Developmental and loco-like effects of a swainsonine-induced inhibition of a-mannosidase in the honey bee, Apis mellifera

Laura Wedd, Regan ASHBY, Sylvain Foret, Ryszard Maleszka

Research output: Contribution to journalArticle

1 Citation (Scopus)
4 Downloads (Pure)

Abstract

Background. Deficiencies in lysosomal a-mannosidase (LAM) activity in animals, caused either by mutations or by consuming toxic alkaloids, lead to severe phenotypic and behavioural consequences. Yet, epialleles adversely affecting LAM expression exist in the honey bee population suggesting that they might be beneficial in certain contexts and cannot be eliminated by natural selection. Methods. We have used a combination of enzymology, molecular biology and metabolomics to characterise the catalytic properties of honey bee LAM (AmLAM) and then used an indolizidine alkaloid swainsonine to inhibit its activity in vitro and in vivo. Results. We show that AmLAM is inhibited in vitro by swainsonine albeit at slightly higher concentrations than in other animals. Dietary exposure of growing larvae to swainsonine leads to pronounced metabolic changes affecting not only saccharides, but also amino acids, polyols and polyamines. Interestingly, the abundance of two fatty acids implicated in epigenetic regulation is significantly reduced in treated individuals. Additionally, swainsonie causes loco-like symptoms, increased mortality and a subtle decrease in the rate of larval growth resulting in a subsequent developmental delay in pupal metamorphosis. Discussion. We consider our findings in the context of cellular LAM function, larval development, environmental toxicity and colony-level impacts. The observed devel- opmental heterochrony in swainsonine-treated larvae with lower LAM activity offer a plausible explanation for the existence of epialleles with impaired LAM expression. Individuals carrying such epialleles provide an additional level of epigenetic diversity that could be beneficial for the functioning of a colony whereby more flexibility in timing of adult emergence might be useful for task allocation.
Original languageEnglish
Article number3109
Pages (from-to)1-22
Number of pages22
JournalPEERJ
Volume5
DOIs
Publication statusPublished - 2017

Fingerprint

Swainsonine
Mannosidases
mannosidases
swainsonine
Honey
Bees
Apis mellifera
honey bees
Alkaloids
Epigenomics
epigenetics
Larva
indolizidine alkaloids
Animals
Indolizidines
enzymology
Molecular biology
ecotoxicology
Metabolomics
polyols

Cite this

@article{3f02cc2632c9484d8c7c8467a86c11ce,
title = "Developmental and loco-like effects of a swainsonine-induced inhibition of a-mannosidase in the honey bee, Apis mellifera",
abstract = "Background. Deficiencies in lysosomal a-mannosidase (LAM) activity in animals, caused either by mutations or by consuming toxic alkaloids, lead to severe phenotypic and behavioural consequences. Yet, epialleles adversely affecting LAM expression exist in the honey bee population suggesting that they might be beneficial in certain contexts and cannot be eliminated by natural selection. Methods. We have used a combination of enzymology, molecular biology and metabolomics to characterise the catalytic properties of honey bee LAM (AmLAM) and then used an indolizidine alkaloid swainsonine to inhibit its activity in vitro and in vivo. Results. We show that AmLAM is inhibited in vitro by swainsonine albeit at slightly higher concentrations than in other animals. Dietary exposure of growing larvae to swainsonine leads to pronounced metabolic changes affecting not only saccharides, but also amino acids, polyols and polyamines. Interestingly, the abundance of two fatty acids implicated in epigenetic regulation is significantly reduced in treated individuals. Additionally, swainsonie causes loco-like symptoms, increased mortality and a subtle decrease in the rate of larval growth resulting in a subsequent developmental delay in pupal metamorphosis. Discussion. We consider our findings in the context of cellular LAM function, larval development, environmental toxicity and colony-level impacts. The observed devel- opmental heterochrony in swainsonine-treated larvae with lower LAM activity offer a plausible explanation for the existence of epialleles with impaired LAM expression. Individuals carrying such epialleles provide an additional level of epigenetic diversity that could be beneficial for the functioning of a colony whereby more flexibility in timing of adult emergence might be useful for task allocation.",
keywords = "Deleterious epialleles, Epigenetic variation, Mannosidosis, Metabolism, Toxic alkaloid",
author = "Laura Wedd and Regan ASHBY and Sylvain Foret and Ryszard Maleszka",
year = "2017",
doi = "10.7717/peerj.3109",
language = "English",
volume = "5",
pages = "1--22",
journal = "PEERJ",
issn = "2167-8359",
publisher = "PeerJ",

}

Developmental and loco-like effects of a swainsonine-induced inhibition of a-mannosidase in the honey bee, Apis mellifera. / Wedd, Laura; ASHBY, Regan; Foret, Sylvain; Maleszka, Ryszard.

