Application of omics technology in ecotoxicology of arthropod in farmland

Abstract

Arthropods, abundant in farmland, have unique biological traits that make them valuable for studying the ecotoxicological impacts of pollutants. Recent advancements in multi-omics technologies have enhanced their use in assessing pollution risks and understanding toxicity mechanisms. This article reviews recent developments in applying omics technologies—genomics, transcriptomics, proteomics, metabolomics, and meta-omics—to ecotoxicological research on farmland arthropods. Agricultural arthropods manage genes and proteins, such as metallothioneins, antioxidant enzyme systems, heat shock proteins, cytochrome P450, carboxylesterases, and glutathione S-transferases, for detoxification and antioxidant purposes. They adjust amino acid, sugar, and lipid metabolism to counteract pollutant-induced energy drain and modify gut microbiota to aid in detoxification. This study advocates for enhanced analysis of compound pollution and emerging pollutants using multi-omics, especially meta-omics, to clarify the toxicological mechanisms underlying arthropod responses to these pollutants. Furthermore, it underscores the urgent need for subsequent gene function mining and validation to support biological control strategies and promote sustainable agricultural practices. The findings of this research provide significant insights into the toxicological impacts and mechanisms of pollutants within farmland ecosystems, thereby contributing to the preservation of arthropod diversity.

Introduction

The alterations in biological phenotypes and behaviors induced by pollution are not solely attributable to individual factors but are instead the consequence of the synergistic effects of gene expression and the interactions of multiple proteins (Gong et al., 2020). Traditional methodologies often fall short in elucidating these intricate biological processes. In contrast, omics technologies within systems biology offer a more holistic molecular perspective. Specifically, the integration of multi-omics data enables a more detailed analysis of the toxic metabolic pathways in organisms (Pinu et al., 2019; Canzler et al., 2020; Zhong et al., 2021). Therefore, multi-omics technologies, including genomics, transcriptomics, proteomics, metabolomics, and metabonomics, are extensively utilized in ecotoxicology research (Gong et al., 2020).

Genomics primarily focuses on the investigation of the structure, function, and evolution of genomes, as well as their influence on organisms (Liu et al., 2022). Transcriptomics, which pertains to the biological process of transcription where genetic information is transferred from DNA to RNA, serves as a crucial foundation for elucidating complex biological pathways, regulatory networks of traits, and molecular mechanisms underlying biological adaptation to environmental changes (Liu et al., 2019). Proteomics primarily examines the composition and dynamic patterns of proteins within cells, tissues, or organisms (Liu et al., 2022). Metabolomics focuses on the comprehensive analysis of metabolic responses elicited by living organisms in reaction to exogenous stimuli, environmental alterations, or genetic modifications (Nicholson et al., 1999). Meta-omics uses molecular biology techniques to investigate the composition, function, and diversity of microbial communities as well as the interactions between microbes and their environment (Handelsman et al. 1998; Yuan et al., 2020). From a toxicological standpoint, omics technologies are capable of effectively and accurately producing pertinent information regarding molecular disruptions induced by substances in cells and tissues linked to adverse outcomes (Canzler et al., 2020).

Arthropods, the most diverse and widely distributed phylum in the animal kingdom, exhibit significant phylogenetic proximity to humans (Stork, 2018). Notably, classes such as Insecta and Arachnida (Li et al., 2019), which constitute an integral component of the agricultural ecosystem, are vital for maintaining its stability (Ma et al., 2022b). The abundance of individual arthropods within a community significantly influences community diversity (Bi et al., 2020). Soil arthropods serve as an essential component of the food chain, contributing crucially to the decomposition and degradation of organic matter. Their activities have profound impacts on soil formation, structure, ecosystem equilibrium, fertility maintenance, nutrient cycling, and energy flow (Li & Fan, 2008; Tie et al., 2021).

