Fast and Sensitive Detection of Paramagnetic Species Using Coupled

Research Article Cite This: ACS Appl. Mater. Interfaces 2019, 11, 24412−24422

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Fast and Sensitive Detection of Paramagnetic Species Using Coupled Charge and Spin Dynamics in Strongly Fluorescent Nanodiamonds F. Gorrini,*,† R. Giri,† C. E. Avalos,‡ S. Tambalo,† S. Mannucci,§ L. Basso,†,∥ N. Bazzanella,∥ C. Dorigoni,† M. Cazzanelli,†,∥ P. Marzola,⊥ A. Miotello,∥ and A. Bifone†,# †

Center for Neuroscience and Cognitive Systems, Istituto Italiano di Tecnologia, Corso Bettini 31, Rovereto, 38068 Trento, Italy Institut des Sciences et Ingénierie Chimiques, Ecole Polytechnique Fédérale de Lausanne (EPFL), Batochime, CH-1015 Lausanne, Switzerland § Department of Neuroscience, Biomedicine and Movement Sciences, University of Verona, Strada Le Grazie 8, 37134 Verona, Italy ∥ Department of Physics, University of Trento, via Sommarive 14, Povo, 38123 Trento, Italy ⊥ Department of Computer Science, University of Verona, Strada Le Grazie 15, 37134 Verona, Italy # Department of Molecular Biotechnology and Health Sciences, University of Torino, Torino 10126, Italy

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‡

S Supporting Information *

ABSTRACT: Sensing of a few unpaired electron spins, such as in metal ions and radicals, is a useful but difficult task in nanoscale physics, biology, and chemistry. Single negatively charged nitrogen-vacancy (NV−) centers in diamond offer high sensitivity and spatial resolution in the optical detection of weak magnetic fields produced by a spin bath but often require long acquisition times on the order of seconds. Here, we present an approach based on coupled spin and charge dynamics in dense NV ensembles in strongly fluorescent nanodiamonds (NDs) to sense external magnetic dipoles. We apply this approach to various paramagnetic species, including gadolinium complexes, magnetite nanoparticles, and hemoglobin in whole blood. Taking advantage of the high NV density, we demonstrate a dramatic reduction in acquisition time (down to tens of milliseconds) while maintaining high sensitivity to paramagnetic centers. Strong luminescence, high sensitivity, and short acquisition time make dense NV− ensembles in NDs a potentially promising tool for biosensing and bioimaging applications. KEYWORDS: nitrogen-vacancy centers, nanodiamonds, spin relaxation, charge dynamics

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schemes without the need to manipulate the NV− spin states with microwaves, which are strongly absorbed by biological samples. Denser ensembles of NV centers may be desirable to increase the signal-to-noise (SNR) ratio in photon detection and to reduce measurement time while retaining high spatial resolution, thus making these promising techniques viable for routine application in biomedicine. However, high concentrations of NVs, defects, and substitutional impurities may favor interconversion between the negative and the neutral charge states of NV centers.27−29 Recently, longitudinal spin relaxation was investigated in strongly fluorescent bulk diamonds containing a high concentration of nitrogen defects (200 ppm) and NV centers (10 ppm).30 The evolution of the fluorescence (FL) signal in this regime showed complex behavior, reflecting the interplay

INTRODUCTION Negatively charged nitrogen-vacancy (NV−) centers in diamond have been extensively used to measure magnetic fields,1−3 electric fields,4−6 and as temperature sensors7,8 at the nanoscale. Owing to their biocompatibility and ease of functionalization, fluorescent nanodiamonds (NDs) are promising as optical imaging probes for biological applications,9 such as in vivo tracking,10,11 magnetic imaging,12,13 and nanothermometry.14,15 More recently, diamond-based nanosensors have been proposed for detection of magnetic dipole interactions by measuring the effects of fluctuating magnetic fields generated by electron spins on the longitudinal spin relaxation time (T1) of NV centers.16 Detection of paramagnetic gadolinium,17−21 manganese,22 superparamagnetic nanoparticles,23 ferritin proteins,22,24,25 and ferromagnetic nanoparticles26 has been demonstrated using single or dilute ensembles of NVs in diamond. Unlike coherent detection methods normally applied for magnetometry, relaxometric measurements can be performed with all-optical detection © 2019 American Chemical Society

Received: April 2, 2019 Accepted: June 14, 2019 Published: June 14, 2019 24412

DOI: 10.1021/acsami.9b05779 ACS Appl. Mater. Interfaces 2019, 11, 24412−24422

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ACS Applied Materials & Interfaces

Figure 1. Time evolution of FL as a function of dark time and amount of gadoteridol. (a) Pulse sequence consists of an initializing pulse, a variable dark time τ, and a probing pulse. The initializing pulse polarizes part of the NV centers and ionizes other NV centers. Then, during the dark time, the spin system relaxes and recharge takes place. The probing pulse detects the FL level after a time τ. Evolution of FL in the dark from samples containing (2.2 ± 0.1) × 109 NDs without the Gd complexes and with intermediate and high amounts of Gd complexes (as indicated by the ratio NGd/NNDs) is reported in (b), (c), and (d), respectively. The data were fitted with the function described by eq 1 (blue curves). The FL decay and rise are attributed to spin and charge dynamics, respectively. For the highest amounts of Gd, a complete inversion of the FL evolution curve is observed, as the dynamics become dominated by recharging in the dark.

