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Title: The pesticidal Cry6Aa toxin from Bacillus thuringiensis is structurally similar to HlyE-family alpha pore-forming toxins

Abstract

Background: The Cry6 family of proteins from Bacillus thuringiensis represents a group of powerful toxins with great potential for use in the control of coleopteran insects and of nematode parasites of importance to agriculture. These proteins are unrelated to other insecticidal toxins at the level of their primary sequences and the structure and function of these proteins has been poorly studied to date. This has inhibited our understanding of these toxins and their mode of action, along with our ability to manipulate the proteins to alter their activity to our advantage. To increase our understanding of their mode of action and to facilitate further development of these proteins we have determined the structure of Cry6Aa in protoxin and trypsin-activated forms and demonstrated a pore-forming mechanism of action. Results: The two forms of the toxin were resolved to 2.7 Å and 2.0 Å respectively and showed very similar structures. We report Cry6Aa shows structural homology to a known class of pore-forming toxins including hemolysin E from Escherichia coli and two Bacillus cereus proteins: the hemolytic toxin HblB and the NheA component of the non-hemolytic toxin (pfam05791). Cry6Aa also shows atypical features compared to other members of this family, including internal repeatmore » sequences and small loop regions within major alpha helices. Trypsin processing was found to result in the loss of some internal sequences while the C-terminal region remains disulfide-linked to the main core of the toxin. Based on the structural similarity of Cry6Aa to other toxins, the mechanism of action of the toxin was probed and its ability to form pores in vivo in Caenorhabditis elegans was demonstrated. A non-toxic mutant was also produced, consistent with the proposed pore-forming mode of action. Conclusions: Cry6 proteins are members of the alpha helical pore-forming toxins – a structural class not previously recognized among the Cry toxins of B. thuringiensis and representing a new paradigm for nematocidal and insecticidal proteins. Elucidation of both the structure and the pore-forming mechanism of action of Cry6Aa now opens the way to more detailed analysis of toxin specificity and the development of new toxin variants with novel activities.« less

Authors:
 [1];  [2];  [3];  [4];  [4];  [4];  [3];  [2];  [4];  [4];  [4];  [4];  [5];  [6];  [6];  [2];  [2];  [3];  [4]; ORCiD logo [2]
+ Show Author Affiliations
  1. Shamrock Structures LLC, Woodridge, IL (United States)
  2. Cardiff Univ. (United Kingdom)
  3. Univ. of Massachusetts Medical School, Worcester, MA (United States)
  4. Dow AgroSciences, LLC, Indianapolis, IN (United States)
  5. 6125 Londonberrie Ct., Midland, MI (United States)
  6. The Chinese Univ. of Hong Kong, Shatin (China)
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Org.:
National Institutes of Health (NIH). National Institute of General Medical Sciences and National Institute of Allergy and Infectious Diseases
OSTI Identifier:
1438863
Grant/Contract Number:  
R01GM071603; R01AI056189
Resource Type:
Accepted Manuscript
Journal Name:
BMC Biology
Additional Journal Information:
Journal Volume: 14; Journal Issue: 1; Journal ID: ISSN 1741-7007
Publisher:
BioMed Central
Country of Publication:
United States
Language:
ENGLISH
Subject:
59 BASIC BIOLOGICAL SCIENCES; Bacillus thuringiensis; Cry6; Insecticidal toxin; Hemolysin

