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Use of an Artificial Miniaturized Enzyme in Hydrogen Peroxide

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Use of an Artificial Miniaturized Enzyme in Hydrogen Peroxide sensors Letter Use of an Artificial Miniaturized Enzyme in Hydrogen Peroxide Detection by Chemiluminescence Gerardo Zambrano , Flavia Nastri , Vincenzo Pavone , Angela Lombardi and Marco Chino * Department of Chemical Sciences, University of Naples “Federico II”. Via Cintia, 80126 Napoli, Italy; [email protected] (G.Z.); fl[email protected] (F.N.); [email protected] (V.P.); [email protected] (A.L.) * Correspondence: [email protected]; Tel.: +39-081-674421 Received: 25 May 2020; Accepted: 3 July 2020; Published: 6 July 2020 Abstract: Advanced oxidation processes represent a viable alternative in water reclamation for potable reuse. Sensing methods of hydrogen peroxide are, therefore, needed to test both process progress and final quality of the produced water. Several bio-based assays have been developed so far, mainly relying on peroxidase enzymes, which have the advantage of being fast, efficient, reusable, and environmentally safe. However, their production/purification and, most of all, batch-to-batch consistency may inherently prevent their standardization. Here, we provide evidence that a synthetic de novo miniaturized designed heme-enzyme, namely Mimochrome VI*a, can be proficiently used in hydrogen peroxide assays. Furthermore, a fast and automated assay has been developed by using a lab-bench microplate reader. Under the best working conditions, the assay showed a linear response in the 10.0–120 µM range, together with a second linearity range between 120 and 500 µM for higher hydrogen peroxide concentrations. The detection limit was 4.6 µM and quantitation limits for the two datasets were 15.5 and 186 µM, respectively. In perspective, Mimochrome VI*a could be used as an active biological sensing unit in different sensor configurations. Keywords: luminescence; hydrogen peroxide; heme proteins; artificial metalloenzymes; luminol 1. Introduction According to the United Nations (UN) and World Health Organization (WHO) reports about the consequences of climate change, extreme weather events and variable climates are affecting food and water supplies [1,2]. Moreover, free access to drinking water is considered a fundamental and universal human right [3]. In this context, water reclamation for potable reuse is nowadays considered a necessary approach to face near-future water scarcity. Among the chemical, physical, and biological treatments to which reclaimed water must be subjected, advanced oxidation processes (AOPs), coupling either UV irradiation or ozonation in the presence of hydrogen peroxide, are effective both in microbial sterilization and organic pollutant oxidative degradation [4–6]. Hydrogen peroxide determination is, therefore, crucial in: (i) Assessing the undesired residual peroxide concentration of the final treated water; (ii) monitoring, hopefully on a real-time basis, the process performance; (iii) tuning the reagent amount in order to get the best results in terms of its ecological and economic costs. The determination of hydrogen peroxide is a historically fervent research field, as its concentration in solution is directly or indirectly related to the activity of several enzymes [7,8]. Many bio-based assays have been developed with potential food, clinical, and biotechnological applications [9–33]. Different techniques may be coupled to these assays, such as spectrophotometry [9], fluorimetry [10,11], electrochemistry [12–17], and chemiluminescence (CL) [18–33], giving rise to a wide spectrum of sensitivities and variable ranges of detection. CL offers several advantages, such as the use of very Sensors 2020, 20, 3793; doi:10.3390/s20133793 www.mdpi.com/journal/sensors SensorsSensors2020 2020,,20 20,, 3793x FOR PEER REVIEW 22 ofof 1414 a wide spectrum of sensitivities and variable ranges of detection. CL offers several advantages, such sensitiveas the use and of very miniaturized sensitive and detectors, miniaturized from lab dete benchctors, PMT from detectorslab bench to PMT smartphone detectors CCDto smartphone cameras, andCCD the cameras, almost and complete the almost absence complete of background absence of signal background [8]. To thissignal aim, [8]. luminol To this hasaim, beenluminol widely has preferredbeen widely over preferred other CL over reagents other thanks CL reagents to its high thanks quantum to its yield, high enabling quantum the yield, detection enabling of trace the amountsdetection of of materials trace amounts [7,23–28 of,34 materials]. Upon oxidation, [7,23–28,34]. luminol Upon (LH oxidation,2) develops luminol blue light (LH with2) develops an emission blue maximumlight with an at 425emission nm. Severalmaximum oxidation at 425 nm. conditions Several haveoxidation