of Cry11Aa and Cry11Ba is Cry2Aa. The PDB ID codes are reported next to the toxin name. Species of origin are annotated in parentheses. Bta, Bti, Btj, Btk, Btm and Btt abbreviate insectidal Bacillus thuringiensis subspecies aizawai, israelensis, jegathesan, kurstaki, medellin and tenebrionis, respectively. Bt-YBT1518 is a strain displaying nematocidal activity.
Fig. 1 Phylogentic tree of delta-endotoxins. Tree plot showing structural relatedness of Cry11Aa and Cry11Ba to the family of 13 delta-endotoxins reported in the PDB. Structural similarity is represented on a phylogenetic tree plot. Shorter connecting lines signify closer structural similarity. Cry11Aa and Cry11Ba are structurally similar to each other, but distant from the other 13 delta-endotoxins. The closest structural homolog of Cry11Aa and Cry11Ba is Cry2Aa. The PDB ID codes are reported next to the toxin name. Species of origin are annotated in parentheses. Bta, Bti, Btj, Btk, Btm and Btt abbreviate insectidal Bacillus thuringiensis subspecies aizawai, israelensis, jegathesan, kurstaki, medellin and tenebrionis, respectively. Bt-YBT1518 is a strain displaying nematocidal activity.CC BY · PubMed Central
Fig. 2 Crystals and overall fold of Cry11 toxins. a, b, Scanning (left; SEM) and transmission (middle, right; TEM) electron micrographs of gold plated and negatively-stained Cry11Aa (a) and Cry11Ba (b) crystals, respectively. The right panels show a close-up view of the crystal surface. SEM and TEM experiments on Cry11Aa were repeated 7 and 2 times, respectively, while those on Cry11Ba were repeated 3 and 16 times, respectively. c Cry11Aa crystal structure, depicted as cartoon. Domain I is shown in light blue, except for central helix α5 which is shown in dark blue; domain II is shown in orange except for the αhβh-handle and βpin which are shown in purple and red, respectively; domain III is shown in pink. d Topology diagram of a Cry11Aa dimer with similar color code as in (c) and with labeling of secondary structure elements in one of the two monomers. The two monomers in a dimer assemble via the βpin, resulting in the formation of a large β-sheet. The short helices α9, α10 and α11, respectively located in the β11-β12, β15-β16 and β21-β22 loops, are not shown in the diagram.
Fig. 2 Crystals and overall fold of Cry11 toxins. a, b, Scanning (left; SEM) and transmission (middle, right; TEM) electron micrographs of gold plated and negatively-stained Cry11Aa (a) and Cry11Ba (b) crystals, respectively. The right panels show a close-up view of the crystal surface. SEM and TEM experiments on Cry11Aa were repeated 7 and 2 times, respectively, while those on Cry11Ba were repeated 3 and 16 times, respectively. c Cry11Aa crystal structure, depicted as cartoon. Domain I is shown in light blue, except for central helix α5 which is shown in dark blue; domain II is shown in orange except for the αhβh-handle and βpin which are shown in purple and red, respectively; domain III is shown in pink. d Topology diagram of a Cry11Aa dimer with similar color code as in (c) and with labeling of secondary structure elements in one of the two monomers. The two monomers in a dimer assemble via the βpin, resulting in the formation of a large β-sheet. The short helices α9, α10 and α11, respectively located in the β11-β12, β15-β16 and β21-β22 loops, are not shown in the diagram.CC BY · PubMed Central
Fig. 3 Monomer interactions in Cry11Aa and Cry11Ba. a Cry11Aa crystal packing, colored according to sequence (from blue to red) indicating the domain-based assembly; and colored according to tetramer assembly (see panel (b)). The highlighted areas indicate the regions shown in (b) (full line) and (c) (dashed line). b Cry11Aa tetramer with zoom on each of the three interfaces identified by PISA (interface #1, #3 and #6), with the involved residues depicted as spheres. Supplementary Fig. 5 shows the residues involved in hydrogen bonds and salt bridges. c Cry11Aa crystal assembly by interactions between neighboring tetramers, formed by interface #2, #4 and #5, visualized as in (b). d, Cry11Ba crystal packing, colored as in (a). e Cry11Ba tetramer with zoom on the interfaces as in (b). f Cry11Ba crystal assembly, visualized as in (c). As compared to Cry11Aa, Cry11Ba crystals contain an additional interface #7 between an A-B pair from two neighboring tetramers. g Interface statistics as identified by PISA for Cry11Aa (blue) and Cry11Ba (red).
