Greatly enhanced photoabsorption and photothermal conversion of

transform photo-energy to heat under light irradiation, which can induce thermal ..... large antimonene nanoflakes with spontaneously partial oxidatio...
1 downloads 0 Views 884KB Size
Subscriber access provided by UNIV OF LOUISIANA

Surfaces, Interfaces, and Applications

Greatly enhanced photoabsorption and photothermal conversion of antimonene quantum dots through spontaneously partial oxidation Xianghong Niu, Yunhai Li, Yehui Zhang, Zhaobo Zhou, and Jinlan Wang ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.9b02771 • Publication Date (Web): 26 Apr 2019 Downloaded from http://pubs.acs.org on April 26, 2019

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 20 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Applied Materials & Interfaces

Greatly enhanced photoabsorption and photothermal conversion of antimonene quantum dots through spontaneously partial oxidation Xianghong Niu1, Yunhai Li2, Yehui Zhang2, Zhaobo Zhou2 and Jinlan Wang2* 1

New Energy Technology Engineering Laboratory of Jiangsu Province & School of Science, Nanjing University of Posts and Telecommunications (NJUPT), Nanjing 210023, China 2 School of Physics, Southeast University, Nanjing 211189, China

Abstract: Two-dimensional quantum dots (2DQDs), as promising photothermal agents in photothermal therapy (PTT) to malignant tumors, have been widely studied experimentally, while the superior photoabsorption and photothermal conversion mechanisms remain unclear. In this work, we present the first excited state dynamics study on the PTT of 2D antimonene (AM) QDs by employing time-dependent density functional theory and ab initio nonadiabatic molecular dynamics calculations. Surprisingly, pristine AMQDs themselves are not good PTAs due to weak photoabsorption and low photothermal conversion performance. The superior PTT capacity of AMQDs actually derives from the spontaneously partial oxidation. The partial oxidation introduces additional band edge states, which not only broadens the optical absorption range, but also strengthens the transition dipole moment. More importantly, the oxidation doubles the non-radiative transition rate arising from the increased non-radiative coupling, which greatly promotes the release of photogenerated electron energy and accelerates the photothermal conversion efficiency. The in-depth insight unveiled here should be of fundamental importance and benefit to efficient utilization of 2DQDs in biomedical field.

ACS Paragon Plus Environment

ACS Applied Materials & Interfaces 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Keywords: antimonene quantum dots, photothermal therapy, photoabsorption, photothermal conversion, time-dependent density functional theory

Introduction Photothermal therapy (PTT), owing to its high selectivity, minimal invasiveness and low systemic side effects, has attracted enormous interest in biomedical field in the past decades.1,

2

PTT adopts optical absorbing agents, i.e., photothermal agent (PTA) to

transform photo-energy to heat under light irradiation, which can induce thermal ablation of cancer cells and therefore kill malignant tumors.3, 4 The ideal PTA should have considerable optical absorption, good photothermal conversion efficiency (PTCE) and health safety.5,

6

Conventional PTAs of inorganic semiconductor quantum dots

(QDs), such as noble-metal Au, Ag, and Cu-based materials, are linked with long-term toxicity and environmental concerns.7, 8 Organic PTAs can reduce biosafety concerns in certain degree, but most of them suffer other limitations such as complicated fabrication and indistinct degradation.9 In recent years, two-dimensional (2D) QDs, such as graphene (G) QDs,10, 11 black phosphorus (BP) QDs12-14, antimonene (AM) QDs15, exhibit good capacities for drug delivery or PTT in cancer therapy field, due to ultrahigh surface area and good photothermal effect. For example, GQDs possess good drug loading capability via π-π stacking, electrostatic attraction or physisorption,11 while BPQD and AMQD based PTAs possess high PTCE of 28.4%16 and 45.5%,15 respectively. In addition, AM-based nanomaterials have demonstrated high doxorubicin loading capacity of 150.0 % 17 and ultrasensitive detection of miRNA.18 Meanwhile, these 2DQDs are low toxic and