In: PEERJ, Vol. 5, 3109, 2017, p. 1-22.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Developmental and loco-like effects of a swainsonine-induced inhibition of a-mannosidase in the honey bee, Apis mellifera

AU - Wedd, Laura

AU - ASHBY, Regan

AU - Foret, Sylvain

AU - Maleszka, Ryszard

PY - 2017

Y1 - 2017

N2 - Background. Deficiencies in lysosomal a-mannosidase (LAM) activity in animals, caused either by mutations or by consuming toxic alkaloids, lead to severe phenotypic and behavioural consequences. Yet, epialleles adversely affecting LAM expression exist in the honey bee population suggesting that they might be beneficial in certain contexts and cannot be eliminated by natural selection. Methods. We have used a combination of enzymology, molecular biology and metabolomics to characterise the catalytic properties of honey bee LAM (AmLAM) and then used an indolizidine alkaloid swainsonine to inhibit its activity in vitro and in vivo. Results. We show that AmLAM is inhibited in vitro by swainsonine albeit at slightly higher concentrations than in other animals. Dietary exposure of growing larvae to swainsonine leads to pronounced metabolic changes affecting not only saccharides, but also amino acids, polyols and polyamines. Interestingly, the abundance of two fatty acids implicated in epigenetic regulation is significantly reduced in treated individuals. Additionally, swainsonie causes loco-like symptoms, increased mortality and a subtle decrease in the rate of larval growth resulting in a subsequent developmental delay in pupal metamorphosis. Discussion. We consider our findings in the context of cellular LAM function, larval development, environmental toxicity and colony-level impacts. The observed devel- opmental heterochrony in swainsonine-treated larvae with lower LAM activity offer a plausible explanation for the existence of epialleles with impaired LAM expression. Individuals carrying such epialleles provide an additional level of epigenetic diversity that could be beneficial for the functioning of a colony whereby more flexibility in timing of adult emergence might be useful for task allocation.

AB - Background. Deficiencies in lysosomal a-mannosidase (LAM) activity in animals, caused either by mutations or by consuming toxic alkaloids, lead to severe phenotypic and behavioural consequences. Yet, epialleles adversely affecting LAM expression exist in the honey bee population suggesting that they might be beneficial in certain contexts and cannot be eliminated by natural selection. Methods. We have used a combination of enzymology, molecular biology and metabolomics to characterise the catalytic properties of honey bee LAM (AmLAM) and then used an indolizidine alkaloid swainsonine to inhibit its activity in vitro and in vivo. Results. We show that AmLAM is inhibited in vitro by swainsonine albeit at slightly higher concentrations than in other animals. Dietary exposure of growing larvae to swainsonine leads to pronounced metabolic changes affecting not only saccharides, but also amino acids, polyols and polyamines. Interestingly, the abundance of two fatty acids implicated in epigenetic regulation is significantly reduced in treated individuals. Additionally, swainsonie causes loco-like symptoms, increased mortality and a subtle decrease in the rate of larval growth resulting in a subsequent developmental delay in pupal metamorphosis. Discussion. We consider our findings in the context of cellular LAM function, larval development, environmental toxicity and colony-level impacts. The observed devel- opmental heterochrony in swainsonine-treated larvae with lower LAM activity offer a plausible explanation for the existence of epialleles with impaired LAM expression. Individuals carrying such epialleles provide an additional level of epigenetic diversity that could be beneficial for the functioning of a colony whereby more flexibility in timing of adult emergence might be useful for task allocation.

KW - Deleterious epialleles

KW - Epigenetic variation

KW - Mannosidosis

KW - Metabolism

KW - Toxic alkaloid

UR - http://www.scopus.com/inward/record.url?scp=85015202062&partnerID=8YFLogxK

UR - http://www.mendeley.com/research/developmental-locolike-effects-swainsonineinduced-inhibition-%CE%B1mannosidase-honey-bee-apis-mellifera

U2 - 10.7717/peerj.3109

DO - 10.7717/peerj.3109

M3 - Article

VL - 5

SP - 1

EP - 22

JO - PEERJ

JF - PEERJ

SN - 2167-8359

M1 - 3109

ER -