Pesticide contamination in agricultural soils represents a critical environmental challenge, and omics-based research on the toxicological effects of pollutants on farmland arthropods has garnered considerable scientific interest (Wei et al., 2018; Mao et al., 2019; Wang et al., 2020b). Comparative genomic analysis conducted by Yu et al. (2009) demonstrated that the ingestion of pesticide-contaminated mulberry leaves by Bombyx mori resulted in the amplification of α-esterase in the intestine, epidermis, and head. Additionally, Cd exposure has been shown to increase the mortality rate of spiders. In a study by Lv et al. (2021a), transcriptome sequencing of the venom glands of Pardosa pseudoannulata revealed that Cd stress may downregulate the expression of acetylcholinesterase (AChE) and heavy metal chelating proteins. This downregulation is potentially mediated through alterations in protein processing and degradation within the endoplasmic reticulum. Insects develop resistance to pesticides, and investigating their resistance mechanisms can yield novel insights for research on pest resistance (Qiao et al., 2023). Ju et al. (2022) conducted a transcriptome analysis, revealing that the expression of ATP-binding cassette (ABC) genes was significantly elevated in Cydia pomonella following treatment with avermectin B. Similarly, Erban et al. (2017) performed a proteomic analysis, demonstrating that under permethrin treatment, proteins such as electron carrier cytochrome b5, ribosomal protein 60S RPL28, eIF4E transport protein, and hypoxia-upregulated protein appeared in high abundance in the pollen beetle Meligethes aeneus. Excessive pesticide use can damage beneficial arthropods. Understanding these ecological risks can help safeguard farmland ecosystems (Flexner et al., 1986). Helander et al. (2023) found that glyphosate-sensitive Candidatus Schmidhempelia increased in bumblebees by altering metabolism and lowering mortality using 16S rRNA gene sequencing. Prolonged exposure to polystyrene microplastics (PS-MPs) does not affect bee survival; however, it leads to decreased feeding rates and body weight (Al Naggar et al., 2023). Fluoride disrupts the microbiota-gut-blood barrier function in the host organism B. mori (Li et al., 2022). Omics technology can provide deeper insights into arthropod detoxification mechanisms.

This article examines the utilization of omics technologies in investigating the ecotoxicological impacts of pollutants on arthropods within agricultural environments. This research enhances the comprehension of environmental toxicology pertaining to agricultural pollutants and offers both theoretical and practical foundations for the maintenance the health of agroecosystem.

Ecotoxicological effect of pollutants on arthropods in farmland

The use of chemical agents in agricultural production, such as pesticides, insecticides, and herbicides, significantly negatively affects species stability and biodiversity within farmland ecosystems (Li et al., 2005; Han et al., 2011). Agricultural films and packaging bags decompose into microplastics through solar radiation, human activity, and biodegradation, thereby contaminating the soil (Steinmetz et al., 2016). The application of sewage sludge as agricultural fertilizer can lead to the accumulation of MPs and nanoplastics (NPs) in the soil, which pose a threat to invertebrates (Ng et al., 2018; Li et al., 2018; Oliveira et al., 2019). Per- and polyfluoroalkyl substances (PFAS) are frequently introduced into the environment through end-use products, industrial waste/by-products, and discharged wastewater treatment effluents (Ankley et al., 2021; Beale et al., 2022a), resulting in toxic effects on agro-ecosystems. Additionally, the widespread use of antibiotics in livestock leads to antibiotic-resistant bacteria and genes entering the soil through manure-based fertilizers and wastewater irrigation (Han et al., 2022). Environmental pollutants are hard to break down but easily accumulate in farmland arthropods through biomagnification, leading to toxicity (Lin et al., 2022).

Arthropods, crucial to agriculture, have short life cycles, rapid growth, large populations, and high sensitivity to environmental stress, making them useful for monitoring and remediating environmental pollution (Li et al., 2006). Arthropods develop specific traits and behaviors to detoxify pollutants and maintain balance. For instance, the metallothionein (MT) in Drosophila melanogaster binds metals to regulate homeostasis (Slobodian et al., 2021), whereas Spodoptera litura Fabricius excretes absorbed Cd (Ding et al., 2012). Arthropods can elevate energy use, weaken immune and neural functions, and hinder growth, development, and reproduction, under heavy metals stress (Li et al., 2019). Heavy metal and pesticide pollution can reduce populations and alter community structures by causing reproductive toxicity in arthropods. For instance, Cd stress affects spermatogenesis, sperm vitality, development, and metabolism in males (Tang et al., 2022). Continuous Cu stress significantly inhibits the growth, development, and reproduction of Ostrinia furnacalis, with greater effects at higher concentrations (Wang et al., 2014). Increasing Pb concentration in the feed reduces the survival rate and body mass of S. litura (Shu et al., 2012). Insecticides extend the development time of Helicoverpa armigera (Guo et al., 2023) and sublethal doses of chlorpyrifos inhibit its growth, development, larval, and pupal weight (Li et al., 2005). High-efficiency chlorpyrifos and permethrin at various concentrations inhibit glutathione S-transferase (GST) activity in Aphis species, whereas cypermethrin, deltamethrin, methoxyfenozide, and fluoropyridalyl increase it (Zhang et al., 2015). Sublethal imidacloprid extends the lifespan and pupation period of Spodoptera exigua larvae, reduces body and pupal weight, lowers emergence rate and egg production, and decreases esterase and multifunctional oxidase activity (Lai et al., 2011). Sublethal doses of acetamiprid reduce the lifespan and fertility of Aphis gossypii Glover and affect offspring development (Yuan et al., 2017). The ingestion of plastic debris by invertebrates has been shown to disrupt normal feeding behaviors and physiological functions (Derraik, 2002; Gregory, 2009). In particular, the inclusion of PS in the diet of Tenebrio molitor resulted in a reduction of protein content and fecal nitrogen in their biomass (Tsochatzis et al., 2022). Furthermore, exposure to perfluorobutanoic acid was found to influence body weight gain during the development of second instar S. exigua larvae and to accelerate molting by affecting the downstream ecdysone receptor/ultraspiracle protein regulatory genes, which are critical for molting and development. Additionally, perfluorobutanoic acid exposure led to a reduction in molting time in these larvae (Omagamre et al., 2020).

