Genome-wide transcriptional response of the archaeon Thermococcus gammatolerans to cadmium

• Published in: PloS one Vol. 7; no. 7; p. e41935
• Main Authors: Lagorce, Arnaud, Fourçans, Aude, Dutertre, Murielle, Bouyssiere, Brice, Zivanovic, Yvan, Confalonieri, Fabrice
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 27.07.2012; Public Library of Science (PLoS)
• Subjects: Adenosine Triphosphate - biosynthesis; Archaea; Archaeal Proteins - genetics; Archaeal Proteins - metabolism; Arsenates; Biochemistry, Molecular Biology; Biology; Biosynthesis; Cadmium; Cadmium - pharmacology; Cadmium content; Cell growth; Cobalt; Cofactors; Copper; Deep sea; Deoxyribonucleic acid; Detoxification; DNA; DNA microarrays; DNA repair; DNA Repair - drug effects; DNA Repair - genetics; Drug Resistance - genetics; E coli; Ecosystems; Escherichia coli; Eukaryotes; Famine; Gamma rays; Gene expression; Genes; Genetic aspects; Genome, Archaeal - genetics; Genomes; Genomics; Heat shock; High resistance; Homeostasis; Homeostasis - drug effects; Homeostasis - genetics; Hydrogenase; Hydrothermal plumes; Hydrothermal systems (Geology); Hydrothermal vents; Iron; Iron - metabolism; Laboratories; Life Sciences; Ligands; Metabolism; Metals; Microbial Sensitivity Tests; Microbiology and Parasitology; Microorganisms; Molecular Sequence Annotation; Nickel; Oligonucleotide Array Sequence Analysis; Oxidation-Reduction - drug effects; Oxidative stress; Permease; Polyamines; Polymerase chain reaction; Prokaryotes; Proteins; Stress, Physiological - drug effects; Stress, Physiological - genetics; Stresses; Sulfur; Sulfur compounds; Thermococcus - drug effects; Thermococcus - enzymology; Thermococcus - genetics; Thermococcus - physiology; Transcription; Transcription (Genetics); Transcription, Genetic - drug effects; Transcriptome - drug effects; Translocation; Transporter; Vents; Zinc; France
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0041935

Thermococcus gammatolerans, the most radioresistant archaeon known to date, is an anaerobic and hyperthermophilic sulfur-reducing organism living in deep-sea hydrothermal vents. Knowledge of mechanisms underlying archaeal metal tolerance in such metal-rich ecosystem is still poorly documented. We showed that T. gammatolerans exhibits high resistance to cadmium (Cd), cobalt (Co) and zinc (Zn), a weaker tolerance to nickel (Ni), copper (Cu) and arsenate (AsO(4)) and that cells exposed to 1 mM Cd exhibit a cellular Cd concentration of 67 µM. A time-dependent transcriptomic analysis using microarrays was performed at a non-toxic (100 µM) and a toxic (1 mM) Cd dose. The reliability of microarray data was strengthened by real time RT-PCR validations. Altogether, 114 Cd responsive genes were revealed and a substantial subset of genes is related to metal homeostasis, drug detoxification, re-oxidization of cofactors and ATP production. This first genome-wide expression profiling study of archaeal cells challenged with Cd showed that T. gammatolerans withstands induced stress through pathways observed in both prokaryotes and eukaryotes but also through new and original strategies. T. gammatolerans cells challenged with 1 mM Cd basically promote: 1) the induction of several transporter/permease encoding genes, probably to detoxify the cell; 2) the upregulation of Fe transporters encoding genes to likely compensate Cd damages in iron-containing proteins; 3) the induction of membrane-bound hydrogenase (Mbh) and membrane-bound hydrogenlyase (Mhy2) subunits encoding genes involved in recycling reduced cofactors and/or in proton translocation for energy production. By contrast to other organisms, redox homeostasis genes appear constitutively expressed and only a few genes encoding DNA repair proteins are regulated. We compared the expression of 27 Cd responsive genes in other stress conditions (Zn, Ni, heat shock, γ-rays), and showed that the Cd transcriptional pattern is comparable to other metal stress transcriptional responses (Cd, Zn, Ni) but not to a general stress response.