Does the presence of heavy metal and catechol contaminants in organic waste challenge the physiological performance of the bioconverter Hermetia illucens?

The worldwide population growth, which ranges from 1 to 2% since the 1960s (Roser et al., 2013), and the booming economy and urbanization have significantly increased the production of solid wastes (Bingemer and Crutzen, 1987, Tarmudi et al., 2009, Nanda and Berruti, 2021). As a result, waste management has become a hot topic over the years, as inappropriate collection, disposal and recycling highly increase the risks of social and environmental issues (reviewed in Ferronato and Torretta, 2019). Owing to the large diversity of solid wastes, several engineering and/or biological techniques are implemented for their management, including combustion, composting (fermentation), pyrolysis, conversion into fuels (Mahmoud et al., 2022) or other solid materials (Chen and He, 2012, Kiran et al., 2014, Bilal et al., 2019, Yaashikaa et al., 2020). Importantly, the solution used for waste management must be technically and financially feasible, in addition to be eco-friendly.

Even if the sources and proportions of solid wastes vary from one country to another, and among urban areas, household wastes account for 55-80% of the total solid waste production (Abdel-Shafy and Mansour, 2018). In the 28-UE countries, for instance, food waste production has been estimated to 100 million tons / year, of which 45% are coming from households (Timmermans, 2015). The per capita household food wastes amounts to 82 kg in Germany, 99 kg in France, or 110 kg in Great Britain (Waste 2012). Food waste treatment has long relied on the use of anaerobic digestion, or composting alternatives. Yet, these procedures are based on fermentation processes which are contributing to greenhouse gas emission, thus increasing the ongoing climate change problem (Ramos-Elorduy, 2009, Meyer-Rochow and Chakravorty, 2013). This context has stimulated a range of investigations aiming at finding alternative waste management procedures, and at improving the recycling stream of solid wastes.

Insect-based bioconversion of food wastes has become very popular in the recent years (Gasco et al., 2020, Ravi et al., 2020, Kim et al., 2021, Lim et al., 2022), and typically represents an eco-friendly biological technology for waste management. Several insect species have been proved efficient models for sustainable food waste management, including the yellow mealworm Tenebrio molitor, the codling moth Cydia pomonella, the housefly Musca domestica, and the black soldier fly Hermetia illucens (see Fowles and Nansen, 2020, for a review). The large diversity of organic wastes the black soldier fly can consume – be it dry or wet – its short life span (Fowles and Nansen, 2020), voracity and high biomass conversion ratio (Surendra et al., 2020), makes it a valuable tool for food waste management. Moreover, larvae of the black soldier fly outperform other technologies in terms of costs, ecological footprints, and overall efficiency (Singh and Kumari, 2019), and have thus become a popular model all around the world for the management of food wastes.

While food wastes are largely made by food residues, they may also contain several additional organic residues, as for instance waste tableware, plastic fragments, or towels. Also, in some municipalities, food wastes are stored into biowaste bags before collection, and these bags have been reported as significant containers of heavy metals (Huerta-Pujol et al., 2010). Heavy metals are naturally present in the environment (volcanoes and erosion, for example), in addition to have an anthropogenic source. Anthropogenic contribution in the transfer of heavy metals to the environment ranges from electronic waste dispersion, unsafe management of medical wastes, industrial production and release of fertilizers, battery production, mining, pesticides, textiles, dyes, or painting (Fulekar et al., 2009, Dixit et al., 2015). The geochemical cycle of heavy metals can further maximize their accumulation in the environment, and this contributes to the destruction of ecosystem balances and loss of biodiversity (D′amore et al., 2005). Several other contaminants can also accumulate in the environment, including pesticides, pharmaceutical, hazardous wastes, or organic contaminants (Kassir et al., 2012, IDA, 2014, Vij, 2015), and vegetables and fruits can thus get contaminated by cadmium, lead, chromium, or iron (Melai et al., 2018, Sharma and Nagpal, 2020). Additional contamination may even occur during the processing and treatment stages of food and food wastes (Thakali et al., 2021). Thus, the potential presence of several classes of contaminants must be taken into account when assessing the insect-based management of food wastes.

The effects of heavy metals on living organisms have been studied intensively over the years (Cosio and Renault, 2020, Soliman et al., 2022), and evidence of the deleterious effects these pollutants have on biodiversity has accumulated. In contaminated soils, plant development may become impossible, as heavy metals inhibit the uptake of nutrients and plant growth, they impair enzymatic activity, induce oxidative stress and damages to macromolecules, ultimately leading to genotoxicity (Rasmussen et al., 2000, Olaniran et al., 2013, Fashola et al., 2016). In insects,heavy metals damage macromolecules, generating protein carbonylation, lipid peroxidation, or DNA strand breaks which are induced by increased levels of oxidative stress (Abdelfattah et al., 2017; Youssef et al., 2017). As a result, assessments of antioxidant capacities can provide a rapid and low-cost evaluation of the capability of the insects to handle exposure to a range of environmental stressors (Lalouette et al., 2011, Lawniczak et al., 2013, Renault et al., 2016), including exposure to heavy metals.

As mentioned above, food wastes can contain a range of contaminants other than heavy metals, as for instance catechol. While little catechol amounts can be found in fruits and vegetables, this compound is also synthesized as precursor of flavors and pesticides, and can reach high levels owing to its capacity to quickly solubilize in aqueous solutions, becoming toxic to living organisms. With the growing importance in finding eco-friendly solutions for food waste management, we are urgently needing information on the effects of food wastes contaminated by heavy metals and catechol on insects. If the insects can handle such contaminated wastes, they may be valuable candidates for bioremediation and elimination of the excess of heavy metals and catechol from food wastes at lower costs as compared with the currently used techniques, such as chemical oxidation reaction, adsorption processes, and electrochemical techniques (Ahluwalia and Goyal, 2007, Wu et al., 2010; Siddique et al., 2015).

In the study, the physiological responses of the black soldier fly H. illucens grown in presence of contaminants - in the form of heavy metals and catechol - in food waste was evaluated. To that aim, 5th instars were used, as this often corresponds to the developmental stage which is considered in laboratory studies examining the impacts of contaminants on gut content and structure of H. illucens (Bonelli et al., 2020, Tanga et al., 2021, Zhineng et al., 2021). Larvae were reared on different types of food wastes (kitchen, fruit, or vegetable wastes), which may supply the insect with a range of compounds having pro-oxidant activities, or inducing oxidative stress (vegetable wastes with vegetables containing phenolic compounds). Food wastes were also contaminated with heavy metals or catechol. Seven days after the larvae were exposed to those experimental conditions, the concentration of H2O2, protein carbonylation, ascorbic acid, SOD activity, PPO activity, reducing power ability, antioxidant ability and antiradical activity DPPH was measured from the gut of the larvae. As heavy metals were formerly reported to have little effects on the growth and development of the black soldier fly larvae, we hypothesized that they would have low impacts on the diverse components of the antioxidant system we considered. Also, by focusing on the physiological effects of catechol and heavy metals at the gut level, an important biological compartment at play during biorecycling processes of organic wastes, we are first suggesting that the monitoring of oxidative stress responses could represent valuable metrics for assessing the effects of contaminants in this important insect biorecycler.

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