Fig. 3 Monomer interactions in Cry11Aa and Cry11Ba. a Cry11Aa crystal packing, colored according to sequence (from blue to red) indicating the domain-based assembly; and colored according to tetramer assembly (see panel (b)). The highlighted areas indicate the regions shown in (b) (full line) and (c) (dashed line). b Cry11Aa tetramer with zoom on each of the three interfaces identified by PISA (interface #1, #3 and #6), with the involved residues depicted as spheres. Supplementary Fig. 5 shows the residues involved in hydrogen bonds and salt bridges. c Cry11Aa crystal assembly by interactions between neighboring tetramers, formed by interface #2, #4 and #5, visualized as in (b). d, Cry11Ba crystal packing, colored as in (a). e Cry11Ba tetramer with zoom on the interfaces as in (b). f Cry11Ba crystal assembly, visualized as in (c). As compared to Cry11Aa, Cry11Ba crystals contain an additional interface #7 between an A-B pair from two neighboring tetramers. g Interface statistics as identified by PISA for Cry11Aa (blue) and Cry11Ba (red).CC BY · PubMed Central
Fig. 4 Point-mutations of Cry11Aa affect the shape, size and pH-sensitivity of in vivo-grown nanocrystals. a Crystals from mutants exhibit similar sigmoidal patterns of crystal solubilization as a function of pH, except F17Y and E583Q that are more and less sensitive to pH, respectively (n = 3 independent measurements, data are presented as mean values ± SEM; Cry11Aa WT: black circles, F17Y: red crosses, Y272Q: brown squares, Y349F: purple triangles, Y449F: blue diamonds, D507N-D514N: orange plus symbols and E583Q: empty green circles). b Cry11Aa WT and mutants exhibit similar heat stability. As expected, toxins are more stable (+17.5 ± 0.3 °C) in their crystalline (diamonds) than soluble form (squares), irrespective of the mutation. The dashed lines are a guide to the eye. c Visualization of a representative crystal for Cry11Aa WT and mutants F17Y, Y272Q, Y349F, Y449F, D507N-D514N and E583Q by SEM (scale bar = 500 nm). d Crystals of F17Y (n = 93 crystals), Y449F (n = 60 crystals) and E583Q (n = 94 crystals) imaged by AFM were all smaller in length (L), width (W), thickness (T) and volume than WT (n = 45 crystals) highlighting a perturbation of the intrinsic crystal organization induced by these mutations. In each graph, the boxes represent the lower and upper quartiles around the median. The whiskers indicate the minimum and maximum values.
