Modulation of Metabolism and Switching to Biofilm Prevail over Exopolysaccharide Production in the Response of Rhizobium alamii to Cadmium
et al. (2011) Modulation of Metabolism and Switching to Biofilm Prevail over Exopolysaccharide
Production in the Response of Rhizobium alamii to Cadmium. PLoS ONE 6(11): e26771. doi:10.1371/journal.pone.0026771
Modulation of Metabolism and Switching to Biofilm Prevail over Exopolysaccharide Production in the Response of Rhizobium alamii to Cadmium
Mathieu Schue 0 1
Agnes Fekete 0 1
Philippe Ortet 0 1
Catherine Brutesco 0 1
Thierry Heulin 0 1
Philippe Schmitt-Kopplin 0 1
Wafa Achouak 0 1
Catherine Santaella 0 1
Paul Cobine, Auburn University, United States of America
0 a Current address: CNRS, UPR 9025, Lab Enzymologie Interfaciale et Physiologie de la Lipolyse , Marseille, France b Current address: CEA, DSV, IBEB , Laboratoire de Bioe nerge tique Cellulaire , Saint-Paul-lez-Durance , France
1 1 CEA, Lab Ecol Microbienne Rhizosphere & Environm Extre , iBEB, DSV, Saint-Paul-lez-Durance, France, 2 CNRS , Unite Mixte Rech Biol Vegetale & Microbiol Enviro, UMR 6191 , Saint-Paul-lez-Durance , France , 3 Universite Aix Marseille , Saint-Paul-lez-Durance , France , 4 Helmholtz-Zentrum Muenchen-German Research Center for Environmental Health, Institute for Ecological Chemistry, Department of BioGeochemistry and Analysis , Neuherberg, Germany , 5 Department for Chemical-Technical Analysis Research Center Weihenstephan for Brewing and Food Quality, Technische Universita t M u nchen , Freising-Weihenstephan , Germany
Heavy metals such as cadmium (Cd2+) affect microbial metabolic processes. Consequently, bacteria adapt by adjusting their cellular machinery. We have investigated the dose-dependent growth effects of Cd2+ on Rhizobium alamii, an exopolysaccharide (EPS)-producing bacterium that forms a biofilm on plant roots. Adsorption isotherms show that the EPS of R. alamii binds cadmium in competition with calcium. A metabonomics approach based on ion cyclotron resonance Fourier transform mass spectrometry has showed that cadmium alters mainly the bacterial metabolism in pathways implying sugars, purine, phosphate, calcium signalling and cell respiration. We determined the influence of EPS on the bacterium response to cadmium, using a mutant of R. alamii impaired in EPS production (MSDGT). Cadmium dosedependent effects on the bacterial growth were not significantly different between the R. alamii wild type (wt) and MSDGT strains. Although cadmium did not modify the quantity of EPS isolated from R. alamii, it triggered the formation of biofilm vs planktonic cells, both by R. alamii wt and by MSDGT. Thus, it appears that cadmium toxicity could be managed by switching to a biofilm way of life, rather than producing EPS. We conclude that modulations of the bacterial metabolism and switching to biofilms prevails in the adaptation of R. alamii to cadmium. These results are original with regard to the conventional role attributed to EPS in a biofilm matrix, and the bacterial response to cadmium.
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The exposure of bacterial cells to heavy metals in their
environment mediates biological effects, usually through the direct
or indirect action of reactive oxygen species [1,2]. In fact,
nonredox-reactive metals, such as cadmium, show a high degree of
reactivity towards sulfur, nitrogen and oxygen atoms in
biomolecules. Cadmium may bind sulfur in essential enzymes, and alter
their functions. Many studies have focused on the molecular
mechanism of bacterial cell tolerance to cadmium, mainly for the
case of species that are resistant to high metal concentrations, such
as Stenotrophomonas [3] or Cupriavidus metallidurans (review in [4]).
However, cadmium concentrations and its availability in metal
contaminated soils are generally low. At low cadmium
concentrations, Dedieu et al. [5] studied the interactions of Sinorhizobium
meliloti extracellular compounds on cadmium speciation and
availability, and Page`s et al. [6] reported on the completely
different adaptation mechanisms of phenotypic variants of
Pseudomonas brassicacearum in the presence of cadmium. Varied
mechanisms account for cadmium detoxication in bacteria,
involving exclusion, binding and sequestration. Cadmium is
removed from cells by metal efflux transporters [7,8,9], reduced
as cadmium sulfide [10], precipitated as insoluble salts [11],
immobilized within the cell walls [12], or linked to chelating agents
[13,14]. Cell exudates, such as proteins, siderophores and to a
minor extent polysaccharide, play a role in the short-term
interaction between Sinorhizobium meliloti and cadmium [5,15].
Because the adsorption of cadmium as well as of other metals
can be associated with the secretion of exopolysaccharide (EPS) or
capsular material [2,16,17], EPSs are considered as potential
metal transporters in soil [18,19].
Gram-negative soil bacteria belonging to the commonly named
rhizobia are able to produce EPSs with a large diversity of
chemical structures [20,21]. These EPSs are the main contributors
in legume-rhizobia interactions, leading to nodulation and
nitrogen fixat (...truncated)