Atmospheric deposition, sewage-based agro-irrigation, and the application of agricultural materials such as fertilizers and solid waste contribute to heavy metal contamination in agricultural fields. The primary sources of emergent pollutants in these fields encompass the application of pesticides, including insecticides, fungicides, and herbicides (You et al., 2023); the utilization of farmyard fertilizers, which result in the accumulation of antibiotic residues and antibiotic resistance genes carried by microorganisms (Liu et al., 2024b); and the introduction of emergent pollutants through irrigation water (Zhang et al., 2023; Lim, 2019). Additionally, the use of agricultural supplies such as films and equipment facilitates the release of MPs and PFAS. These substances, along with PFAS-containing pesticides and sewage, accumulate in agricultural fields (Jin et al., 2022). Neutral and ionic PFAS predominantly occur in the atmospheric gas and particle phases, respectively (Zhu et al., 2024). In aquatic environments, PFAS are primarily composed of short- and medium-chain monomers, including perfluorobutyl sulfonate, perfluorooctane sulfonate, and perfluorooctanoic acid (Song et al., 2022). Furthermore, perfluorooctane sulfonate and perfluorooctanoic acid are the principal PFAS detected in soil (Zhu et al., 2024). Additionally, agricultural activities contribute significantly to air pollution through the emission of substances such as ammonia, methane, nitrogen oxides, volatile organic compounds, and persistent organic pollutants. These emissions originate from various sources, including fertilizer application on farmland, livestock breeding, pesticide use, combustion of agricultural residues, operation of agricultural machinery, and agricultural irrigation (Ge et al., 2021). Pollution sources in agricultural ecosystems and their toxic effects on arthropods include affecting population structure, decreased predation performance, hindered reproduction, reduced survival rates, and population instability, etc. (Figure 1).