Citation Formats

Dementiev, Alexey, Board, Jason, Sitaram, Anand, Hey, Timothy, Kelker, Matthew S., Xu, Xiaoping, Hu, Yan, Vidal-Quist, Cristian, Chikwana, Vimbai, Griffin, Samantha, McCaskill, David, Wang, Nick X., Hung, Shao-Ching, Chan, Michael K., Lee, Marianne M., Hughes, Jessica, Wegener, Alice, Aroian, Raffi V., Narva, Kenneth E., and Berry, Colin. The pesticidal Cry6Aa toxin from Bacillus thuringiensis is structurally similar to HlyE-family alpha pore-forming toxins. United States: N. p., 2016. Web. doi:10.1186/s12915-016-0295-9.
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Dementiev, Alexey, Board, Jason, Sitaram, Anand, Hey, Timothy, Kelker, Matthew S., Xu, Xiaoping, Hu, Yan, Vidal-Quist, Cristian, Chikwana, Vimbai, Griffin, Samantha, McCaskill, David, Wang, Nick X., Hung, Shao-Ching, Chan, Michael K., Lee, Marianne M., Hughes, Jessica, Wegener, Alice, Aroian, Raffi V., Narva, Kenneth E., & Berry, Colin. The pesticidal Cry6Aa toxin from Bacillus thuringiensis is structurally similar to HlyE-family alpha pore-forming toxins. United States. https://doi.org/10.1186/s12915-016-0295-9
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Dementiev, Alexey, Board, Jason, Sitaram, Anand, Hey, Timothy, Kelker, Matthew S., Xu, Xiaoping, Hu, Yan, Vidal-Quist, Cristian, Chikwana, Vimbai, Griffin, Samantha, McCaskill, David, Wang, Nick X., Hung, Shao-Ching, Chan, Michael K., Lee, Marianne M., Hughes, Jessica, Wegener, Alice, Aroian, Raffi V., Narva, Kenneth E., and Berry, Colin. Tue . "The pesticidal Cry6Aa toxin from Bacillus thuringiensis is structurally similar to HlyE-family alpha pore-forming toxins". United States. https://doi.org/10.1186/s12915-016-0295-9. https://www.osti.gov/servlets/purl/1438863.
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@article{osti_1438863,
title = {The pesticidal Cry6Aa toxin from Bacillus thuringiensis is structurally similar to HlyE-family alpha pore-forming toxins},
author = {Dementiev, Alexey and Board, Jason and Sitaram, Anand and Hey, Timothy and Kelker, Matthew S. and Xu, Xiaoping and Hu, Yan and Vidal-Quist, Cristian and Chikwana, Vimbai and Griffin, Samantha and McCaskill, David and Wang, Nick X. and Hung, Shao-Ching and Chan, Michael K. and Lee, Marianne M. and Hughes, Jessica and Wegener, Alice and Aroian, Raffi V. and Narva, Kenneth E. and Berry, Colin},
abstractNote = {Background: The Cry6 family of proteins from Bacillus thuringiensis represents a group of powerful toxins with great potential for use in the control of coleopteran insects and of nematode parasites of importance to agriculture. These proteins are unrelated to other insecticidal toxins at the level of their primary sequences and the structure and function of these proteins has been poorly studied to date. This has inhibited our understanding of these toxins and their mode of action, along with our ability to manipulate the proteins to alter their activity to our advantage. To increase our understanding of their mode of action and to facilitate further development of these proteins we have determined the structure of Cry6Aa in protoxin and trypsin-activated forms and demonstrated a pore-forming mechanism of action. Results: The two forms of the toxin were resolved to 2.7 Å and 2.0 Å respectively and showed very similar structures. We report Cry6Aa shows structural homology to a known class of pore-forming toxins including hemolysin E from Escherichia coli and two Bacillus cereus proteins: the hemolytic toxin HblB and the NheA component of the non-hemolytic toxin (pfam05791). Cry6Aa also shows atypical features compared to other members of this family, including internal repeat sequences and small loop regions within major alpha helices. Trypsin processing was found to result in the loss of some internal sequences while the C-terminal region remains disulfide-linked to the main core of the toxin. Based on the structural similarity of Cry6Aa to other toxins, the mechanism of action of the toxin was probed and its ability to form pores in vivo in Caenorhabditis elegans was demonstrated. A non-toxic mutant was also produced, consistent with the proposed pore-forming mode of action. Conclusions: Cry6 proteins are members of the alpha helical pore-forming toxins – a structural class not previously recognized among the Cry toxins of B. thuringiensis and representing a new paradigm for nematocidal and insecticidal proteins. Elucidation of both the structure and the pore-forming mechanism of action of Cry6Aa now opens the way to more detailed analysis of toxin specificity and the development of new toxin variants with novel activities.},
doi = {10.1186/s12915-016-0295-9},
journal = {BMC Biology},
number = 1,
volume = 14,
place = {United States},
year = {Tue Aug 30 00:00:00 EDT 2016},
month = {Tue Aug 30 00:00:00 EDT 2016}
}
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https://doi.org/10.1186/s12915-016-0295-9
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Resistance to root-knot nematode in tomato roots expressing a nematicidal Bacillus thuringiensis crystal protein
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text, January 2015

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Structure of the NheA Component of the Nhe Toxin from Bacillus cereus: Implications for Function
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Lysinibacillus sphaericus binary toxin induces apoptosis in susceptible Culex quinquefasciatus larvae
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  • Journal of Invertebrate Pathology, Vol. 128
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THE GENETICS OF CAENORHABDITIS ELEGANS
journal, May 1974

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