Abstract
Co-contamination of metals and organic pollutants is a global problem as metals interfere with the metabolism of complex organics by bacteria. Based on a prior observation that metal tolerance was altered by the sole carbon source being used for growth, we sought to understand how metal toxicity specifically affects bacteria using an organic pollutant as their sole carbon source. To this end metabolomics was used to compare cultures of Pseudomonas pseudoalcaligenes KF707 grown on either biphenyl (Bp) or succinate (Sc) as the sole carbon source in the presence of either aluminum (Al) or copper (Cu). Using multivariate statistical analysis it was found that the metals caused perturbations to more cellular processes in the cultures grown on Bp than those grown on Sc. Al induced many changes that were indicative of increased oxidative stress as metabolites involved in DNA damage and protection, the Krebs cycle and anti-oxidant production were altered. Cu also caused metabolic changes that were indicative of similar stress, as well as appearing to disrupt other key enzymes such as fumarase. Additionally, both metals caused the accumulation of Bp degradation intermediates indicating that they interfered with Bp metabolism. Together these results provide a basic understanding of how metal toxicity specifically affects bacteria at a biochemical level during the degradation of an organic pollutant and implicate the catabolism of this carbon source as a major factor that exacerbates metal toxicity.
Highlights
Anthropogenic pollution in the form of organic compounds and metal elements is widespread around the globe (Darnault et al, 2005; Zalasiewicz et al, 2011)
Compared to other metals and bacteria, P. pseudoalcaligenes KF707 was found to be more sensitive to Cu and aluminum (Al; Tremaroli et al, 2010) but was able to tolerate higher concentrations of these metals when grown on succinate (Sc) compared to Bp (Booth et al, 2013a)
Culture Growth Pseudomonas pseudoalcaligenes KF707 was routinely cultured in minimal salts medium (MSM) consisting of K2HPO4, 4.4; KH2PO4, 1.7; (NH4)2SO4, 2.6; MgSO4·7H2O, 0.4; CaSO4·2H2O, 0.0031; MnSO4·H2O, 0.05; FeSO4·7H2O, 0.1 (Tremaroli et al, 2010)
Summary
Anthropogenic pollution in the form of organic compounds and metal elements is widespread around the globe (Darnault et al, 2005; Zalasiewicz et al, 2011). Compared to other metals and bacteria, P. pseudoalcaligenes KF707 was found to be more sensitive to Cu and aluminum (Al; Tremaroli et al, 2010) but was able to tolerate higher concentrations of these metals when grown on succinate (Sc) compared to Bp (Booth et al, 2013a) Both of these metals have been found in co-contamination with polycyclic aromatic hydrocarbons and polychlorinated biphenyls (Allen, 2008; Burgess et al, 2009; Renzi et al, 2009; Jartun and Pettersen, 2010; Annicchiarico et al, 2011; Hassanvand et al, 2015) especially in electronic waste (Robinson, 2009; Fornalczyk et al, 2013; Liu et al, 2013; Itai et al, 2014; Pradhan and Kumar, 2014) their mechanisms of toxicity have been characterized in other systems (Macomber et al, 2007; Macomber and Imlay, 2009; Lemire et al, 2010; Mailloux et al, 2011) and are physicochemically very distinct from one-another (Lemire et al, 2013). These insights into the physiological effects of metal toxicity in an environmentally isolated bacterium should provide a basis for further investigations into the biochemical mechanisms of how metal toxicity disrupts the metabolism of complex aromatic substrates
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