Fig. 4 Point-mutations of Cry11Aa affect the shape, size and pH-sensitivity of in vivo-grown nanocrystals. a Crystals from mutants exhibit similar sigmoidal patterns of crystal solubilization as a function of pH, except F17Y and E583Q that are more and less sensitive to pH, respectively (n = 3 independent measurements, data are presented as mean values ± SEM; Cry11Aa WT: black circles, F17Y: red crosses, Y272Q: brown squares, Y349F: purple triangles, Y449F: blue diamonds, D507N-D514N: orange plus symbols and E583Q: empty green circles). b Cry11Aa WT and mutants exhibit similar heat stability. As expected, toxins are more stable (+17.5 ± 0.3 °C) in their crystalline (diamonds) than soluble form (squares), irrespective of the mutation. The dashed lines are a guide to the eye. c Visualization of a representative crystal for Cry11Aa WT and mutants F17Y, Y272Q, Y349F, Y449F, D507N-D514N and E583Q by SEM (scale bar = 500 nm). d Crystals of F17Y (n = 93 crystals), Y449F (n = 60 crystals) and E583Q (n = 94 crystals) imaged by AFM were all smaller in length (L), width (W), thickness (T) and volume than WT (n = 45 crystals) highlighting a perturbation of the intrinsic crystal organization induced by these mutations. In each graph, the boxes represent the lower and upper quartiles around the median. The whiskers indicate the minimum and maximum values.CC BY · PubMed Central

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Research works printed but not linked: 97

  1. Vachon, V., Laprade, R. & Schwartz, J. L. Current models of the mode of action of Bacillus thuringiensis insecticidal crystal proteins: a critical review. J. Invertebr. Pathol. 111, 1–12 (2012). · DOI
  2. Delecluse, A., Rosso, M. L. & Ragni, A. Cloning and expression of a novel toxin gene from Bacillus thuringiensis subsp. jegathesan encoding a highly mosquitocidal protein. Appl. Env. Microbiol 61, 4230–4235 (1995). · DOI
  3. Federici, B. A., Park, H.-W. & Sakano, Y. Insecticidal Protein Crystals of Bacillus thuringiensis. in Inclusions in Prokaryotes (ed. Shively, J. M.) 195–236 (Springer, 2006). · DOI
  4. Boonserm, P., Mo, M., Angsuthanasombat, C. & Lescar, J. Structure of the functional form of the mosquito larvicidal Cry4Aa toxin from Bacillus thuringiensis at a 2.8-Angstrom resolution. J. Bacteriol. 188, 3391–3401 (2006). · DOI
  5. Boonserm, P., Davis, P., Ellar, D. J. & Li, J. Crystal structure of the mosquito-larvicidal toxin Cry4Ba and its biological implications. J. Mol. Biol. 348, 363–382 (2005). · DOI
  6. Cohen, S. et al. Cyt1Aa toxin: crystal structure reveals implications for its membrane-perforating function. J. Mol. Biol. 413, 804–814 (2011). · DOI
  7. Gutierrez, P., Alzate, O. & Orduz, S. A theoretical model of the tridimensional structure of Bacillus thuringiensis subsp. medellin Cry 11Bb toxin deduced by homology modelling. Mem. Inst. Oswaldo Cruz 96, 357–364 (2001). · DOI
  8. Chapman, H. N. et al. Femtosecond X-ray protein nanocrystallography. Nature 470, 73–77 (2011). · DOI
  9. Schlichting, I. Serial femtosecond crystallography: the first five years. IUCrJ 2, 246–255 (2015). · DOI
  10. Boutet, S., Fromme, P. & Hunter, M. S. X-ray Free Electron Lasers - A Revolution in Structural Biology. vol. 1 (Springer International Publishing, 2018). · DOI
  11. Tetreau, G. et al. Serial femtosecond crystallography on in vivo-grown crystals drives elucidation of mosquitocidal Cyt1Aa bioactivation cascade. Nat. Commun. 11, 1153 (2020). · DOI
  12. Li, J. D., Carroll, J. & Ellar, D. J. Crystal structure of insecticidal delta-endotoxin from Bacillus thuringiensis at 2.5 A resolution. Nature 353, 815–821 (1991). · DOI
