Comparative transcriptome analysis uncovers roles of hydrogen sulfide for alleviating cadmium toxicity in Tetrahymena thermophila

Abstract

Background Cadmium (Cd) is a nonessential heavy metal with potentially deleterious effects on different organisms. The organisms have evolved sophisticated defense system to alleviate heavy metal toxicity. Hydrogen sulfide (H2S) effectively alleviates heavy metal toxicity in plants and reduces oxidative stress in mammals. However, the function of H2S for alleviating heavy metal toxicity in aquatic organisms remains less clear. Tetrahymena thermophila is an important model organism to evaluate toxic contaminants in an aquatic environment. In this study, the molecular roles of exogenously H2S application were explored by RNA sequencing under Cd stress in T. thermophila. Results The exposure of 30 μM Cd resulted in T. thermophila growth inhibition, cell nigrescence, and malondialdehyde (MDA) content considerably increase. However, exogenous NaHS (donor of H2S, 70 μM) significantly alleviated the Cd-induced toxicity by inhibiting Cd absorbtion, promoting CdS nanoparticles formation and improving antioxidant system. Comparative transcriptome analysis showed that the expression levels of 9152 genes changed under Cd stress (4658 upregulated and 4494 downregulated). However, only 1359 genes were differentially expressed with NaHS treatment under Cd stress (1087 upregulated and 272 downregulated). The functional categories of the differentially expressed genes (DEGs) by gene ontology (GO) revealed that the transcripts involved in the oxidation–reduction process, oxidoreductase activity, glutathione peroxidase activity, and cell redox homeostasis were the considerable enrichments between Cd stress and NaHS treatment under Cd stress. Kyoto Encyclopedia of Genes and Genomes (KEGG) indicated that the carbon metabolism, glutathione metabolism, metabolism of xenobiotics by cytochrome P450, and ABC transporters were significantly differentially expressed components between Cd stress and NaHS treatment under Cd stress in T. thermophila. The relative expression levels of six DEGs were further confirmed through quantitative real-time polymerase chain reaction (qRT-PCR). Conclusion NaHS alleviated Cd stress mainly through inhibiting Cd absorbtion, promoting CdS nanoparticles formation, increasing oxidation resistance, and regulation of transport in free-living unicellular T. thermophila. These findings will expand our understanding for H2S functions in the freshwater protozoa.

Glyphosate metabolism in Tetrahymena thermophila: A shotgun proteomic analysis approach

“…Most ABC transporter proteins are integral membrane proteins that act as ATP‐driven transporters 66 . In T. thermophila , increased activities of ABC transporters are associated with enhanced tolerance toward xenobiotics 67 . For instance, upregulation of membrane pump proteins (ABC‐transporters) enhanced the tolerance of T. thermophila to DDT by pumping out the toxicants to extracellular spaces and reducing ROS production 68 .…”

“…66 In T. thermophila, increased activities of ABC transporters are associated with enhanced tolerance toward xenobiotics. 67 For instance, upregulation of membrane pump proteins (ABC-transporters) enhanced the tolerance of T. thermophila to DDT by pumping out the toxicants to extracellular spaces and reducing ROS production. 68 Here we have observed that some isoforms of ABC transporters were upregulated at a different dosage.…”

Melatonin Confers Plant Cadmium Tolerance: An Update

“…SA, methane (CH 4 ), and WRKY DNA-binding protein 13 (WRKY13) transcription factor were suggested to be involved in the above process [30,111,112]. H 2 S regulated the activities of key enzymes and AsA-GSH cycle involved in ROS homeostasis to alleviate Cd-induced oxidative stress [113][114][115][116][117][118][119][120]. For example, H 2 S enhanced the activities of antioxidant enzymes, such as POD, CAT, APX, and SOD, and thereby decreased ROS accumulation [120].…”

“…Increasing evidence demonstrates that H 2 S also regulates Cd uptake and translocation in plants [30,117,119,121]. H 2 S enhanced the expression of genes encoding metallothionein (MTs) and phytochelatin (PCS) in Arabidopsis roots [117].…”

“…These results suggested that H 2 S and NO can function in a coordinated way under certain signaling cascades in plants under Cd stress. Increasing evidence demonstrates that H2S also regulates Cd uptake and translocation in plants [30,117,119,121]. H2S enhanced the expression of genes encoding metallothionein (MTs) and phytochelatin (PCS) in Arabidopsis roots [117].…”