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Extracellular enzymes are master recyclers of organic matter, and to predict their functional lifetime, we need to understand their environmental transformation processes. In surface waters, direct and indirect photochemical transformation is a known driver of inactivation. We investigated molecular changes that occur along with inactivation in aminopeptidase, an abundant class of extracellular enzymes. We studied the inactivation kinetics and localized oxidation caused by singlet oxygen, 1 O 2 , a major photochemically derived oxidant toward amino acids. Aminopeptidase showed second-order inactivation rate constants with 1 O 2 comparable to those of free amino acids. We then visualized site-specific oxidation kinetics within the three-dimensional protein and demonstrated that fastest oxidation occurred around the active site and at other reactive amino acids. However, second-order oxidation rate constants did not correlate strictly with the 1 O 2 -accessible surface areas of those amino acids. We inspected site-specific processes by a comprehensive suspect screening for 723,288 possible transformation products. We concluded that histidine involved in zinc coordination at the active site reacted slower than what was expected by its accessibility, and we differentiated between two competing reaction pathways of 1 O 2 with tryptophan residues. This systematic analysis can be directly applied to other proteins and transformation reactions.

Inactivation and Site-specific Oxidation of Aquatic Extracellular Bacterial Leucine Aminopeptidase by Singlet Oxygen