Figure 2. Parameters extracted from the fit of FL decay curves. (a) Longitudinal spin relaxation time is plotted as a function of the amount of deposited Gd, for U40 and U100 NDs. The black square on the y-axis indicates the baseline T1 of NV centers in NDs without Gd, very similar for both types of NDs. The characteristic time for recharge is assumed to be constant throughout the range of NGd/NNDs considered here. Relaxing this assumption does not qualitatively change the results (see the Discussion section). The solid curves represent the theoretical dependence of T1 on Gd amount calculated from eq 2 and describe accurately the behavior at low amounts of Gd. At higher amounts of Gd, however, the theoretical predictions deviate slightly from the best evolution profile (dashed curves), probably because of a simplified theoretical model. (b) Position of the minimum of FL depends on the amount of gadoteridol and can be used in addition to T1 to estimate the average number of paramagnetic gadoteridol molecules per nanodiamond. Dashed curves are guides for the eye. Mixing between gadoteridol and NDs was not uniform, so reported values in (a) and (b) are averaged over 10−20 acquisitions, and standard deviation sets the error bars. (c, d) Optically detected magnetic resonance (ODMR) spectra of U100 NDs and U40 NDs with and without Gd. With high Gd amounts, FL contrast is drastically reduced, indicative of a low level of spin polarization achieved by the preparation pulse, a consequence of the fast T1 relaxation induced by paramagnetic interactions.

between two different mechanisms involving spin and charge dynamics.30,31 Indeed, optical irradiation can induce polarization of the electron spin state of NV− centers as well as charge state conversion.27,29,32−37 Whether effective sensing of magnetic interactions can be performed in a regime of intense charge conversion, however, remains unclear. Here, we study the effect of fluctuating magnetic noise in the gigahertz (GHz) frequency range, induced by paramagnetic agents, on spin and charge dynamics in fluorescent NDs with dense NV ensembles. We exploit these complex dynamics for sensing magnetic dipolar interaction with (a) gadoteridol, a paramagnetic chelate complex of Gd3+ widely used as a contrast agent for diagnostic magnetic resonance imaging; (b) magnetosomes (MNs),38,39 superparamagnetic nanostructures of magnetite naturally synthesized by magnetotactic bacteria; (c) blood, containing paramagnetic deoxygenated hemoglobin. We demonstrate detection of few tens of Gd spins per nanodiamond. Moreover, exploiting the high NV density, we introduce single-point detection schemes that enable detection

of variations in spin density with ultrashort acquisition times of few tens of milliseconds.

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RESULTS We used three types of highly fluorescent NDs (BikantaBerkeley, CA): unfunctionalized NDs with nominal diameters of 100 and 40 nm, and 100 nm NDs coated with a 10 nm layer of silica (labeled as U100, U40, and SC100, respectively). All samples have a high concentration of NV centers (about 5 ppm) with short coherence time (T*2 ) in the range of 50−80 ns (see Table S1 in Supporting Information). In Figure 1a, we present the pulse sequence used to measure the longitudinal spin relaxation dynamics. The ground state of the NV center is a spin triplet, with the ms = ±1 levels upshifted by 2.87 GHz (the zero-field splitting, ZFS) with respect to the ms = 0 level. The first 532 nm laser pulse (1 ms, 2 mW) preferentially populates the ms = 0 level through a spin-dependent transition from the excited state through the metastable singlet states.40 As a consequence, the fluorescence of the ms = ±1 levels is 24413


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and α and β are pre-exponential coefficients. The stretching exponents n and m account for the distribution of spin relaxation times T1 and recharge times Tr, respectively, in the ensemble of NV centers. The two pre-exponential coefficients α and β depend on the relaxation mechanisms as well as on the laser pulse parameters (see the Supporting Information for more details). The coefficient β is related mainly to the degree of polarization of the ms = 0 state, which becomes preferentially populated upon laser irradiation, while α has a more complex dependence on the competing processes of ionization and polarization during the initialization laser pulse. The dynamics of spin and charge are coupled in the sense that both contribute to the definition of α and β. Since the fluorescence measurements are performed on ensembles of NVs, all of the parameters of eq 1 are mean values. In particular, T1 is an effective value of the longitudinal spin relaxation time (a full derivation can be found in the Supporting Information). Fit curves described by eq 1 are shown in blue color in Figure 1b−d. The longitudinal relaxation time T1 was thus extracted and plotted in Figure 2a for the U100 NDs (in blue) and for the U40 NDs (in pink). The T1 and all of the relevant parameters are expressed as a function of NGd/NNDs. Optimal fits were obtained for n in the range 0.5−1.0. For both ND types, T1 decreased by 2 orders of magnitude, from 400−450 μs (black square on the y-axis) to 1−5 μs, with NGd/NNDs increasing from few tens to few millions. Shortening of T1 can be attributed to high-frequency magnetic noise17−21 produced by the fluctuating spin bath of Gd ions that induces transitions between the ms = 0 and ms = ±1 levels. If the Gd−Gd interaction is of dipolar type, the relation between T1 and the bath parameters is17−19