Application research of omics in the ecotoxicology of arthropods in farmland

Genomics

Genomic methodologies offer a comprehensive insight into the alterations occurring across the entire genome of agricultural arthropods when exposed to toxic substances. In reaction to exogenous pollutants, detoxification enzyme families, including cytochrome P450s (P450s), carboxylesterases (CarEs), and GSTs, are likely to play a pivotal role in the detoxification processes of these organisms. Van Straalen et al. (2011) identified that the Cyp6g1 gene is implicated in stress tolerance in Musca domestica L., exhibiting toxicity through mechanisms such as upregulation, gene duplication, or structural modifications. Zhou et al. (2015a) identified numerous detoxification enzyme genes in the whole genome sequencing of Anopheles, including P450s, GSTs, and choline/carboxylesterases. The overexpression of certain P450 genes has been shown to enhance the metabolic capacity of pests to degrade insecticides. Notable examples include the overexpression of cytochrome oxidase genes CYP6P9a and CYP6P9b in Anopheles funestus, CYP6B7 in H. armigera, and CYP6A51 in Ceratitis capitata (Zhang et al., 2010a; Ibrahim et al., 2015; Arouri et al., 2015). Similarly, the overexpression of GST genes such as GSTE2, BmGSTe2, CpGSTd1, and CpGSTd2 in Anopheles gambiae, Culex pipiens, and B. mori confers metabolic resistance to insecticides (David et al., 2005; Samra et al., 2012; Zhou et al., 2015b). The primary mechanism underlying the metabolic resistance of M. domestica to pyrethroid insecticides is likely the overexpression of the carboxylesterase MdαE7 gene (Zhang et al., 2010b). The expression of MT genes, induced by Cd, Cu, and Zn in the larvae of Culex quinquefasciatus, can mitigate the toxicity associated with these heavy metals (Sarkar et al., 2004). Additionally, Cd significantly upregulates the expression of MT genes in Collembola (Van Straalen et al., 2011). Poynton et al. (2007) elucidated distinct expression profiles in Daphnia magna subjected to sublethal concentrations of Cu, Cd, and Zn, revealing that Cd may induce oxidative stress, Cu may lead to immunosuppression, and Zn may affect chitinase activity. In addition to the upregulation of detoxification genes, specific gene mutations can also mitigate the toxic effects of pollutants. For instance, Culicidae develop drug resistance through mutations in VGSC genes, altering channel proteins and reducing insecticide sensitivity (Yuan et al., 2021). Muhammad et al. (2021) showed that PS-MPs induced an increase in the expression of B. mori lysozyme, SOD and GST genes, and an increase in the activities of superoxide dismutase (SOD), GST, and catalase enzymes, whereas PS-NPs were more inhibitory to SOD activity and expression. In addition, genomic technology applied in other farmland arthropod toxicology (Table 1).

Transcriptomics

Transcriptomic analysis can assess the impacts of various modes of action, dosages, and exposure durations of pollutants in agroecosystems on the transcriptional expression profiles of arthropods. This approach aids in elucidating the genetic characteristics and evolutionary adaptability of arthropods within farmland environments. Exposure to pesticides and herbicides changes the expression of genes like P450, GST, CarE, UDP-glucuronosyltransferase (UGT), and ABC transporters in insects (Yu et al., 2023). Transcriptomic analysis of the cephalothorax of P. pseudoannulata reveals that CYP450, GST, AChE, nicotinic acetylcholine receptor, γ-aminobutyric acid receptor, and glutamate-gated chloride channels are single genes encoding detoxification metabolic enzymes and target receptor genes in this species (Meng et al., 2015a). Certain agricultural insects enhance their resistance to pesticide stress by overexpressing resistance enzyme activity. For instance, comprehensive transcriptome and functional analyses have demonstrated the upregulation of P450 genes in the fat body and gut of Rhynchophorus ferrugineus larvae (Antony et al., 2019). Similarly, de novo transcriptomic analysis has revealed the upregulation of CYP450, GST, and UGT genes in Spodoptera frugiperda (Hafeez et al., 2021). Quantitative real-time polymerase chain reaction showed that the P450 gene CYP4G68 is overexpressed in Bemisia tabaci populations resistant to imidacloprid and thiamethoxam (Liang et al., 2022). Notably, significant upregulation of GSTd2 and GSTe2 genes has been associated with resistance to pyrethroids in Anopheles sinensis (Tao et al., 2022). Additionally, the transcription factor aryl hydrocarbon receptor has been shown to regulate the expression of the C. pomonella GST gene, thereby enhancing resistance (Hu et al., 2023). Additionally, the amplification of E4 and FE4 in carboxylesterase genes has been associated with increased expression of CarEs, contributing to resistance against organophosphorus insecticides (Srigiriraju et al., 2009). As a potential bioindicator for heavy metal pollution in agroecosystems, scholars have performed transcriptomic analyses on various tissues and organs of spiders, including venom glands, brain ganglia, and ampullate glands. These studies have demonstrated that Cd induces selective differential expression of genes associated with detoxification, immunity, and antioxidant stress responses, thereby mitigating toxicity (Li et al., 2016; YaNg et al., 2018a, 2018b, 2021, 2023). Prolonged Cd exposure can disrupt ion binding and neurotransmitter receptors, leading to neurotoxicity and reduced energy metabolism in spiders (Lv et al., 2021b). Yang et al. (2023) found that combined Cd and Pb exposure in Araneus ventricosus upregulated ampullate silk protein and Far genes, downregulated amino acid synthesis and TUBA genes, and overexpressed AChE and Glu genes. Transcriptome analysis and Kyoto Encyclopedia of Genes and Genomes profiling by Zhong et al. (2022) showed that T. molitor acts as a downstream catabolizer in plastic depolymerization, and that the fatty acid degradation pathway may play an important role in the digestion of plastic degradation intermediates produced by intestinal bacteria. In addition, transcriptomic technology applied in other farmland arthropod toxicology (Table 2).