  13. Morse, R. J., Yamamoto, T. & Stroud, R. M. Structure of Cry2Aa Suggests an Unexpected Receptor Binding Epitope. Structure 9, 409–417 (2001). · DOI
  14. Grochulski, P. et al. Bacillus thuringiensis CrylA(a) Insecticidal Toxin: Crystal Structure and Channel Formation. J. Mol. Biol. 254, 447–464 (1995). · DOI
  15. Engilberge, S. et al. Crystallophore: a versatile lanthanide complex for protein crystallography combining nucleating effects, phasing properties, and luminescence. Chem. Sci. 8, 5909–5917 (2017). · DOI
  16. Engilberge, S. et al. Protein crystal structure determination with the crystallophore, a nucleating and phasing agent. J. Appl. Crystallogr. 52, 722–731 (2019). · DOI
  17. Xu, C., Wang, B. C., Yu, Z. & Sun, M. Structural insights into Bacillus thuringiensis Cry, Cyt and parasporin toxins. Toxins 6, 2732–2770 (2014). · DOI
  18. Promponas, V. J. et al. CAST: an iterative algorithm for the complexity analysis of sequence tracts. Bioinformatics 16, 915–922 (2000). · DOI
  19. Wootton, J. C. & Federhen, S. Statistics of local complexity in amino acid sequences and sequence databases. Comput. Chem. 17, 149–163 (1993). · DOI
  20. Liang, M. et al. The Coherent X-ray Imaging instrument at the Linac Coherent Light Source. J. Synchrotron Radiat. 22, 514–519 (2015). · DOI
  21. Sierra, R. G. et al. Concentric-flow electrokinetic injector enables serial crystallography of ribosome and photosystem II. Nat. Methods 13, 59–62 (2016). · DOI
  22. DePonte, D. P. et al. Gas dynamic virtual nozzle for generation of microscopic droplet streams. J. Phys. -Appl. Phys. 41, 7 (2008). · DOI
  23. Leaver-Fay, A. et al. Rosetta3: An Object-Oriented Software Suite for the Simulation and Design of Macromolecules. Methods Enzymol. 487, 545–574 (2011). · DOI
  24. Bairoch, A. & Apweiler, R. The SWISS-PROT protein sequence data bank and its supplement TrEMBL in 1999. Nucleic Acids Res. 27, 49–54 (1999). · DOI
  25. Pardo-Lopez, L., Soberon, M. & Bravo, A. Bacillus thuringiensis insecticidal three-domain Cry toxins: mode of action, insect resistance and consequences for crop protection. FEMS Microbiol. Rev. 37, 3–22 (2013). · DOI
  26. Krissinel, E. & Henrick, K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774–797 (2007). · DOI
  27. Colletier, J.-P. et al. De novo phasing with X-ray laser reveals mosquito larvicide BinAB structure. Nature 539, 43–47 (2016). · DOI
  28. Oestergaard, J., Ehlers, R. U., Martinez-Ramirez, A. C. & Real, M. D. Binding of Cyt1Aa and Cry11Aa toxins of Bacillus thuringiensis serovar israelensis to brush border membrane vesicles of Tipula paludosa (Diptera: Nematocera) and subsequent pore formation. Appl. Environ. Microbiol. 73, 3623–3629 (2007). · DOI
  29. Yamagiwa, M., Sakagawa, K. & Sakai, H. Functional Analysis of Two Processed Fragments of Bacillus thuringiensis Cry11A Toxin. Biosci. Biotechnol. Biochem. 68, 523–528 (2014). · DOI
  30. Munoz-Garay, C. et al. Oligomerization of Cry11Aa from Bacillus thuringiensis Has an Important Role in Toxicity against Aedes aegypti. Appl. Environ. Microbiol. 75, 7548–7550 (2009). · DOI
  31. Fernandez, L. E. et al. Cry11Aa toxin from Bacillus thuringiensis binds its receptor in Aedes aegypti mosquito larvae through loop alpha-8 of domain II. Febs Lett. 579, 3508–3514 (2005). · DOI
  32. Carmona, D. et al. Dominant Negative Phenotype of Bacillus thuringiensis Cry1Ab, Cry11Aa and Cry4Ba Mutants Suggest Hetero-Oligomer Formation among Different Cry Toxins. PLoS ONE 6, e19952 (2011). · DOI
