Potential acetylcholine-based communication in honeybee haemocytes and its modulation by a neonicotinoid insecticide

PeerJ. 2024 Sep 13:12:e17978. doi: 10.7717/peerj.17978. eCollection 2024.

Abstract

There is growing concern that some managed and wild insect pollinator populations are in decline, potentially threatening biodiversity and sustainable food production on a global scale. In recent years, there has been increasing evidence that sub-lethal exposure to neurotoxic, neonicotinoid pesticides can negatively affect pollinator immunocompetence and could amplify the effects of diseases, likely contributing to pollinator declines. However, a direct pathway connecting neonicotinoids and immune functions remains elusive. In this study we show that haemocytes and non-neural tissues of the honeybee Apis mellifera express the building blocks of the nicotinic acetylcholine receptors that are the target of neonicotinoids. In addition, we demonstrate that the haemocytes, which form the cellular arm of the innate immune system, actively express choline acetyltransferase, a key enzyme necessary to synthesize acetylcholine. In a last step, we show that the expression of this key enzyme is affected by field-realistic doses of clothianidin, a widely used neonicotinoid. These results support a potential mechanistic framework to explain the effects of sub-lethal doses of neonicotinoids on the immune function of pollinators.

Keywords: Bee health; Clothianidin; Haemocytes; Immune regulation; Immunosuppression; Innate immune system; Neonicotinoid; Pesticide.

MeSH terms

  • Acetylcholine* / metabolism
  • Animals
  • Bees / drug effects
  • Bees / immunology
  • Choline O-Acetyltransferase / metabolism
  • Guanidines* / toxicity
  • Hemocytes* / drug effects
  • Hemocytes* / immunology
  • Hemocytes* / metabolism
  • Insecticides* / toxicity
  • Neonicotinoids* / toxicity
  • Receptors, Nicotinic / drug effects
  • Receptors, Nicotinic / metabolism
  • Thiazoles

Substances

  • Insecticides
  • Neonicotinoids
  • Acetylcholine
  • Guanidines
  • clothianidin
  • Thiazoles
  • Receptors, Nicotinic
  • Choline O-Acetyltransferase

Grants and funding

Tobias Pamminger was funded by an EC FP7 Marie Curie Fellowship PIEF-GA-2013-626585. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.