Secreted major Venus flytrap chitinase enables digestion of Arthropod prey

Paulina Paszota; Maria Escalante-Perez; Line R Thomsen; Michael Wulff Risør; Alicja Dembski; Laura  Sanglas; Tania A Nielsen; Henrik Karring; Ida B Thøgersen; Rainer Hedrich; Jan Johannes Enghild; Ines Kreuzer; Kristian W Sanggaard

doi:10.1016/j.bbapap.2013.11.009

Secreted major Venus flytrap chitinase enables digestion of Arthropod prey

Paulina Paszota, Maria Escalante-Perez, Line R Thomsen, Michael Wulff Risør, Alicja Dembski, Laura Sanglas, Tania A Nielsen, Henrik Karring, Ida B Thøgersen, Rainer Hedrich, Jan Johannes Enghild, Ines Kreuzer, Kristian W Sanggaard

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

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Abstract

Predation plays a major role in energy and nutrient flow in the biological food chain. Plant carnivory has attracted much interest since Darwin's time, but many fundamental properties of the carnivorous lifestyle are largely unexplored. In particular, the chain of events leading from prey perception to its digestive utilization remains to be elucidated. One of the first steps after the capture of animal prey, i.e. the enzymatic breakup of the insects' chitin-based shell, is reflected by considerable chitinase activity in the secreted digestive fluid in the carnivorous plant Venus flytrap. This study addresses the molecular nature, function, and regulation of the underlying enzyme, VF chitinase I. Using mass spectrometry based de novo sequencing, VF chitinase I was identified in the secreted fluid. As anticipated for one of the most prominent proteins in the flytrap's "green stomach" during prey digestion, transcription of VF chitinase I is restricted to glands and enhanced by secretion-inducing stimuli. In their natural habitat, Venus flytrap is exposed to high temperatures. We expressed and purified recombinant VF chitinase I and show that the enzyme exhibits the hallmark properties expected from an enzyme active in the hot and acidic digestive fluid of Dionaea muscipula. Structural modeling revealed a relative compact globular form of VF chitinase I, which might contribute to its overall stability and resistance to proteolysis. These peculiar characteristics could well serve industrial purposes, especially because of the ability to hydrolyze both soluble and crystalline chitin substrates including the commercially important cleavage of α-chitin.

Original language	English
Journal	BBA General Subjects
Volume	1844
Issue	2
Pages (from-to)	374–383
ISSN	0304-4165
DOIs	https://doi.org/10.1016/j.bbapap.2013.11.009
Publication status	Published - Feb 2014

Keywords

Carnivorous plants
Plant biology
Digestive enzymes
Chitin
Chitinases

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10.1016/j.bbapap.2013.11.009

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Paszota, P., Escalante-Perez, M., Thomsen, L. R., Risør, M. W., Dembski, A., Sanglas, L., Nielsen, T. A., Karring, H., Thøgersen, I. B., Hedrich, R., Enghild, J. J., Kreuzer, I., & Sanggaard, K. W. (2014). Secreted major Venus flytrap chitinase enables digestion of Arthropod prey. BBA General Subjects, 1844(2), 374–383. https://doi.org/10.1016/j.bbapap.2013.11.009

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title = "Secreted major Venus flytrap chitinase enables digestion of Arthropod prey",

abstract = "Predation plays a major role in energy and nutrient flow in the biological food chain. Plant carnivory has attracted much interest since Darwin's time, but many fundamental properties of the carnivorous lifestyle are largely unexplored. In particular, the chain of events leading from prey perception to its digestive utilization remains to be elucidated. One of the first steps after the capture of animal prey, i.e. the enzymatic breakup of the insects' chitin-based shell, is reflected by considerable chitinase activity in the secreted digestive fluid in the carnivorous plant Venus flytrap. This study addresses the molecular nature, function, and regulation of the underlying enzyme, VF chitinase I. Using mass spectrometry based de novo sequencing, VF chitinase I was identified in the secreted fluid. As anticipated for one of the most prominent proteins in the flytrap's {"}green stomach{"} during prey digestion, transcription of VF chitinase I is restricted to glands and enhanced by secretion-inducing stimuli. In their natural habitat, Venus flytrap is exposed to high temperatures. We expressed and purified recombinant VF chitinase I and show that the enzyme exhibits the hallmark properties expected from an enzyme active in the hot and acidic digestive fluid of Dionaea muscipula. Structural modeling revealed a relative compact globular form of VF chitinase I, which might contribute to its overall stability and resistance to proteolysis. These peculiar characteristics could well serve industrial purposes, especially because of the ability to hydrolyze both soluble and crystalline chitin substrates including the commercially important cleavage of α-chitin.",