  33. Du, J. P., Knowles, B. H., Li, J. & Ellar, D. J. Biochemical characterization of Bacillus thuringiensis cytolytic toxins in association with a phospholipid bilayer. Biochem. J. 338, 185–193 (1999). · DOI
  34. Ntountoumi, C. et al. Low complexity regions in the proteins of prokaryotes perform important functional roles and are highly conserved. Nucleic Acids Res. 47, 9998–10009 (2019). · DOI
  35. Lanzarotti, E., Defelipe, L. A., Marti, M. A. & Turjanski, A. G. Aromatic clusters in protein–protein and protein–drug complexes. J. Cheminformatics 12, 30 (2020). · DOI
  36. Wiedorn, M. O. et al. Megahertz serial crystallography. Nat. Commun. 9, 4025 (2018). · DOI
  37. Grünbein, M. L. et al. Megahertz data collection from protein microcrystals at an X-ray free-electron laser. Nat. Commun. 9, 3487 (2018). · DOI
  38. Henrich, B. et al. The adaptive gain integrating pixel detector AGIPD a detector for the European XFEL. Nucl. Instrum. Methods Phys. Res. Sect. Accel. Spectrometers Detect. Assoc. Equip. 633, S11–S14 (2011). · DOI
  39. Likitvivatanavong, S. et al. Multiple Receptors as Targets of Cry Toxins in Mosquitoes. J. Agric. Food Chem. 59, 2829–2838 (2011). · DOI
  40. Fernandez, L. E., Aimanova, K. G., Gill, S. S., Bravo, A. & Soberon, M. A GPI-anchored alkaline phosphatase is a functional midgut receptor of Cry11Aa toxin in Aedes aegypti larvae. Biochem. J. 394, 77–84 (2006). · DOI
  41. Lopez-Diaz, J. A., Emiliano Canton, P., Gill, S. S., Soberon, M. & Bravo, A. Oligomerization is a key step in Cyt1Aa membrane insertion and toxicity but not necessary to synergize Cry11Aa toxicity in Aedes aegypti larvae. Environ. Microbiol. 15, 3030–3039 (2013). · DOI
  42. Pérez, C. et al. Bacillus thuringiensis subsp. israelensis Cyt1Aa synergizes Cry11Aa toxin by functioning as a membrane-bound receptor. Proc. Natl. Acad. Sci. USA 102, 18303–18308 (2005). · DOI
  43. Sawaya, M. R. et al. Protein crystal structure obtained at 2.9 Å resolution from injecting bacterial cells into an X-ray free-electron laser beam. Proc. Natl. Acad. Sci. 111, 12769–12774 (2014). · DOI
  44. Galitsky, N. et al. Structure of the insecticidal bacterial delta-endotoxin Cry3Bb1 of Bacillus thuringiensis. Acta Crystallogr. D. Biol. Crystallogr. 57, 1101–1109 (2001). · DOI
  45. Adalat, R., Saleem, F., Crickmore, N., Naz, S. & Shakoori, A. R. In vivo crystallization of three-domain Cry Toxins. Toxins Basel 9, (2017). · DOI
  46. Hughes, M. P. et al. Atomic structures of low-complexity protein segments reveal kinked β sheets that assemble networks. Science 359, 698–701 (2018). · DOI
  47. Salinas, N., Colletier, J. P., Moshe, A. & Landau, M. Extreme amyloid polymorphism in Staphylococcus aureus virulent PSMα peptides. Nat. Commun. 9, 3512 (2018). · DOI
  48. Sun, Y. et al. Construction and characterization of the interdomain chimeras using Cry11Aa and Cry11Ba from Bacillus thuringiensis and identification of a possible novel toxic chimera. Biotechnol. Lett. 36, 105–111 (2013). · DOI
  49. Fernandez, L. E. et al. Cry11Aa toxin from Bacillus thuringiensis binds its receptor in Aedes aegypti mosquito larvae through loop alpha-8 of domain II. Febs Lett. 579, 3508–3514 (2005). · DOI
  50. Perez, C. et al. Bacillus thuringiensis subsp israelensis Cyt1Aa synergizes Cry11Aa toxin by functioning as a membrane-bound receptor. Proc. Natl. Acad. Sci. USA 102, 18303–18308 (2005). · DOI
  51. Perez, C. et al. Bacillus thuringiensis ssp israelensis Cyt1Aa enhances activity of Cry11Aa toxin by facilitating the formation of a pre-pore oligomeric structure. Cell. Microbiol. 9, 2931–2937 (2007). · DOI