Proteomics

Proteomics facilitates the analysis of global protein expression changes in agricultural arthropods subjected to various pollutants or environmental conditions. Hua et al. (2023) confirmed the differential expression of proteins associated with resistance in Aedes albopictus, identifying that alanine aminotransferase, uridine-cytidine kinase, and GST were upregulated in resistant specimens. Culicidae exhibit the ability to modulate their tolerance to heavy metals through alterations in their proteome. Rono et al. (2019) used differential proteomics to observe a marked downregulation of proteins associated with the immune response, energy metabolism, antioxidant enzymes, protein synthesis, and proton transport in Culicidae following Cd exposure. Choi & Ha (2009) also utilized proteomics analysis to demonstrate that Cd exposure induces changes in the expression of hemolymph proteins and total hemoglobin in Chironomus riparius Mg. Cadmium and Cu induce both qualitative and quantitative alterations in the hemolymph proteome of spiders, prompting the midgut gland to synthesize substantial quantities of MTs to safeguard the hemocytes within the hemolymph proteins (Kuhn-Nentwig & Nentwig, 2013; Wiśniewska et al., 2022, 2023). Cadmium typically disrupts protein processing and endoplasmic reticulum degradation, thereby downregulating the immune function of the spider venom gland (Lv et al., 2021a). The primary mechanism by which insects develop resistance to Bacillus thuringiensis toxin involves mutations or downregulation of midgut receptor proteins (Peng et al., 2024). The mutation of the cadherin allele Ha Cad, which results in a nonfunctional protein, imparts resistance to the Cry1Ac toxin in H. armigera (Xiao et al., 2017). In a resistant strain of S. frugiperda, a mutation in the ABCC2 gene causes protein truncation, thereby inhibiting the translated protein from functioning as a toxin receptor (Flagel et al., 2018). In addition, proteomics techniques applied in other farmland arthropods toxicology (Table 3).

Metabolomics

Metabolomics technology provides insights into the effects of pollutants on the metabolic profiles of arthropods. Shi et al. (2018) utilized liquid chromatography-mass spectrometry and gas chromatography-mass spectrometry techniques to determine that subchronic exposure to the neonicotinoid insecticide thiacloprid resulted in the upregulation of most differential metabolites in the Apis head, significantly affecting glutathione metabolism and glycerophospholipid metabolism pathways. Similarly, Yu et al. (2022) used nuclear magnetic resonance spectroscopy to demonstrate that insecticides adversely affect the growth and development of S. litura Fabricius by inhibiting sugar metabolism and chitin synthesis. Chlorpyrifos inhibited the growth and nutritional indicators of the Chinese tallow caterpillar (Hyphantria cunea) by downregulating adenosine 5′-monophosphate (AMP)-activated protein kinase-related genes, resulting in reduced levels of carbohydrates, adenosine triphosphate, and pyruvic acid, and consequently leading to metabolic disorders in the larvae (Zhao et al., 2023a). De Bont & Van Larebeke (2004) investigated the effects of Zn exposure on Chironomid and observed that low Zn exposure significantly increased phosphorylated sugars, deoxyhexose, and phosphofructokinase activity, whereas high Zn treatment upregulated MT gene expression in the larvae. Furthermore, elevated concentrations of Cd markedly affect the drug metabolism-CYP450 pathway in Glyphodes pyloalis Walker, leading to detrimental effects on detoxification and metabolic processes (Zhao et al., 2024). Beale et al. (2022b) conducted an analysis of central carbon metabolism metabolites utilizing targeted triggered multiple reaction monitoring liquid chromatography triple quadrupole mass spectrometry. Their findings indicated that black soldier fly (BSF), mealworm, and wax moth (WM) larvae exposed to various plastic matrices exhibited distinct metabolic responses. Specifically, BSF larvae reared on polyethylene terephthalate demonstrated elevated pyrimidine metabolism, while the purine metabolic pathway was prominently expressed in larvae exposed to polyethylene, PS, expanded PS, polypropylene, and polylactic acid (PLA). Additionally, BSF larvae displayed an increased metabolic rate of vitamin B6 across all plastic types, attributed to the disruption of intestinal symbionts and the downregulation of vitamin B6 metabolism. In contrast, mealworm and WM larvae showed heightened metabolic activity on PLA and styrofoam, with WM larvae exhibiting increased vitamin B6 metabolism. Furthermore, Beale et al. (2022c) used lipid staining techniques to demonstrate that exposure to PFAS led to enhanced lipid accumulation in Daphnia, suggesting that the increase in lipid content results from the repression of genes associated with fatty acid uptake and catabolism. In addition, metabolomic techniques applied in other farmland arthropod toxicology (Table 4).