lower than that of the ms = 0 level. In the variable dark time τ, the system relaxes toward the equilibrium condition. The characteristic time scale for this mechanism is known as the longitudinal spin relaxation time (T1). Mechanisms that are known to influence T1 are interactions with phonons,41 NV− NV dipolar coupling,42,43 and surface charges.19,44 In addition to these mechanisms, the T1 of NV centers can also be affected by a spin bath, inducing magnetic fluctuations resonant with the |0⟩ ↔ | ± 1⟩ transitions.45 The second laser pulse of much shorter duration (1 μs) was used to read out the remaining spin polarization at different τ. A reset time of about 5 ms was applied to allow the system to reach charge equilibrium before another pumping pulse was applied. The pulse sequence involved only laser light irradiation, and no microwaves were applied. In Figure 1b, we show the exponential decay profile of the fluorescence from the U100 NDs. We measured T1 ≈ 0.41 ms, slightly shorter than in bulk diamond samples with similar concentrations of NVs.46 This originates from interaction with surface spins (unpaired electron spins in dangling bonds at the surface), whose strength is larger in nanoscopic particles.19 When NDs are mixed with gadoteridol solutions (molecular structure in the inset of Figure 1d) at different concentrations and then dried on a microscope slide (see Materials and Methods), NVs close to the ND surface couple to the unpaired electrons of the Gd3+ ion via the magnetic dipole interaction. The effects of these interactions with various amounts of gadoteridol are shown in Figure 1c,d. We chose to quantify the amount of deposited Gd chelates on the dry glass slide as the ratio NGd/NNDs, where NGd is the number of gadoteridol molecules and NNDs is the number of NDs, which was kept constant, (2.2 ± 0.1) × 109. It is worth noting that the mixing between gadoteridol and NDs is not homogeneous, so the number NGd/NNDs mentioned in Figure 2 is representative of an average value. The fluorescence decay profile of NDs mixed with Gd complexes is no longer described by a simple exponential. When NGd/NNDs increases, the exponentially decaying component becomes steeper and a second growing component appears and becomes more prominent. At the highest amounts of Gd (Figure 1d), the growing component dominates the FL profile, building up with the increasing dark time. This Gd-induced behavior can be qualitatively described in terms of dynamics of spin and charge at different time scales.29,30,43 The decreasing component represents the T1 relaxation of the spin-polarized ms = 0 level. However, the preparation pulse can also affect the charge state of the NV− centers. The recovery of FL on longer time scales can be attributed to the recharge of NV0 centers in the dark, as was also observed in the case of bulk diamond.30 As T1 decreases because of strong magnetic interactions, recharging in the dark gradually dominates the evolution of the FL signal. Notably, the large number of photons emitted by these strongly fluorescent NDs make it possible to acquire the full decay curve (usually 15−20 time points) in a few tens of seconds (see Materials and Methods). To estimate the parameters pertaining to the two competing dynamics, we empirically fit the FL profile with a sum of two stretched exponentials30 m

3γe2⟨B⊥2 ⟩fGd 1 1 = 0 + 2 T1 T1 + D2 ) 2π (fGd

where D is the ZFS, T01 is the longitudinal spin relaxation time of the NV centers without Gd, ⟨B2⊥⟩ is the transverse magnetic field variance (with zero mean) produced by the paramagnetic environment, f Gd is its frequency, and γe ≈ 2π × 28 GHz/T is the electron gyromagnetic ratio. Both ⟨B2⊥⟩ and f Gd do depend on the amount of deposited gadoteridol (eq S13 in the Supporting Information). Theoretical predictions based on eq 2 are in good agreement with experimental data for smaller amounts of Gd but overestimate T1 at the highest amounts (blue and pink solid curves in Figure 2a). This might be explained when considering that the fluorescence takes the contribution of many NDs of different sizes and shapes (in fact, the laser spot size is ≈2.6 μm, much bigger than each nanodiamond), while the simplified theoretical model assumes spherical NDs of the same size, neglecting shape anisotropies and the size distribution (see Table S1 in the Supporting information). Purely magnetic noise is unlikely to affect the dynamics of electric charges (ionization and recharging of the NV− centers), and the related parameters Tr and m should not vary. We determined Tr = 3 ± 1 ms for the U100 NDs and Tr = 0.96 ± 0.05 ms for the U40 NDs, with m = 0.5 ± 0.05 for both, from statistical averaging of the fit of experimental data. Empirically, it was observed that the polarization-related coefficient β decreases slightly with increasing amounts of Gd (Figure S3 in the Supporting Information). This reduction can be explained by considering that a large number of Gd

n

I(t ) = Ieq[1 − α e−(t / Tr) + β e−(t / T1) ]

(2)

(1)

where Ieq is the equilibrium value of FL at long times (≈20 ms), Tr is the recharge time, m and n are stretching exponents, 24414


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Figure 3. FL decay profile and ODMR for U40 NDs and SC100 NDs, for comparison. The results are similar to those obtained with the U100 NDs. In particular, without gadoteridol, the spin relaxation is the only observable phenomenon (a and c), but in the presence of Gd chelates, a second component appears in the FL curve and dominates the profile at the highest amounts of Gd (b and d). A high amount of gadoteridol also decreases the level of polarization that can be achieved, thus reducing the ODMR contrast (e and f).

