Cadmium triggers an integrated reprogramming of the metabolism of Synechocystis PCC6803, under the control of the Slr1738 regulator.
BACKGROUND
Cadmium is a persistent pollutant that threatens most biological organisms, including cyanobacteria that support a large part of the biosphere. Using a multifaceted approach, we have investigated the global responses to Cd and other relevant stresses (H2O2 and Fe) in the model cyanobacterium Synechocystis PCC6803.


RESULTS
We found that cells respond to the Cd stress in a two main temporal phases process. In the "early" phase cells mainly limit Cd entry through the negative and positive regulation of numerous genes operating in metal uptake and export, respectively. As time proceeds, the number of responsive genes increases. In this "massive" phase, Cd downregulates most genes operating in (i) photosynthesis (PS) that normally provides ATP and NADPH; (ii) assimilation of carbon, nitrogen and sulfur that requires ATP and NAD(P)H; and (iii) translation machinery, a major consumer of ATP and nutrients. Simultaneously, many genes are upregulated, such as those involved in Fe acquisition, stress tolerance, and protein degradation (crucial to nutrients recycling). The most striking common effect of Cd and H2O2 is the disturbance of both light tolerance and Fe homeostasis, which appeared to be interdependent. Our results indicate that cells challenged with H2O2 or Cd use different strategies for the same purpose of supplying Fe atoms to Fe-requiring metalloenzymes and the SUF machinery, which synthesizes or repairs Fe-S centers. Cd-stressed cells preferentially breakdown their Fe-rich PS machinery, whereas H2O2-challenged cells preferentially accelerate the intake of Fe atoms from the medium.


CONCLUSIONS
We view the responses to Cd as an integrated "Yin Yang" reprogramming of the whole metabolism, we found to be controlled by the Slr1738 regulator. As the Yin process, the ATP- and nutrients-sparing downregulation of anabolism limits the poisoning incorporation of Cd into metalloenzymes. As the compensatory Yang process, the PS breakdown liberates nutrient assimilates for the synthesis of Cd-tolerance proteins, among which we found the Slr0946 arsenate reductase enzyme.
Houot
Laetitia
L
Commissariat à l'Energie Atomique, Institut de Biologie et Tecnologies de Saclay, Service de Biologie Intégrative et Génétique Moléculaire, CEA Saclay F-91191 Gif sur Yvette CEDEX, France. Laetitia.Houot@childrens.harvard.edu
Floutier
Martin
M
Marteyn
Benoit
B
Michaut
Magali
M
Picciocchi
Antoine
A
Legrain
Pierre
P
Aude
Jean-Christophe
JC
Cassier-Chauvat
Corinne
C
Chauvat
Franck
F
D053502:Arsenate Reductases / Q000502:physiology; D001426:Bacterial Proteins / Q000378:metabolism*; D002104:Cadmium / Q000633:toxicity*; D020869:Gene Expression Profiling; D015964:Gene Expression Regulation, Bacterial / Q000187:drug effects; D006706:Homeostasis / Q000187:drug effects / Q000235:genetics; D006861:Hydrogen Peroxide / Q000494:pharmacology; D007501:Iron / Q000378:metabolism; D053858:Metabolic Networks and Pathways / Q000187:drug effects* / Q000235:genetics; D008670:Metals / Q000378:metabolism; D050296:Microbial Viability / Q000187:drug effects; D009584:Nitrogen / Q000378:metabolism; D020411:Oligonucleotide Array Sequence Analysis; D010100:Oxygen / Q000494:pharmacology; D010788:Photosynthesis / Q000187:drug effects / Q000235:genetics; D011499:Protein Processing, Post-Translational / Q000187:drug effects; D046939:Synechocystis / Q000187:drug effects* / Q000235:genetics / Q000378:metabolism*; D013997:Time Factors; D014158:Transcription, Genetic / Q000187:drug effects
D001426:Bacterial Proteins; D008670:Metals; C109473:orange carotenoid protein, Synechocystis; D002104:Cadmium; D006861:Hydrogen Peroxide; D007501:Iron; D053502:Arsenate Reductases; D009584:Nitrogen; D010100:Oxygen