Cadmium detoxification induced by salt stress improves cadmium tolerance of multi-stress-tolerant Pichia kudriavzevii

Highlights: • Salt stress induced obvious cross-protection for Cd tolerance in P. kudriavzevii. • Improved Cd conjugation with GSH and transport by YCF1 and YOR1 reduced Cd toxicity. • Salt stress improved antioxidative ability to alleviate Cd-induced oxidative stress. • HSPs and trehalose contributed to improved Cd tolerance by salt stress. • Inhibited ZRT1 and enhanced YOR1 decreased intracellular Cd concentration. Heavy metal tolerance of microorganisms is the basis of heavy metal removal by growing cells. In this study, a cross-protection effect generated by salt stress significantly enhanced the cadmium tolerance of multi-stress-tolerant Pichia kudriavzevii. Comparative transcriptome analysis using RNA-Seq linked with physiological and biochemical observation was used to elucidate the underlying mechanisms of the improved cadmium tolerance. The expression of cadmium transport related genes (GSTY2, GLR1, GLO2, YCF1 and YOR1), GSH content and GST activity were elevated by salt stress, suggesting enhanced cadmium conjugation and detoxification in yeast cells. The inhibited cadmium uptake by ZRT1 and enhanced cadmium efflux by YOR1 contributed to the decrease in the intracellular cadmium concentration. The improved expression of antioxidant enzyme genes (SOD1, SOD2, SOD6, CAT1 and PRXIID), along with the enhanced activities of antioxidant enzymes (SOD, CAT and POD) resulted in a decrease in cadmium-induced ROS production, protein carbonylation, lipid peroxidation and cell death. The abundant expression of heat shock protein genes (HSP12, HSP10 and SSC1) and genes related to trehalose synthesis (TPS1 and TSL1) induced by salt stress protected yeast cells against complex stress conditions, contributing to the improved cadmium tolerance. These findings will be useful to develop cadmium-tolerant yeasts for cadmium removal by growing cells.