Figure 4. Effect of MNs on the spin and charge dynamics of U100 NDs. (a) SEM image of NDs mixed with MNs. Backscattered and secondary electrons are used to distinguish NDs (in green) from MNs (in orange). (b) Interactions with MNs induce a reduction of the ODMR contrast and (c) shortening of T1 with a gradual reversal of the FL curve, similarly to Gd. These findings corroborate the idea that the anomalous decay profile of the NV− FL originates from magnetic interactions with the paramagnetic agents.

complexes in close proximity to the NV− ensemble induce a fast depopulation of the ms = 0 level even during the initial step of laser irradiation, thus reducing the net polarization achievable by the initializing pulse for a certain laser power and pulse duration. The same phenomenon is at the basis of the striking reduction in the optically detected magnetic resonance (ODMR) contrast at the highest amounts of gadoteridol (millions of Gd complexes per ND), as shown in Figure 2c,d. In fact, the ODMR contrast is also proportional to the polarization of the ms = 0 level, and its strong reduction is once again indicative of the fast depolarization effect induced by gadoteridol.

Given the two-component nature of the FL decay curve, a minimum is attained at tmin, when the spin-related decreasing component intercepts the charge-related rising component. In Figure 2b, we show that tmin varies by 2 and 3 orders of magnitude for the U100 and U40 NDs, respectively, in the range of NGd/NNDs explored here, providing a very sensitive measure of the number of paramagnets. Importantly, the dependence of T1 on NGd/NNDs flattens out at low Gd amounts (left side of the curve in Figure 2a), limiting the sensitivity to tiny variations of NGd/NNDs. On the contrary, tmin dependence on NGd/NNDs remains linear on a log−log scale (Figure 2b). Assuming comparable error bars between T1 and tmin, this means that tmin is more sensitive than T1 to estimate 24415


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Figure 5. FL decay profile of unfunctionalized NDs mixed with blood. (a) FL decay of pure NDs, (b) NDs mixed with blood/saline solution, and (c) NDs mixed with blood/distilled water. Water is non-isotonic and induces hemolysis and release of paramagnetic deoxyhemoglobin. This leads to a further reduction of T1 compared to that in the blood/saline case. No inversion of the curve was observed under these conditions, in which the evolution of the curve is dominated by spin relaxation.

the value of NGd/NNDs, in the low-Gd-amount region. Moreover, T1 is always extracted from a fit, and its value is affected by the choice of the fitting function (e.g., simple or stretched exponentials) and fitting parameters (e.g., fixed or variable pre-exponential coefficients; see Discussion section). The fitting procedure is particularly arduous for large values of NGd/NNDs, where the spin-related curve decays rapidly. On the other hand, tmin can be determined unambiguously from experimental data even for large values of NGd/NNDs. For all of these reasons, estimates of NGd/NNDs based on tmin may prove advantageous compared to more traditional approaches based on T1 fitting. It is worth noting that the large error bars affecting some of the points depend purely on the heterogeneity of the sample when the mixing between gadoteridol and NDs is not uniform. On the contrary, the relative error in a typical FL curve is about 1% or, equivalently, the signal-to-noise ratio (SNR) is ≈100 (Figure 1b−d). For this reason, we acquired several FL decay curves for each sample and performed a statistical averaging (see Materials and Methods). Analogous experiments were performed with silica-coated NDs (SC100) to explore the effect of surface charge, attributed to a different surface termination. In these NDs, a 10 nm dielectric silica layer prevents direct chemical and charge interactions with the surface of the diamond and increases the minimum distance between the Gd chelates and the NV centers. Indeed, in addition to the known effect of magnetic noise on spin relaxation, electric noise at the surface of ND could in principle affect the charge dynamics of the NV centers and alter the evolution of the FL. However, also in this case, we observed reduced ODMR contrast and shortening of T1 with increasing amounts of Gd and an inversion of the FL profile at the largest Gd amounts (Figure 3), with no appreciable difference from the uncoated ND case. Moreover, the charge of the Gd3+ ion is compensated by the charges carried by the chelating agent, so the gadoteridol molecule is charge-neutral. The results from the silica-coated NDs support the idea that long-distance magnetic interactions dominate the

FL signal evolution and that electric noise, either from surface charges or Gd complexes, is unlikely to contribute significantly. The NV centers can also be utilized for efficient detection of superparamagnetic23,47 and ferromagnetic26 nanoparticles. We tested the effects of magnetosomes (MNs) on the spin and charge properties of the ensemble of NV centers. The MNs are nanoparticles of magnetite (Fe3O4) with an average size of 40 nm (estimated from transmission electron microscopy) and a single magnetic domain38,39 that lends superparamagnetic properties. Figure 4a shows a scanning electron microscope (SEM) false color image of U100 NDs (shown in green) mixed with MNs (shown in orange) on a silicon substrate. The ODMR spectrum shows a strong reduction in contrast and some broadening (Figure 4b). With increasing amounts of MNs, the same qualitative behavior observed with Gd emerges (Figure 4c), with faster spin relaxation and inversion of the FL profile. This effect can be explained considering that the magnetic moment of each magnetosome inverts direction over a time scale of τN, known as the Néel relaxation time, as a result of thermal fluctuations.48 The magnetic field produced by a single nanoparticle fluctuates at a rate 1 i KV yz zz = ν0 expjjj− τN k kT {

(3)

where ν0 ≈ 1 ÷ 10 GHz is the attempt frequency,49 V is the volume of a single magnetosome, and K = 1.1 × 104 Jm−3 is the anisotropy energy constant for magnetite.50 Given the exponential dependence on the volume of eq 3, the bigger MNs (>15 nm) have a slow varying magnetization that might be considered static, resulting in localized constant magnetic fields acting on the NVs and a small inhomogeneous broadening of the ODMR spectrum. However, MNs smaller than 15 nm can facilitate spin relaxation by producing a fluctuating magnetic field resonant with the NVs’ zero-field transition (2.87 GHz). In line with previous results, the NV recharge dynamics dominate at the largest amounts of the superparamagnetic agent we explored, when T1 is considerably shorter. 24416