ACS Paragon Plus Environment

Page 2 of 20

Page 3 of 20 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Applied Materials & Interfaces

biologically friendly given that carbon provides the backbone of living matter, phosphorus is a vital biological element consisting of ~ 1% of the total weight of body,19 and antimonial drugs have been applied to medicine for several centuries.20 More interesting, 2DQD-based PTAs also have unique near-infrared (NIR) induced degradability after achieving therapeutic effects in vivo, which can be smoothly discharged from human body.15,

21, 22

Nevertheless, the mechanism of the superior

photoabsorption and photothermal conversion remains elusive. Meanwhile, it has been widely reported that oxidation is inevitable in preparation of QDs,15, 23-25 while how the oxidation influences the optical absorption or PTCE of QDs is not explored yet. In fact, PTT is a typically excited state dynamics process, the deep understanding acquires enough dynamics information on the photoabsorption and photo-thermal conversion from atomic level. In this work, we provide the first excited state dynamics study to understand the excellent performance of 2D AMQDs as PTAs for PTT by employing time-dependent density functional theory (TD-DFT) and ab initio nonadiabatic molecular dynamics (NAMD) calculations. Our computations reveal that pristine AMQDs themselves are not good PTAs due to weak photoabsorption and low photothermal conversion performance, while the spontaneously partial oxidation can remarkably improve the optical absorption and PTCE of AMQDs near NIR. The partial oxidation introduces additional band edge states, which not only provides more electronic transition channels, but also reduces the band gap, red-shifts the absorption spectra, and eventually increases the photoabsorption in NIR region. Meanwhile, the oxidation enhances the

ACS Paragon Plus Environment

ACS Applied Materials & Interfaces 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 4 of 20

non-radiative de-excitation probability via increasing the nonradiative coupling coefficient, and speeds up the release of photo-energy, which greatly improves the PTCE of pristine AMQDs.

Computational details The TD-DFT calculations were performed using the Amsterdam Density Functional program package (ADF).26, 27 The exchange-correlation interactions were treated by the Perdew-Burke-Ernzerhof (PBE)28 along with the Slater-type triple-zata plus polarization (TZP) basis set.

29

More than fifty excited states of AMQDs were taken

into account to investigate the photoabsorption property. All optimizations were done without any symmetry constraint. The dynamics of the excited electrons of QDs was obtained based on NAMD30, 31 using Hefei-NAMD code.32-35 After geometry optimization, the repeated velocity rescaling was employed to raise the temperature of system to 300 K. A 5 ps microcanonical ab initio MD trajectory was then generated using a 1 fs time step, implemented in the Vienna ab initio Simulation Package (VASP)

36, 37.

The kinetic

energy cutoff of 500 eV was adopted for plane-wave basis sets. The NAMD results were obtained by averaging over 100 different initial configurations selected from the MD trajectory based on the classical path approximation, and 2×104 trajectories were sampled for the last 4 ps for each chosen initial structure.38,

39

The vacuum space

between two adjacent QDs was set to be at least 15 Å to eliminate the interactive effect on each other.

Results and discussion

ACS Paragon Plus Environment

Page 5 of 20 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Applied Materials & Interfaces

