Cu(II) adsorption onto ammonia-oxidizing bacteria and archaea

Nitrogen cycling is dependent on ammonia-oxidizing bacteria and archaea transforming ammonia to nitrite. Copper is an essential cofactor for ammonia monooxygenase in ammonia-oxidizing archaea and bacteria. Copper is also essential for several electron carriers in ammonia-oxidizing archaea. Hence, copper acquisition is a critical step for complete enzyme maturation and metabolic function. In this work, we describe copper adsorption onto the bacterial species Nitrosococcus oceani C-107 (N. oceani) and Nitrosomonas europaea C-31 (N. europaea) and archaeal species Nitrosopumilus maritimus SCM1 (N. maritimus). Surface complexation models described copper adsorption onto bacterial species with one reaction, while N. maritimus required two reactions to adequately describe adsorption. Enthalpies of copper adsorption derived from isothermal titration calorimetry combined with surface complexation modeling revealed slightly exothermic enthalpies for N. maritimus and thermoneutral to endothermic enthalpies for the bacterial species. Entropies of copper adsorption were positive and indicative of entropy-driven inner-sphere complexation reactions. Thermodynamic parameters describing copper adsorption onto N. maritimus are consistent with adsorption onto a mixture of phosphorous-bearing anionic oxygen and thiol ligands. Thermodynamic parameters describing Cu(II) adsorption onto N. oceani and N. europaea were consistent with Cu(II) adsorption onto phosphorous-bearing anionic oxygen ligands. Modeling competitive copper complexation between N. maritimus and two organic acids, to mimic dissolved organic carbon, showed that N. maritimus could compete with nitrilotriacetic acid and triethylenetetramine under conditions similar to experimental measurements of copper adsorption. These results suggest that selectivity of the N. maritimus surface may confer some advantage in low-copper environments.