Meta-omics

Meta-omics, including metagenomics, metatranscriptomics, and metaproteomics, offers profound insights into the community structure and functional alterations of gut microbiota in agricultural arthropods subjected to pollutant stress, elucidating the interactions between microbial communities and their hosts within physiological mechanisms. Gut microbes and their hosts engage in a symbiotic relationship, contributing to host nutrient absorption, metabolic functions, immune system modulation, development, and detoxification (Cao & Ning, 2018). The gut microbiome of insects comprises Protozoa, Fungi, Archaea, and Bacteria (Siddiqui et al., 2022). Various agricultural arthropods harbor distinct gut microbes capable of degrading toxins, pesticides, and other pollutants. For example, in Chang et al. (2023), 16S rRNA sequencing revealed that the gut microbiota of S. frugiperda is predominantly composed of Proteobacteria and Firmicutes. However, following pesticide exposure, there was a significant increase in the abundance of Nitrospirae, Bacillus, Thioalbus, and Flavobacterium. Chen et al. (2021b) showed by RNA sequencing that antibiotic treatment decreased Firmicutes in S. frugiperda, with a significant decrease in the abundance of Enterococcus and Weissella. In addition, metatranscriptomic analysis revealed that energy production, metabolism, and autophagy-lysosome signaling pathways were affected. Results from 16S rRNA sequencing of the gut bacteria in Chironomid larvae indicated that heavy metal pollution did not affect the dominant bacterial phyla; however, genes associated with metabolism exhibited a significantly high relative abundance (Ma et al., 2023). In Sun et al. (2022), 16S rRNA gene sequencing revealed that Cu pollution significantly increased the relative abundance of Comamonas, Stenotrophomonas, and Yersinia, whereas diazinon exposure raised Serratia levels, altering the gut microbial community in Propsilocerus akamusi. Additionally, transcriptome and gut microbiota analyses in P. akamusi showed that rifampicin exposure led to a significant rise in Deferribacteres and Bacteroidetes, with Tetragena positively correlated with detoxifying genes PaCYP6GF1 and PaCYP9HL1 (Sun et al., 2023). YaNg et al. (2018c) used metatranscriptomics to study gut microbes in P. pseudoannulata, finding that Cd exposure significantly altered microbial community structure and gene expression. Eukaryotes, bacteria, and viruses decreased, whereas Archaea increased. The Cd stress also affected genes related to carbon, protein, amino acid, glucose metabolism, oxidative phosphorylation, and glutathione metabolism. The community structure and function of gut microbiota in farmland arthropods appear to exhibit varying responses to pollutants. Yang et al. (2020) used high-throughput 16S rRNA sequencing to find that Citrobacter sp. and Enterobacter sp. were associated with the polypropylene diet in the gut microbiome of Zophobas atratus larvae, whereas Kluyvera was predominant in T. molitor larvae. Furthermore, numerous meta-omics technologies have been utilized in the field of agricultural arthropod toxicology research (Table 5).