For the most stable β-phase antimonene,23,

40, 41

each Sb atom bonds with three

adjacent Sb by sp3 hybridization, forming the buckled hexangular honeycomb atomic structure (see Figure 1a).42, 43 The edge dangling bonds are passivated by hydrogen, since H atoms are generally believed to uninvolve in photo-physics process. As a good PTA, excellent photo-absorption performance is the necessary prerequisite, especially in the infrared region. Surprisingly, the absorption spectrum of pristine AMQD only has a weak absorption peak around 2.2 eV, and the absorption range is rather narrow (2.05~2.35eV) as displayed in Figure 1a. Molecular orbital theory analysis reveals that the absorption spectrum of pristine AMQD is attributed by the interorbital transition of electrons from five occupied molecular orbitals to five unoccupied molecular orbitals around Fermi level. The pristine AMQD retains the indirect band structure property of pristine antimonene,44, 45 and the transition dipole moment is rather weak between these frontier orbitals in pristine AMQD. The poor photo-absorption performance makes pristine AMQDs not good PTAs. It has also been widely reported that spontaneously partial oxidation is unavoidable in the preparation of AMQDs or nanosheets no matter using mechanical23 or liquid exfoliation15, 24, 25 or van der Waals epitaxy growth40. Therefore, we further explore the effect of oxidation on PTT performance of AMQDs. Regarding the oxidation, since the each Sb atom has the nonbonding lone pair electrons, the oxygen atom is likely to adsorb onto the surface of antimonene forming dangling oxygen in accordance with the Lewis structure. The stable dangling oxygen at AMQDs face can be expected, and this type of oxidation should be the dominating oxidized form.44 In addition, the oxygen

ACS Paragon Plus Environment

ACS Applied Materials & Interfaces 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

atom also stands a chance to form interstitial oxygen bridge at surface or edge sites in the process of preparation, similar to BPQDs.46, 47 These cases lead to the appearance of oxygen at X-ray photoelectron spectrum of experiments.15, 23, 25, 40 Therefore, we constructed three different oxidative configurations in Figure 1c, including dangling oxygen at face and interstitial oxygen bridge at face or edge. The oxygen content is very small, generally lower than 6%, in spontaneously partial oxidation AMQDs, according to energy dispersive spectroscopy,40 Compared with heavy oxidation in AMQDs, spontaneously partial oxidation has no observable side effects or tissue damage for biomedical applications via the in vivo therapeutic studies.15, 17 We only consider one (~ 2 %) or two (~ 4 %) O atoms absorbing onto AMQDs to simulate the spontaneously partial oxidation.

Figure 1. (a) & (b) Absorption for pristine and oxidized AMQDs. The embedded figure

ACS Paragon Plus Environment

Page 6 of 20

Page 7 of 20 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Applied Materials & Interfaces

of (a) is the structure of pristine AMQD. The mark number (I) denotes pristine AMQD, others mark numbers represent corresponding oxidized AMQDs displayed in (c). (c) The corresponding top and side views of oxidized structure with one or two O atoms: interstitial oxygen bridge at face (II, V), dangling oxygen at face (III, VI) and interstitial oxygen bridge at edge (IV, VII). Purple, antimony; red, oxygen; white, hydrogen. Differently from pristine AMQD, the absorption range of partially oxidized AMQDs exhibits a significant red-shift, which promotes the NIR absorption. More interestingly, the strength of NIR absorption is enhanced with the increase of the oxidization degree. As shown in Figure 2b, c, the oxidation induces the band edge states near the unoccupied orbitals, which forms the new lowest unoccupied molecular orbital (LUMO) and local quantum entrapment.44 Compared with the delocalized LUMO of pristine AMQD, the LUMO of oxidized AMQDs generally localizes around the oxygen sites (see Figure 2a). The localized LUMO behaves as the dominating photo-generated electron accepting state which increases the transition dipole moments of electrons. Meanwhile, the oxidation further enhances the transition of electrons in AMQDs, which greatly improves the good photo-absorption property. Simultaneously, the band edge states narrow the band gap, causing the red-shift of absorption spectrum and facilitating the NIR absorption. The phenomenon is different from the homogeneous BPQDs. The pristine BPQDs also possess poor NIR photo-absorption performance,48 whereas the partial oxidation leads to the slight blue-shift of absorption spectrum for BPQDs.47, 49 The difference derives from the distinction in the antibonding states between oxygen and phosphorus/antimony. Instead of producing band edge states, the antibonding state

ACS Paragon Plus Environment

ACS Applied Materials & Interfaces 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

of P-O bonds is generally located at far from the Fermi level in oxidized BPQDs.46, 47