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Figure 6. Schematics of spin and charge dynamics. (a) After the initial pulse, an NV center can be polarized or ionized. Trap states momentarily capture photoexcited electrons. During the dark time, the system evolves toward an equilibrium configuration, while spin relaxation and recharge take place. The probing pulse detects the FL level, which depends on both the remaining polarization and the absolute number of NV− after a variable dark time. (b) Selective measurement of FL from NV− and NV0 centers shows the charge state conversion due to recharging in the dark.

proceeds from NV− to NV0 during the dark time (in the absence of any optical or thermal excitation). Tunneling29,30,43,56 is the suggested mechanism for the charge state conversion during the dark time. Thus, in these cases, the charge dynamics leads to a reduction in the number of NV− centers in the dark and to a decrease of the charge-related component of the FL, a feature which is often mistaken as a T1 relaxation. In our samples, we observed the opposite behavior, with an increase in FL during the dark time when the dynamics are charge-dominated. This behavior suggests that electrons are transferred from NV− to neighboring charge-trapping defects via laser-induced ionization30,36 and from the defects back to the NV0 via tunneling during the dark time, for all of the three types of NDs. Similar behavior was reported in bulk diamond by our group30,31 and also observed by Mrózek et al.42 We note that in the NDs used for the present study, as well as in the bulk diamond samples investigated by Giri and Mrózek, the density of NV centers was larger (2−40 ppm) than in previous reports. Under these conditions, it has been hypothesized that tunneling-mediated charge transfer may be responsible for the NV− replenishment30 and might explain the rising component of FL during the dark time (Figure 1c,d). The two alternative paths of charge dynamics (ionization/ recharge) and spin dynamics (polarization/relaxation) are indicated in the scheme of Figure 6a. This hypothesis is also supported by experimental data. With an appropriate combination of bandpass filters, we recorded the FL of NV− centers (750−800 nm range) and NV0 centers (550−600 nm range), at the same point on the sample and under the same laser initialization conditions (Figure 6b), for U100 NDs. Both curves, related to spin and charge dynamics, can be observed in the NV− FL, but only a single component, attributed to charge dynamics, is present in the NV0 FL. The increase in the NV− FL, due to recharge, is mirrored by a reduction in the NV0 FL, with comparable time scales of ≈2−3 ms, corroborating the picture of an NV0 → NV− charge conversion during the dark time. Finally, the NV0 FL decay rate is independent of the total number of gadoteridol molecules per ND, as opposed to the NV− FL decay rate, which does depend on the number of gadoteridol molecules. The NV− recharging in the dark is independent of the type of magnetic environment (paramagnetic ions or superparamagnetic nanoparticles), as is apparent when T1 is sufficiently short and charge dynamics dominate the signal evolution. These observations suggest that recharge is always present, but it can be revealed only when T1 and β decrease by

Finally, we tested the sensing capabilities of NV ensembles in the presence of blood, a weak paramagnetic system. Red blood cells are packed with hemoglobin, and the heme groups in the deoxygenated state are paramagnetic, with a magnetic moment of ≈5.4 μB per heme group,51,52 where μB is the Bohr magneton. Freshly drawn rat blood was mixed with heparin and diluted with either a saline solution or distilled water (see Materials and Methods). Then, U100 NDs were added to these solutions before depositing on a glass slide. While isotonic saline solution preserves the integrity of the erythrocytes, deionized water induces hemolysis and the release of hemoglobin. Hence, we could assess the effects of hemoglobin segregated in the red blood cells or dispersed in the plasma, where it could interact directly with the ND surface. The FL decay curve for the blood/water sample (Figure 5c) decays more rapidly than the same curve for the blood/saline sample (Figure 5b), suggesting a high exposure of NDs to deoxyhemoglobin, as expected. Both curves decay faster than the reference curve acquired without blood (Figure 5a). However, the second, growing component related to charge dynamics was not observed in any of the three curves. Several reasons may explain the lack of inversion of the FL curve in the presence of blood compared to the other magnetic agents investigated in this study. First, the magnetic moment of Fe2+ ions is ≈5.4 μB, slightly less than ≈7.9 μB, the value of Gd3+ magnetic moment. Second, hemoglobin is a large molecule (about 5 nm).53 By comparison, gadoteridol has a molecular size of ≈1.1 nm. The amplitude of the magnetic noise increases with the magnetic moment and decreases with distance, so Fe2+ ions are farther and cannot produce the same noise amplitude on the NVs. Third, no strong dipolar coupling among Fe2+ ions is expected,51,52 so the noise spectral density at 2.87 GHz should be lower compared to that in the Gd3+ case. Finally, deoxygenated, paramagnetic hemoglobin is a small fraction of the total hemoglobin, which is prevalently in the oxygenated diamagnetic form.54 Sample preparation and optical experiments were performed in air, and hemoglobin is likely to be predominantly in the oxygenated state (>96%).

