Transcriptome analysis of a springtail, Folsomia candida, reveals energy constraint and oxidative stress during petroleum hydrocarbon exposure

Abstract

Petroleum hydrocarbon (PHC) contamination in soil is ubiquitous and poses harmful consequences to many organisms. The toxicity of PHC-impacted soil is difficult to predict due to variations in mixture composition and the impacts of natural weathering processes. Hence, high-throughput methods to assess PHC-impacted soils is required to expedite land management decisions. Next-generation sequencing is a robust tool that allows researchers to investigate the effects of contaminants on the transcriptome of organisms and identify molecular biomarkers. In this study, the effects of PHCs on conventional endpoints (i.e., survival and reproduction) and gene expression rates of a model springtail species, Folsomia candida were investigated. Age-synchronized F. candida were exposed to ecologically-relevant concentrations of soils spiked with fresh crude oil to calculate the reproductive EC25 and EC50 values using conventional toxicity testing. Soils spiked to these concentrations were then used to evaluate effects on the F. candida transcriptome over a 7-day exposure period. RNA-seq analysis found 98 and 132 differentially expressed genes when compared to the control for the EC25 and EC50 treatment groups, respectively. The majority of up-regulated genes were related to xenobiotic biotransformation reactions and oxidative stress response, while down-regulated genes coded for carbohydrate and peptide metabolic processes. Promotion of the pentose phosphate pathway was also found. Results suggest that the decreased reproduction rates of F. candida exposed to PHCs is due to energy constraints caused by inhibition of carbohydrate metabolic processes and allocation of remaining energy to detoxify xenobiotics. These findings provide insights into the molecular effects in F. candida following exposure to crude oil for seven days and highlight their potential to be used as a high-throughput screening test for PHC-contaminated sites. Adverse molecular effects can be measured as early as 24 h following exposure, whereas conventional toxicity tests may require a minimum of four weeks.