keywords = "Carnivorous plants, Plant biology, Digestive enzymes, Chitin, Chitinases",

author = "Paulina Paszota and Maria Escalante-Perez and Thomsen, {Line R} and Ris{\o}r, {Michael Wulff} and Alicja Dembski and Laura Sanglas and Nielsen, {Tania A} and Henrik Karring and Th{\o}gersen, {Ida B} and Rainer Hedrich and Enghild, {Jan Johannes} and Ines Kreuzer and Sanggaard, {Kristian W}",

note = "Copyright {\textcopyright} 2013. Published by Elsevier B.V.",

year = "2014",

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doi = "10.1016/j.bbapap.2013.11.009",

language = "English",

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T1 - Secreted major Venus flytrap chitinase enables digestion of Arthropod prey

AU - Paszota, Paulina

AU - Escalante-Perez, Maria

AU - Thomsen, Line R

AU - Risør, Michael Wulff

AU - Dembski, Alicja

AU - Sanglas, Laura

AU - Nielsen, Tania A

AU - Karring, Henrik

AU - Thøgersen, Ida B

AU - Hedrich, Rainer

AU - Enghild, Jan Johannes

AU - Kreuzer, Ines

AU - Sanggaard, Kristian W

PY - 2014/2

Y1 - 2014/2

N2 - Predation plays a major role in energy and nutrient flow in the biological food chain. Plant carnivory has attracted much interest since Darwin's time, but many fundamental properties of the carnivorous lifestyle are largely unexplored. In particular, the chain of events leading from prey perception to its digestive utilization remains to be elucidated. One of the first steps after the capture of animal prey, i.e. the enzymatic breakup of the insects' chitin-based shell, is reflected by considerable chitinase activity in the secreted digestive fluid in the carnivorous plant Venus flytrap. This study addresses the molecular nature, function, and regulation of the underlying enzyme, VF chitinase I. Using mass spectrometry based de novo sequencing, VF chitinase I was identified in the secreted fluid. As anticipated for one of the most prominent proteins in the flytrap's "green stomach" during prey digestion, transcription of VF chitinase I is restricted to glands and enhanced by secretion-inducing stimuli. In their natural habitat, Venus flytrap is exposed to high temperatures. We expressed and purified recombinant VF chitinase I and show that the enzyme exhibits the hallmark properties expected from an enzyme active in the hot and acidic digestive fluid of Dionaea muscipula. Structural modeling revealed a relative compact globular form of VF chitinase I, which might contribute to its overall stability and resistance to proteolysis. These peculiar characteristics could well serve industrial purposes, especially because of the ability to hydrolyze both soluble and crystalline chitin substrates including the commercially important cleavage of α-chitin.

AB - Predation plays a major role in energy and nutrient flow in the biological food chain. Plant carnivory has attracted much interest since Darwin's time, but many fundamental properties of the carnivorous lifestyle are largely unexplored. In particular, the chain of events leading from prey perception to its digestive utilization remains to be elucidated. One of the first steps after the capture of animal prey, i.e. the enzymatic breakup of the insects' chitin-based shell, is reflected by considerable chitinase activity in the secreted digestive fluid in the carnivorous plant Venus flytrap. This study addresses the molecular nature, function, and regulation of the underlying enzyme, VF chitinase I. Using mass spectrometry based de novo sequencing, VF chitinase I was identified in the secreted fluid. As anticipated for one of the most prominent proteins in the flytrap's "green stomach" during prey digestion, transcription of VF chitinase I is restricted to glands and enhanced by secretion-inducing stimuli. In their natural habitat, Venus flytrap is exposed to high temperatures. We expressed and purified recombinant VF chitinase I and show that the enzyme exhibits the hallmark properties expected from an enzyme active in the hot and acidic digestive fluid of Dionaea muscipula. Structural modeling revealed a relative compact globular form of VF chitinase I, which might contribute to its overall stability and resistance to proteolysis. These peculiar characteristics could well serve industrial purposes, especially because of the ability to hydrolyze both soluble and crystalline chitin substrates including the commercially important cleavage of α-chitin.

KW - Carnivorous plants

KW - Plant biology

KW - Digestive enzymes

KW - Chitin

KW - Chitinases

U2 - 10.1016/j.bbapap.2013.11.009

DO - 10.1016/j.bbapap.2013.11.009

M3 - Journal article

C2 - 24275507

SN - 0304-4165

VL - 1844

SP - 374

EP - 383

JO - BBA General Subjects

JF - BBA General Subjects

IS - 2

ER -

Secreted major Venus flytrap chitinase enables digestion of Arthropod prey

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Keywords

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