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DISCUSSION Photo-induced charge conversion from NV− to NV0 and from NV0 to NV− has been reported previously.27,55,56 Modification of the NV charge state was shown to depend on laser wavelength,33 on the distance from the surface,36 and on the presence of defects and trap states.28,29,37,56 For shallow NV centers,29,37 it has been reported that charge conversion 24417


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either T1/2 or tmin (see eqs S18 and S19 and the related text in the Supporting Information). In Figure S7 of the Supporting Information section, we plot the calculated integration time needed to detect a 50% difference in Gd concentration for various NGd/NNDs ratios. For example, using U100 NDs, a 50% variation over 106 spins per ND can be detected in ≈35 ms, using an initialization time τin of 200 μs and a readout time τro of 50 μs, with 120 iterations. Using the more sensitive U40 NDs, we calculated an acquisition time shorter than 60 ms for values of NGd/NNDs ranging from few tens to 1000. These values are unprecedently short for this kind of detection schemes.17−19,21,22 We note that a short acquisition time is possible due to the high number of detected photons from samples with high NV concentrations and by a long τro. Since the readout time for NV ensembles can be much longer compared to the one of single NVs (>10 μs in the former case30 and ≈300 ns in the latter case40), the above values lead to fast acquisition of the signal, without considerably repolarizing the NV ensemble. We also note that the inhomogeneity of the mix between gadoteridol and NDs, expressed by the error bars shown in Figure 2, does not significantly alter the picture: short acquisition times are mostly due to the change of the spin- and charge-related parameters with NGd/NNDs, which are the general features in this kind of experiments, independent of the detailed empirical fit or uncertainty of parameters in eq 1 (check for instance the drop of T1 by 2 orders of magnitude in Figure 2). In our setup, the deposited sample is exposed to air and not ideal for measurements in a liquid environment, where the solvent can evaporate during the measurement, thus affecting the concentration of the paramagnetic agent. Hence, to accurately measure the evolution of the FL over time under stable conditions, all of the samples were dried for the experiments (gadoteridol, magnetosomes, and blood). To assess whether the gadolinium-dependent interplay between spin and charge dynamics can also be detected in an aqueous solution, we exploited a fast, single-point measurement. To this end, we deposited U40 NDs on a cover glass following the same procedure described above and subsequently a drop of gadoteridol solution. Our single-point detection scheme was sufficiently fast (tens of milliseconds) to measure the instantaneous concentration without significant evaporation of the solvent during the measurement, which took place in ≈1 h (see Figure S8). Interestingly, we found that charge dynamics can dominate the evolution of the FL also in the liquid phase, when the concentration of paramagnetic species is sufficient (see the Supporting Information for further details). It is conceivable that such a fast detection scheme might serve in the future for biological applications, such as monitoring the accumulation of paramagnetic species in tissues and bodily fluids, detection of reactive oxygen species in living cells, or measurement of blood oxygenation levels. Finally, we point out that, in the interpretation of our results, we considered only the effects of external agents, without explicitly accounting for surface charges and NV−NV crossrelaxation. Surface charges are mainly due to dangling bonds with unpaired electron spins on the diamond surface. These spins provide additional magnetic noise on the NVs and a shortening of T1, which is inversely proportional to the ND size.19 Because of a large number of NDs within the laser spot size, this contribution is always averaged over NDs of different sizes and shapes, independent of NGd/NNDs. Moreover, we observed a similar T1 for the three types of NDs without Gd,

about 1 order of magnitude as a result of paramagnetic interactions. Hence, Tr was constrained when fitting the signal evolution as a function of the dark time. Conversely, the prefactor α in eq 1 was left unconstrained, since it depends on the competing processes of ionization and polarization during the initialization pulse (see the Supporting Information). Tr = 3 ± 1 ms and m = 0.5 ± 0.05 were determined from the decay of the NV0 FL and fixed when fitting the NV− experimental data. The same kind of fitting procedure was adopted for the U40 and for the SC100 NDs. Conceivably, the features of the recharge mechanism are peculiar to each sample, depending on the number of bulk and subsurface defects, with time scales ranging from few tens of microseconds to over than a week.27,29,35,36,57 In our ND samples, the recharge times of ≈1−3 ms are approximately 1 order of magnitude longer than the shortest reported.30,43 It is important to note that T1 always decreases with increasing NGd/NNDs, irrespective of the detailed structure of the fitting function. In fact, we fitted the NV− FL with two simple exponentials, where the parameters of recharge, as well as those of spin dynamics, were left free and did not see any qualitative difference with the behavior shown in Figure 2a. Because of these spin and charge dynamics, other parameters, in addition to T1, can be used for a quantitative estimate of paramagnet concentration. In Figure 2a,b, we showed that T1 and tmin decrease over the range of NGd/NNDs we explored. For the U100 NDs, both parameters drop steeply with NGd/NNDs between (5.6 ± 2.0) × 103 and (5.6 ± 1.1) × 105, with a tendency to saturate at low values. In this case, the limit of sensitivity can be taken as NGd/NNDs = 560 ± 200, or equivalently a density of 0.018 ± 0.006 spins/nm2 decorating the surface of each ND, a value comparable with previous reports.17,19,22 However, it is unlikely that all of the Gd chelates stick to the surface of NDs, and this estimate of sensitivity is very conservative. In the case of U40 NDs, the decrease of T1 and tmin is even more consistent and down to 36 ± 9 molecules of gadoteridol per ND can be detected (Figure 2). This higher sensitivity achieved with small NDs can be easily explained: in small NDs, all of the NV centers are involved in the detection, while in bigger NDs, the segregated, bulk NV centers are hardly affected by the external magnetic noise, which scales as the sixth power of the distance. As far as blood samples are concerned, if we assume that paramagnetic deoxyhemoglobin and methemoglobin are 4% of total hemoglobin, a total of 260 spins at the most can be found in the proximity of each ND. Even if this low number of spins (together with the Fe2+ magnetic moment, compared to Gd3+) is not sufficient to reveal the recharge dynamics, it can still reduce T1 by a detectable amount (Figure 5a−c). A key advantage of using dense ensembles of NDs for sensing applications is fast data acquisition. The typical acquisition time needed to measure a full curve with 20 time points and a high SNR for accurate parameter determination (≈100) is often less than 1 min, in some cases approaching a few seconds (see Materials and Methods). Ultrafast detection schemes17,18 relying on the so-called single-point detection have also been proposed. With this technique, it is possible to extract variations in the NGd/NNDs ratio by measuring the FL drop of a preferential single reference point. In the absence of charge dynamics, the optimal point17,19 is around T1/2. However, in our NDs, both the spin- and the charge-related components change with NGd/NNDs (meaning the parameters α, β, n, and T1) and the optimal point does not correspond to 24418