  52. Carmona, D. et al. Dominant negative phenotype of bacillus thuringiensis Cry1Ab, Cry11Aa and Cry4Ba mutants suggest hetero-oligomer formation among different cry toxins. PLoS ONE 6, e19952 (2011). · DOI
  53. Likitvivatanavong, S., Aimanova, K. G. & Gill, S. S. Loop residues of the receptor binding domain of Bacillus thuringiensis Cry11Ba toxin are important for mosquitocidal activity. FEBS Lett. 583, 2021–2030 (2009). · DOI
  54. Gevorkov, Y. et al. XGANDALF - extended gradient descent algorithm for lattice finding. Acta Crystallogr. Sect. Found. Adv. 75, 694–704 (2019). · DOI
  55. White, T. A. Processing serial crystallography data with CrystFEL: a step-by-step guide. Acta Crystallogr. Sect. Struct. Biol. 75, 219–233 (2019). · DOI
  56. Cowtan, K. Completion of autobuilt protein models using a database of protein fragments. Acta Crystallogr. D. Biol. Crystallogr. 68, 328–335 (2012). · DOI
  57. Murshudov, G. N. et al. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D. Biol. Crystallogr. 67, 355–367 (2011). · DOI
  58. Banneville, A.-S. et al. Structural and functional characterization of DdrC, a novel DNA damage-induced nucleoid associated protein involved in DNA compaction, Nucleic Acids Res. (2022) https://doi.org/10.1093/nar/gkac563. · DOI
  59. Park, H. W., Delecluse, A. & Federici, B. A. Construction and characterization of a recombinant Bacillus thuringiensis subsp israelensis strain that produces Cry11B. J. Invertebr. Pathol. 78, 37–44 (2001). · DOI
  60. Wu, D. & Federici, B. A. Improved production of the insecticidal CryIVD protein in Bacillus-thuringiensis using CryLA(c) promoters to express the gene for an associated 20-KDa protein. Appl. Microbiol. Biotechnol. 42, 697–702 (1995). · DOI
  61. Kirmitzoglou, I. & Promponas, V. J. LCR-eXXXplorer: a web platform to search, visualize and share data for low complexity regions in protein sequences. Bioinformatics 31, 2208–2210 (2015). · DOI
  62. Girish, V. & Vijayalakshmi, A. Affordable image analysis using NIH Image/ImageJ. Indian J. Cancer 41, 47 (2004). · DOI
  63. Sakano, Y., Park, H. W., Bideshi, D. K., Ge, B. & Federici, B. A. Contributions of 5’-UTR and 3’-UTR cis elements to Cyt1Aa synthesis in Bacillus thuringiensis subsp. israelensis. J. Invertebr. Pathol. 149, 66–75 (2017). · DOI
  64. Lereclus, D., Arantès, O., Chaufaux, J. & Lecadet, M. Transformation and expression of a cloned delta-endotoxin gene in Bacillus thuringiensis. FEMS Microbiol Lett. 51, 211–217 (1989).
  65. Nečas, D. & Klapetek, P. Gwyddion: an open-source software for SPM data analysis. Cent. Eur. J. Phys. 10, 181–188 (2012).
  66. Chen, S. W. & Pellequer, J.-L. DeStripe: frequency-based algorithm for removing stripe noises from AFM images. BMC Struct. Biol. 11, 7 (2011). · DOI
  67. Waterman, D. G. et al. Diffraction-geometry refinement in the DIALS framework. Acta Crystallogr. Sect. Struct. Biol. 72, 558–575 (2016). · DOI
  68. Sauter, N. K., Hattne, J., Grosse-Kunstleve, R. W. & Echols, N. New Python-based methods for data processing. Acta Crystallogr. D. Biol. Crystallogr. 69, 1274–1282 (2013). · DOI
  69. Hattne, J. et al. Accurate macromolecular structures using minimal measurements from X-ray free-electron lasers. Nat. Methods 11, 545–548 (2014). · DOI
  70. Winter, G. et al. DIALS: implementation and evaluation of a new integration package. Acta Crystallogr. Sect. Struct. Biol. 74, 85–97 (2018). · DOI
  71. Vagin, A. & Teplyakov, A. MOLREP: an Automated Program for Molecular Replacement. J. Appl. Crystallogr. 30, 1022–1025 (1997). · DOI
  72. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658–674 (2007). · DOI · Paper page