been conditions reported in have the literature,been reported involving in the eitherliterature, catalyzed involving activation either ofcatalyzed hydrogen activation peroxide of in hydrogen alkaline medium,peroxide orin inalkaline situ formation medium, of or singlet in situ 1 1 dioxygenformationspecies of singlet ( O 2dioxygen)[26,35–38 species]. Biomolecule-based ( O2) [26,35–38]. activation Biomolecule-based of hydrogen activation peroxide of has hydrogen several advantagesperoxide has over several other advantages methods, it over is generally other methods, highly selective it is generally and effi highlycient, the selective catalyst and can efficient, be recycled, the andcatalyst the usecan ofbe toxic recycled, reagents and is the avoided use of [ 22toxic–25 ].reag Horseradishents is avoided peroxidase [22–25]. (HRP) Horseradish catalyzes peroxidase hydrogen peroxide(HRP) catalyzes activation hydrogen and further peroxide oxidation activation of luminol, and further thus generating oxidation a of moderately luminol, thus high generating and durable a luminescencemoderately high signal and (LS). durable The mechanismluminescence of luminolsignal (LS). oxidation The mechanism by HRP has of beenluminol studied oxidation in detail by andHRP involves has been several studied steps in detail before and light involves emission several [37,39 steps–44]. before First, hydrogenlight emission peroxide [37,39–44]. induces First, the formationhydrogen ofperoxide the high induces oxidation the state formation compound of the I (C-I)high intermediateoxidation state (Scheme compound1; step I 1),(C-I) which, intermediate in turn, oxidizes(Scheme two I; step equivalents 1), which, of luminol,in turn, inoxidizes the deprotonated two equivalents form LH of— luminol,under alkaline in the conditions,deprotonated through form theLH— formation under alkaline of the compoundconditions, IIthrough (C-II) intermediate the formation (Scheme of the1 ;compound steps 2–3). II Subsequently, (C-II) intermediate rapid dismutation(Scheme I; steps of the 2–3). early Subsequently produced radical, rapid species dismutation yields the of fullythe early oxidized produced diazaquinone radical species (L; Scheme yields1; stepthe fully 4). Finally, oxidized an uncatalyzed diazaquinone coupling (L; scheme between I; step a second 4). Finally, equivalent an uncatalyzed of H2O2 and coupling L takes place between in the a rate-limitingsecond equivalent step, whichof H2O gives2 and rise L takes to dinitrogen place in the release rate-limiting and formation step, which of 3-aminophtalate gives rise to dinitrogen (3-AP) in anrelease excited and triplet formation state (Schemeof 3-aminophtalate1; step 5). Intersystem (3-AP) in crossingan excited then triplet leads state to the (scheme decay toward I; step the 5). emissiveIntersystem singlet crossing state. then leads to the decay toward the emissive singlet state. HRP + H2O2 C-I + H2O (step 1) C-I + LH— C-II + LH•— (step 2) C-II + LH— HRP + LH•— (step 3) 2 LH•— L + LH2 (step 4) L + H2O2 3-AP + N2 + hν (step 5) SchemeScheme 1.I. Mechanism of horseradish peroxidase-catalyzed luminolluminol oxidation by hydrogen peroxide, and subsequent luminescence. and subsequent luminescence. SuitabilitySuitability ofof thethe HRPHRP/luminol/luminol reactionreaction systemsystem inin thethe determinationdetermination ofof hydrogenhydrogen peroxideperoxide hashas beenbeen recognized many many years years ago ago [18]. [18 Both]. Both batch batch and andflow flowassays assays have been have developed, been developed, even though even thoughonly a limited only a limitedresponse, response, in terms in of terms linearity of linearityrange and range limit and of detection limit of detection (LOD), could (LOD), be couldachieved be achieved[9,21–25]. [ 9A,21 –substantial25]. A substantial upgrade upgrade of the of sensin the sensingg capacity capacity was was accomplished accomplished both both by by enzymeenzyme immobilizationimmobilization onto onto di differentfferent matrices matrices and and by by LS LS enhancers enhancers [9, 22[9,22–25,45,46].–25,45,46]. LS LS could could be modulatedbe modulated by theby the presence presence of di offf differenterent organic organic molecules molecules (generally (generally aromatic), aromatic), detergents, detergents, and and metal metal ions, ions, both both in thein the enhancement enhancement and and in the in suppressionthe suppression of the of emitted the emitted light, allowinglight, allowing the determination the determination of several of analytesseveral analytes [23–25]. [23–25]. Finally, bi-enzymaticFinally, bi-enzymatic sensors could sensors be could developed be developed by coupling by coupling HRP/luminol HRP/luminol LS either toLS H either2O2-dependent to H2O2-dependent enzymes, asenzymes, glucose as oxidase glucose (GOx) oxidase enzyme (GOx) for
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