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Electronic) produced the desired pulsed laser sequence (Figure 1a). The same objective was then used to collect the FL signal, which was filtered and attenuated by a series of bandpass filters before reaching the detector (a single photon counter, Excelitas SPCM-AQRH-14FC). Microwaves produced by a Keysight N5171B generator were amplified and selectively pulsed with a microwave switch (MiniCircuits, ZASWA-2-50DR+). The sample sat on a custom-made copper loop, connected to the microwave line. All of the optical and microwave pulse sequences were remotely controlled by a programmable TTL pulse generator (PulseBlaster ESR-PRO, SpinCore Technologies). A data acquisition card (PCIe-6323, National Instruments) was used to record the experimental data. Optically Detected Magnetic Resonance Experiments. Continuous wave ODMR is a technique used to determine the sublevel structure of the ground state. We continuously irradiated the ND samples with the same 532 nm laser and with the same power (≈2 mW) as for the T1 experiments, to polarize the NVs into the ms = 0 state. Microwaves (500 mW) were swept from 2.8 to 2.94 GHz at 1 MHz step. When the microwaves were resonant with the ms = 0 ↔ ms = ±1 transition, which corresponds to 2.87 GHz, the ms = ±1 states are populated and a drop in the FL was recorded. We were particularly interested in measuring the reduction in the contrast with high amounts of paramagnets. This phenomenon is indicative of a low polarization of the ms = 0 level or, equivalently, a fast relaxation of the ms = 0 level induced by the magnetic noise coming from the spin bath. Experimental Acquisition Time. In the FL decay experiments, we sampled the dark time interval using Np exponentially spaced points. The initialization time τin and the readout time τro were kept constant for all of the sampling points. Then, the duty cycle time can be calculated

irrespective of the size and surface coating, suggesting that surface charges play a minor role. In fact, surface charges might only provide a substantial contribution to T1 relaxation for NDs smaller than ≈20 nm, as shown by Tetienne et al.19 Cross-relaxation is another source of T1 relaxation and involves the fast depolarization of coupled NVs in a dense ensemble.43,46 This mechanism is quenched by a static magnetic field that can remove degeneracy between differently oriented NV centers,30,42 but is hardly sensitive to the highfrequency magnetic field of a spin bath. For these reasons, any contribution to T1 from surface charges and cross-relaxation is not expected to depend on NGd/NNDs.

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CONCLUSIONS In conclusion, we investigated the spin and charge dynamics of dense ensembles of NV centers in NDs in the presence of GHz-frequency magnetic fluctuations due to external paramagnetic agents. Our results show that the changes in the FL intensity are related to two different mechanisms. The fast component, decaying with a characteristic time T1, comes from spin depolarization dynamics and is strongly influenced by the amount of magnetic noise induced by paramagnetic molecules (gadoteridol and deoxyhemoglobin) or superparamagnetic nanoparticles (magnetosomes). The slowly increasing component characterized by Tr is due to recharging in the dark. The latter mechanism is thought to be due to tunneling-mediated charge conversion29,30,43 from NV0 to NV− during the dark time, and it might be accentuated by a large number of lattice defects in these samples. Interestingly, the mechanism of recharge dominates when T1 is drastically reduced. Further, we showed that high FL and long readout times can speed up the acquisition time to few tens of milliseconds in single-point detection schemes. Additionally, the minimum of the FL profile was found to be a novel indicator of the number of paramagnets interacting with the NDs. Our results are important for understanding the fundamental physics of spin and charge dynamics of dense NV ensembles in the presence of paramagnets and for application purposes. Strongly fluorescent NDs with a short acquisition time, high magnetic field sensitivity, and long-range detection ability might find future applications in quantitative biosensing of magnetic dipolar interactions.

