Exposure to polylactic acid induces oxidative stress and reduces the ceramide levels in larvae of greater wax moth (Galleria mellonella)

Rohan Shah; Thao V Nguyen; Anna Marcora; Angela Ruffell; Andrew Hulthen; Khoa Pham; Gene Wijffels; Cate Paull; David J Beale

doi:10.1016/j.envres.2022.115137

Exposure to polylactic acid induces oxidative stress and reduces the ceramide levels in larvae of greater wax moth (Galleria mellonella)

Environ Res. 2023 Mar 1:220:115137. doi: 10.1016/j.envres.2022.115137. Epub 2022 Dec 20.

Authors

Rohan Shah¹, Thao V Nguyen¹, Anna Marcora², Angela Ruffell³, Andrew Hulthen², Khoa Pham⁴, Gene Wijffels³, Cate Paull², David J Beale⁵

Affiliations

¹ Land and Water, Commonwealth Scientific and Industrial Research Organisation, Ecosciences Precinct, Dutton Park QLD 4102, Australia.
² Agriculture and Food, Commonwealth Scientific and Industrial Research Organisation, Ecosciences Precinct, Dutton Park QLD 4102, Australia.
³ Agriculture and Food, Commonwealth Scientific and Industrial Research Organisation, Queensland Bioscience Precinct, St Lucia, QLD 4067, Australia.
⁴ CSIRO Manufacturing, Commonwealth Scientific and Industrial Research Organisation, Clayton VIC 4067, Australia.
⁵ Land and Water, Commonwealth Scientific and Industrial Research Organisation, Ecosciences Precinct, Dutton Park QLD 4102, Australia. Electronic address: david.beale@csiro.au.

PMID: 36563977
DOI: 10.1016/j.envres.2022.115137

Abstract

Plastic biodegradation by insects has made significant progress, opening up new avenues for the treatment of plastic waste. Wax moth larvae, for example, have attracted the attention of the scientific community because they are known to chew, ingest, and biodegrade natural polymer bee waxes. Despite this, we know very little about how these insects perform on manufactured plastics or how manufactured plastics affect insect metabolism. As a result, we studied the metabolism of greater wax moths (Galleria mellonella) fed on molasses-supplemented polylactic acid plastic (PLA) blocks. An analysis of the central carbon metabolism (CCM) metabolites was performed using liquid chromatography triple quadrupole mass spectrometry (LC-QQQ-MS), while an analysis of untargeted metabolites and lipids was conducted using liquid chromatography quadrupole time-of-flight mass spectrometry (LC-QToF-MS). In total, 169 targeted CCM metabolites, 222 untargeted polar metabolites, and 196 untargeted nonpolar lipids were identified within the insect samples. In contrast, compared to control larvae, PLA-fed larvae displayed significantly different levels of 97 CCM metabolites, 75 polar metabolites, and 57 lipids. Purine and pyrimidine metabolisms were affected by PLA feeding, as well as amino acid metabolism, carbohydrates, cofactors, vitamins, and related metabolisms. Additionally, PLA exposure disrupted insect energy metabolism and oxidative stress, among other metabolic disturbances. The larvae fed PLA have lower levels of several lipids, suggesting a reduction in lipid reserves, and ceramide levels are likely to have changed due to apoptosis and inflammation. The study indicates that G. mellonella larvae could ingest PLA but this process causes some metabolic stress for the host. Future studies of the molecular pathways of this biodegradation process might help to provide strategies for stress reduction that would speed up insect digestion of plastic.

Keywords: Insects; Lipidomics; Metabolomics; Omics; Plastic biodegradation; Polylactic acid.

MeSH terms

Animals
Bees
Larva / metabolism
Lipids
Moths* / metabolism
Oxidative Stress
Plastics
Polyesters
Waxes / metabolism

Substances

poly(lactide)
Polyesters
Plastics
Waxes
Lipids