Joint application of multi-omics

The extensive application of multi-omics joint analysis enables a more systematic understanding of the differences in gene and protein expression, metabolite composition, and response changes of gut microbiota in agricultural arthropods exposed to pollutants. This approach offers comprehensive insights into the ecological toxicology of these organisms. Combined transcriptomic and metabolomic analyses have demonstrated that pesticide exposure induces alterations in arginine, glutamic acid, aspartic acid, and lysine, resulting in the mortality of S. frugiperda larvae and subsequently influencing population dynamics (Gao et al., 2022). A combined analysis of targeted lipidomics and metabolomics has revealed that neonicotinoid insecticides significantly elevate lactate dehydrogenase activity and caspase levels, attributable to their impact on cellular necrosis and apoptosis, thereby disrupting lipid peroxidation and glutathione metabolic pathways (Wang et al., 2022b). Wu et al. (2022) investigated the sublethal effects of chlorantraniliprole on Coccinella septempunctata larvae, reporting adverse outcomes, including diminished predation efficiency, weight reduction, shortened lifespan, decreased reproductive capacity, and prolonged developmental stages. Transcriptome sequencing and real-time fluorescence quantitative analysis revealed alterations in genes associated with the biosynthesis of retinol, carcinogens, insect steroid hormones, P450 metabolism, and exogenous biometabolism. Chen et al. (2021a) demonstrated that low-level heavy metal stress induces stimulation, whereas high-level heavy metal stress results in inhibition at the transcriptome and proteome levels. Additionally, transcriptomic and proteomic analyses of silk glands indicated that Cd exposure markedly inhibited growth, development, and amino acid metabolism in P. pseudoannulata (Lv et al., 2023). Muhammad et al. (2024) used a multi-omics approach of metabolomics, 16S rRNA, and transcriptomics to study the changes in B. mori exposed to PS and micro- and nano plastic (MNP) and found that there is a significant alteration in lipid metabolism, which is used to increase energy reserves. Additionally, various multi-omics methodologies have been used in the study of arthropod toxicology within agricultural contexts (Table 6).

Summary and outlook

Potential mechanisms of ecotoxicity of pollutants on arthropods in farmland

Pollutants present in agricultural fields can interfere with the cellular growth, proliferation, differentiation, and damage repair processes in arthropods, leading to cell apoptosis, triggering immune responses, inducing oxidative damage, enzyme inactivation, metabolic disorders, and genotoxicity (Balali-Mood et al., 2021). Arthropods have evolved distinct physiological and biochemical characteristics, as well as behaviors, to mitigate the detrimental effects of pollutants and maintain homeostasis. For example, they possess mechanisms to store and accumulate pollutants internally, excrete them, and adapt to these environmental stressors. In arthropods, hemolymph proteins like vitellogenin, lipoproteins, and storage proteins regulate detoxification, immune functions, cell physiology, and nutrient metabolism (Gianazza et al., 2021). Metal detoxification primarily involves MT, antioxidant enzymes, heat shock proteins, and energy compensation. Metallothioneins bind heavy metals competitively, reducing their nonspecific cell binding and toxicity (Amiard et al., 2006). Insect detoxifying enzymes such as P450s, CarEs, GSTs, and so forth, reduce toxicity by enhancing the conversion and degradation of exogenous toxic compounds (Huang & Qiao, 2002; Sweetlove & Fernie, 2018). Arthropods in farmland mainly cope with pollutant exposure by regulating amino acid metabolism, gluconeogenesis, glycolysis, lipid and carbohydrate metabolism (Dai et al., 2021; Chen et al., 2022b; Singh et al., 2022). Under pollutant stress, arthropod gut microbial diversity and abundance shift, typically dominated by Proteobacteria and Firmicutes (Chang et al., 2023; Liu et al., 2020). Omic studies reveal that agricultural arthropods respond to pollutants by regulating detoxification genes and proteins, altering energy metabolism and transport, and interacting with gut microbes (Figure 2).

Outlook

Currently, omics analysis is extensively used in the ecotoxicological investigation of agricultural arthropods; however, several limitations persist. Specifically, there is a paucity of research examining the toxic effects of combined exposure to multiple pollutants, and studies addressing the impacts of emerging pollutants, such as antibiotics and microplastics, remain inadequate (Niu et al., 2022; Wei et al., 2023a). Future research should focus on integrating omics analysis with studies on compound pollution and novel pollutants. This approach would enhance our understanding of the responses of agricultural arthropods to emerging pollutants and elucidate their detoxification mechanisms (Teng et al., 2021; Zhi & Wang, 2024). Certain arthropods possess distinct physiological characteristics that facilitate the transformation and elimination of pollutants. Beale et al. (2022b) proposed the development of an insect biotransformation pipeline to connect specialized insect models with the issue of plastic waste. For instance, G. mellonella, known for its biodegradation capabilities, has been shown to ingest PLA plastics (Shah et al., 2023). Additionally, Tepper et al. (2023) provided the first evidence that the BSF can remediate methylmercury by converting it into volatile mercury oxide. Numerous other research methodologies exist, highlighting the urgent need for the development of innovative technologies and methods that integrate agroecology and biodiversity conservation to advance green and sustainable development.