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Tdc = Np(τin + τro) + Tmin

Np /(Np − 1)

( ) ( ) Tmax Tmin

Tmax Tmin

1/(Np − 1)

−1 −1

(4)

where Tmin and Tmax are respectively the minimum and the maximum values of the dark time interval. The duty cycle was repeated from several hundreds to several thousands of times to increase the SNR. Typical acquisition parameters were Tmin = 1 μs, Tmax = 20 ms, Np = 20, τin = 500 μs, and τro = 5 μs, giving Tdc ≈ 49 ms. As an example, a thousand iterations of the duty cycle result in a total acquisition time of 49 s for a full curve. Preparation of the ND Mixture with Gadoteridol. The two unfunctionalized NDs were supplied in water, at a concentration of 1 mg/mL. The silica-coated NDs were supplied in ethanol, at the same concentration. Suspensions of NDs were hand-shaken and then sonicated for up to 1 h to disperse NDs. In the first experimental session, we prepared several solutions of Gd3+ complexes at different concentrations by repeated dilutions of gadoteridol (Prohance, Bracco Diagnostic Inc.; initial concentration, 0.5 M) with deionized water. At each step, the solution of gadoteridol was diluted 10-fold. Two microliters of each gadoteridol solution was mixed with 4 μL of ND suspensions (containing approximately 2 × 109 NDs). The total 6 μL of the mixture was deposited onto glass slides and left to air-dry, which results in ND deposited area of ≈2 mm diameter. The amount of deposited gadoteridol was varied from 1 pmol to 100 nmol. For each sample, FL was recorded on several (10−20) different spots. For the 40 nm NDs, we added 10 μL of ND suspensions to 10 μL of diluted Gd solutions before deposition, while 2 μL of the silica-coated NDs was first taken from the ethanol bath and mixed with 2 μL of deionized water before the same kind of processing. The distribution of NDs on the glass slide was checked with a wide-field FL microscope (Nikon Eclipse Ti-E). Since the samples were prepared by repeated dilution of a starting solution, the estimated error in the NGd/NNDs ratio is larger for more diluted samples (note the different magnitudes of the error bars on the horizontal axes in Figure 2a,b). Preparation of the ND Mixture with Magnetosomes (MNs). We mixed NDs with iron oxide magnetic nanoparticles extracted from magnetotactic bacteria, as described by Mannucci et al.38 MNs

MATERIALS AND METHODS

Samples. The NDs used for this study were obtained from Bikanta-Berkeley, CA. We acquired three different types of NDs: unfunctionalized NDs with nominal diameters of 100 and 40 nm and 100 nm NDs coated with an ≈10 nm layer of silica (labeled as U100, U40, and SC100, respectively). All samples have the same concentration of NV centers, of about 5 ppm, as reported by the vendor. We also confirmed the concentration by comparing the FL levels of NDs with those of a reference sample of known NV concentration. All of the three samples have short coherence times in the range 50−80 ns (see Table S1 in the Supporting Information). We noticed a reduction of T1 over several months, possibly an effect of sample aging. We did not characterize these effects thoroughly; however, each set of experiments was performed with the same type of NDs and within a very short period of time (hours or days max) for internal consistency. Experimental Setup. We used a home-built microscope system to study the dynamics of depolarization of NV ensembles. An objective with a numerical aperture of 0.25 (Plan N, Olympus) focused the excitation laser (532 nm, of Coherent Verdi) to a focal spot size of ≈2.6 μm. Laser power was kept in the range of 1−10 mW. An acousto-optic modulator (MT200-A0, 5-VIS, AA Opto 24419


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ACS Applied Materials & Interfaces suspended in saline buffer were precipitated and concentrated by exposing the vial to a magnetic field generated by a small permanent magnet. Different volumes (1, 2, and 4 μL) of highly concentrated nanoparticles were sampled and mixed with a 2 μL sample of 100 nm uncoated NDs. The new mixture was then deposited on a circular glass slide and allowed to dry before acquiring the FL. Part of the MN suspension was mixed with an acid, and spectroscopic analyses determined the concentration of dissolved iron. Since all of the iron was bound to oxygen in the magnetite phase (Fe3O4), from the iron (Fe) concentration it was possible to extract the number of MNs, considering a standard MN size of 40 nm. Preparation of the ND Mixture with Deoxygenated Blood and Heparin. Freshly drawn deoxygenated rat blood was collected in heparinized centrifuge tubes to avoid sample coagulation. Two microliters of blood was then mixed with either 2 μL of saline solution or 2 μL of deionized water. The mixture with water was intended to induce hemolysis and release paramagnetic deoxyhemoglobin. Then, we added 2 μL of uncoated NDs to each solution. The two liquid volumes were deposited onto glass slides and then dried, and finally, the FL decay curve was recorded.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsami.9b05779.

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Characterization of the dephasing and repolarization times of NDs, calculation of populations after the initializing pulse, the theoretical computation of T1 reduction with gadoteridol, estimate of sensitivity and acquisition time, and results of the single-point measurement in a liquid environment (PDF)

AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. ORCID

F. Gorrini: 0000-0002-6420-4104 M. Cazzanelli: 0000-0002-3182-5908 Author Contributions

A.B., F.G., R.G., and S.T. conceived the experiments. F.G. and R.G. performed the experiments, with the assistance of S.T., C.D., and M.C. in the preparation of the samples. F.G., R.G., C.E.A., and A.B. interpreted the results. S.M. and P.M. provided and characterized the magnetosomes. N.B. conducted the electron microscopy measurement. F.G. elaborated the theoretical model with the help of L.B. and A.M. F.G. wrote the manuscript with the input of R.G., C.E.A., and A.B. All of the authors reviewed the manuscript. A.B. supervised the whole project. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We gratefully acknowledge Prof. Roberto Bassi, University of Verona, for his support in the production of magnetosomes.

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REFERENCES

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