  73. Coquelle, N. et al. Raster-scanning serial protein crystallography using micro- and nano-focused synchrotron beams. Acta Crystallogr. D. Biol. Crystallogr. 71, 1184–1196 (2015). · DOI
  74. Foucar, L. et al. CASS—CFEL-ASG software suite. Comput. Phys. Commun. 183, 2207–2213 (2012). · DOI
  75. Skubák, P. & Pannu, N. S. Automatic protein structure solution from weak X-ray data. Nat. Commun. 4, 1–6 (2013). · DOI
  76. Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D. Biol. Crystallogr. 67, 235–242 (2011). · DOI · Paper page
  77. Duisenberg, A. J. M. Indexing in single-crystal diffractometry with an obstinate list of reflections. J. Appl. Crystallogr. 25, 92–96 (1992). · DOI
  78. Ginn, H. M. et al. ıt TakeTwo: an indexing algorithm suited to still images with known crystal parameters. Acta Crystallogr. Sect. D. 72, 956–965 (2016). · DOI
  79. Leslie, A. G. W. The integration of macromolecular diffraction data. Acta Crystallogr. D. Biol. Crystallogr. 62, 48–57 (2006). · DOI
  80. Krissinel, E., Uski, V., Lebedev, A., Winn, M. & Ballard, C. Distributed computing for macromolecular crystallography. Acta Crystallogr. Sect. Struct. Biol. 74, 143–151 (2018). · DOI
  81. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr Biol. Crystallogr 60, 2126–2132 (2004). · DOI · Paper page
  82. Afonine, P. V. et al. Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr. D. Biol. Crystallogr. 68, 352–367 (2012). · DOI · Paper page
  83. Uervirojnangkoorn, M. et al. Enabling X-ray free electron laser crystallography for challenging biological systems from a limited number of crystals. eLife 4, e05421 (2015). · DOI
  84. Blanc, E. et al. Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr. D. Biol. Crystallogr. 60, 2210–2221 (2004). · DOI
  85. Bond, C. S. & Schüttelkopf, A. W. ALINE: a WYSIWYG protein-sequence alignment editor for publication-quality alignments. Acta Crystallogr Biol. Crystallogr 65, 510–512 (2009). · DOI
  86. Madeira, F. et al. The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res. 47, W636–W641 (2019). · DOI · Paper page
  87. Krissinel, E. & Henrick, K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr Biol. Crystallogr 60, 2256–2268 (2004). · DOI
  88. Gille, C. & Frömmel, C. STRAP: editor for STRuctural Alignments of Proteins. Bioinformatics 17, 377–378 (2001). · DOI
  89. Gille, C., Fähling, M., Weyand, B., Wieland, T. & Gille, A. Alignment-Annotator web server: rendering and annotating sequence alignments. Nucleic Acids Res. 42, W3–W6 (2014). · DOI
  90. Boc, A., Diallo, A. B. & Makarenkov, V. T-REX: a web server for inferring, validating and visualizing phylogenetic trees and networks. Nucleic Acids Res. 40, W573–W579 (2012). · DOI
  91. Mirdita, M., Steinegger, M., Breitwieser, F., Söding, J. & Levy Karin, E. Fast and sensitive taxonomic assignment to metagenomic contigs. Bioinformatics 37, 3029–3031 (2021). · DOI
  92. Steinegger, M. & Söding, J. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat. Biotechnol. 35, 1026–1028 (2017). · DOI · Paper page
  93. Prakash, A., Jeffryes, M., Bateman, A. & Finn, R. D. The HMMER Web Server for Protein Sequence Similarity Search. Curr. Protoc. Bioinforma. 60, 3.15.1–3.15.23 (2017). · DOI
  94. Savi, M. K., Mangamana, E. T., Deguenon, J. M., Hounmenou, C. G. & Kakaï, R. G. Determination of Lethal Concentrations Using an R Software Function Integrating the Abbott Correction. J. Agric. Sci. Technol. A 7, 25–30 (2017). · DOI
  95. Wheeler, M. W., Park, R. M. & Bailer, A. J. Comparing median lethal concentration values using confidence interval overlap or ratio tests. Env. Toxicol. Chem. 25, 1441–1444 (2006). · DOI