The physiological functions and mechanisms of organisms are inherently complex, rendering a singular omics approach inadequate for a comprehensive elucidation of detoxification mechanisms (Mao et al., 2019). It is imperative to advance the integrated application of meta-omics alongside other omics methodologies to elucidate the synergistic effects of gut microbiota and symbiotic bacteria in ecotoxicology of agricultural arthropods (Gao & Chu, 2020; Zhang et al., 2017). Many insect gut microorganisms have been tested and shown to degrade a wide range of plastics, including the T. molitor (Lou et al., 2021), Tenebrio obscurus (Peng et al., 2019), and others. Conducting research from multiple perspectives, systems, and disciplines furnishes a robust scientific foundation for risk assessment and the judicious application of agricultural pollutants on arthropods.

Omics technologies serve as the principal methodologies for investigating the responses and underlying mechanisms of agricultural arthropods to pollutants. Presently, there is a pressing need to conduct research focused on the identification and validation of key regulatory genes, proteins, and functional microorganisms (Zhao et al., 2023b). Meng et al. (2016, 2017) identified novel functional AChEs in P. pseudoannulata, whereas Zhang et al. (2014) successfully cloned several AChE genes (Pp-ace1-5) from the natural predators of P. pseudoannulata. Meng et al. (2015b) used RNAi technology for the first time to study the sensitivity of two AChEs to pesticides in P. pseudoannulata. These studies are pivotal for advancing research on novel insecticides. Consequently, the application of emerging technologies and the exploration of new gene functions furnish a robust theoretical and practical foundation for the development of biological control methods and the promotion of sustainable agriculture (Wu & Song, 2020; Tan, 2022).

The FAIR principles, as outlined by Berrios et al. (2018), serve as a foundational framework for ensuring data findability, accessibility, interoperability, and reusability. To transition from multiple histology datasets to integrated multi-histology datasets, ecosystems must adhere to these principles. This adherence will facilitate the harmonization of data repositories, thereby enhancing multi-histology data storage, interoperability, and communication across diverse communities, as noted by Giannattasio et al. (2023). Rund et al. (2019) introduced Minimum Information for Reusable Arthropod Abundance Data, the inaugural standard for arthropod abundance data, which aims to harmonize data across research initiatives and communities engaged in the surveillance and control of vector-borne diseases and pests. Furthermore, Hutchins et al. (2023) used the Indigenous Data Sovereignty framework to address practical considerations related to genomic data, including data collection, governance, and communication. Consequently, there is an urgent imperative to advance research efforts focused on the sharing, mining, and utilization of extensive arthropod genomic data.

Histologic studies in ecotoxicology face challenges (Forbes et al., 2006), but advancements are being made with richer genomic data for nonmodel species and expanding public databases. Improved bioinformatics tools are needed to integrate genomic, proteomic, lipidomic, and metabolic data across taxa (Ebner, 2021). Combining genomics with biochemical and computational methods can enhance mechanistic studies of nonmodel organisms, addressing issues like population diversity, tolerance to contaminants, phenotypic plasticity, and disease susceptibility (Rosner et al., 2023). Species within taxa often share similar genomic structures and cellular pathways (Benson & Giulio, 2006). Cross-taxonomic studies can prevent redundant research on the same species and stressors, whereas understanding common methods and frequently studied taxa can enhance the application of histological techniques to new groups (Ebner, 2021). Merging characterization data from distantly related taxa can advance functional ecology (Luza et al., 2023). Thus, conducting cross-taxon research on genes, proteins, and biological pathways is crucial in the expansive field of arthropod genomics.

Data availability

The authors confirm that this review article does not include any supporting information. All data and information essential for understanding and evaluating the content of this article are presented within the main text and references. Therefore, there are no additional datasets, files, or other supplementary materials to be made accessible. We are committed to transparency and accessibility in research and affirm that all pertinent information is readily available in the published article.

Author contributions

Zhongyuan Li (Writing – review & editing), Cuimei Gao (Methodology), Zhuoman Wang (Visualization), Siqi Huang (Formal analysis), Zijian Jiang (Formal analysis), Jing Liu (Writing – review & editing, Supervision), and Huilin Yang (Writing – review & editing, Supervision)

Funding

This study was funded by the National Natural Science Foundation of China (Nos. 32001205), Natural Science Foundation of Hunan province (Nos. 2023JJ30299, 2019JJ50236), Hunan University Student Innovation and Entrepreneurship training program (Nos. 2664).

Conflicts of interest

The authors declare no conflicts of interest.

Acknowledgments

Our deepest gratitude goes to the anonymous reviewer(s) for their careful work and thoughtful suggestions that helped improve this article substantially.

References