  96. Rosenfeld, J., Capdevielle, J., Guillemot, J. C. & Ferrara, P. In-gel digestion of proteins for internal sequence analysis after one- or two-dimensional gel electrophoresis. Anal. Biochem. 203, 173–179 (1992). · DOI
  97. Laganowsky, A., Reading, E., Hopper, J. T. S. & Robinson, C. V. Mass spectrometry of intact membrane protein complexes. Nat. Protoc. 8, 639–651 (2013). · DOI · Paper page

Metadata

Authors
Tetreau, G., Sawaya, M. R., De Zitter, E., Andreeva, E. A., Banneville, A.-S., Schibrowsky, N. A., Coquelle, N., Brewster, A. S., Grünbein, M. L., Kovacs, G. N., Hunter, M. S., Kloos, M., Sierra, R. G., Schiro, G., Qiao, P., Stricker, M., Bideshi, D., Young, I. D., Zala, N., Engilberge, S., Gorel, A., Signor, L., Teulon, J.-M., Hilpert, M., Foucar, L., Bielecki, J., Bean, R., de Wijn, R., Sato, T., Kirkwood, H., Letrun, R., Batyuk, A., Snigireva, I., Fenel, D., Schubert, R., Canfield, E. J., Alba, M. M., Laporte, F., Després, L., Bacia, M., Roux, A., Chapelle, C., Riobé, F., Maury, O., Ling, W. L., Boutet, S., Mancuso, A., Gutsche, I., Girard, E., Barends, T. R. M., Pellequer, J.-L., Park, H.-W., Laganowsky, A. D., Rodriguez, J., Burghammer, M., Shoeman, R. L., Doak, R. B., Weik, M., Sauter, N. K., Federici, B., Cascio, D., Schlichting, I., & Colletier, J.-P.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • University of California, Los Angeles (US)
  • Institut Laue-Langevin (FR)
  • Lawrence Berkeley National Laboratory (US)
  • Max Planck Institute for Medical Research (DE)
  • SLAC National Accelerator Laboratory (US)
  • Texas A&M University (US)
  • University of California, Riverside (US)
  • European X-Ray Free-Electron Laser (DE)
  • European Synchrotron Radiation Facility (FR)
  • University of Southern California (US)
  • Lyon 1 Université (FR)
Corresponding author
Colletier, Jacques-Philippe
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2022-07-28
Volume
13
Issue
1
Pages
4376-4376
ISSN
2041-1723 (ISSN-L)
DOI
10.1038/s41467-022-31746-x
PMC
PMC9334358
OpenAlex
W4288096555
Cited by
28
References
6
Citations by year
2026: 4 · 2025: 6 · 2024: 8 · 2023: 9 · 2022: 1
FWCI
1.69
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Communications (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
  • HAL (submittedVersion, other-oa)
  • HAL (submittedVersion, cc-by-nc)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion)
  • European XFEL (submittedVersion)
Funders
  • U.S. Department of Health & Human Services | National Institutes of Health (GM117126, P41RR001209, P41GM103393)
  • DOE | Office of Science (DE-AC02-76SF00515)
  • Centre National de la Recherche Scientifique (PEPS SASLELX)
  • U.S. Department of Health & Human Services | Centers for Disease Control and Prevention (1U01CK000516)
  • Agence Nationale de la Recherche (ANR-2018-CE11-0005-02, ANR-10-INBS-05-02, ANR-17-EURE-0003, NR-17-CE11-0018-01)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Enzyme Structure and Function
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Insect Resistance and Genetics
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Entomopathogenic Microorganisms in Pest Control
Keywords
Cry11Aa, mosquitocidal toxin, Bacillus thuringiensis var. israelensis, nanocrystals, serial femtosecond crystallography, de novo structure determination, single-wavelength anomalous dispersion, protoxin, mosquito control, toxin toxicity
MeSH terms
Animals, Bacillus thuringiensis, Bacterial Proteins, Endotoxins, Hemolysin Proteins, Larva, Mosquito Control, Nanoparticles

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review