Figure 2. Real space distribution of LUMO (a) and density of states (DOS) (b) & (c) of pristine and oxidized AMQDs. I: pristine, II, V: interstitial oxygen bridge at face, III, VI: dangling oxygen at face and IV, VII: interstitial oxygen bridge at edge. The II-IV represent one oxidation cases, and the V-VII represent two oxidation cases. To further demonstrate the generality of the effect of oxidation at AMQDs, we also construct other possible shapes of AMQDs, such as triangular, as shown in Figure S1. As expected, the oxidation also produces the band edge states similar to hexagonal shape of AMQDs, which leads to the red-shift of spectrum and enhances the NIR absorption intensity. In addition, no matter for hexagonal or triangular AMQDs, the oxidation in AMQDs generally affects the unoccupied molecular orbitals, and the occupied states have no obvious difference between pristine and oxidized AMQDs as displayed in Figure 2, S2-6. Only AMQD with interstitial oxygen bridge at edge induces band edge states near the occupied molecular orbitals, and forms the new highest

ACS Paragon Plus Environment

Page 8 of 20

Page 9 of 20 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Applied Materials & Interfaces

occupied molecular orbital (HOMO) localized around the oxidation sites. The reason is that the interstitial oxygen slightly shortens the Sb-Sb bond length near the oxidation sites, and causes the localization of the orbital. To be a good PTA, powerful photo-absorptivity is just one of the prerequisites. Another necessary condition is the excellent photothermal conversion. The energy of photo-generated carriers can be released via two pathways, radiative and non-radiative transitions. The non-radiative transition can transform the optical energy to thermal energy. Therefore, the rapid non-radiative transition and release of photo-energy are conducive to the photothermal conversion and PTT performance. To explore the nonradiative transition process of AMQDs, we take the pristine and oxidized AMQDs with two dangling oxygen at face as examples, and perform the NAMD calculations.

Figure 3. (a) Averaged photo-generated carrier non-radiative recombination dynamics in pristine and oxidized AMQDs. The inset shows the averaged absolute values of NAC elements in pristine and oxidized AMQDs. (b) Time dependence of average energy relaxation of the photo-generated electrons of pristine and oxidized AMQDs. The temperature is set to be 300K. After the excitation of occupied orbital electrons, the photo-generated electrons

ACS Paragon Plus Environment

ACS Applied Materials & Interfaces 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 10 of 20

undergo rapid energy relaxation to the first excited state which is mainly constituted by the LUMO. We initiate the NAMD calculations with photo-generated electrons localized on LUMO of AMQDs. As shown in Figure 3, after 4 ps, around 2% and 6% of photo-generated electron-hole pairs recombine for pristine and oxidized AMQDs, respectively. This indicates that the recombination timescale is obviously longer than the picosecond magnitude. Although it is hard to obtain the accurate recombination time from these NAMD simulations, the timescale of non-radiative recombination can be roughly estimated to be around ~ 0.2 and 0.1 ns fitting by an exponential function P(t) = exp(-t/τ) for pristine and oxidized AMQDs,50 respectively. The slow nonradiative recombination in pristine AMQD means that the release of photo-generated electron energy is not easy, which therefore will reduce the thermal generation. Differently, the rapid recombination in oxidized AMQDs can accelerate the release of photo-generated electron energy, and promotes the thermal generation. For the non-radiative transitions in NAMD, the hopping probability of photogenerated carriers between LUMO and HOMO is mainly dominated by the nonadiabatic coupling (NAC) elements, described as,51 d jk   j |

 |  H |  k    | k   j R R t k   j

(1)

Where H is the Kohn-Sham Hamiltonian, 𝜑𝑗, 𝜑𝑘,  j ,  k are the wave functions and corresponding eigenvalues for j and k electronic states, and Ṙ is velocity of the nuclei. The inset of Figure 3 presents the averaged NAC elements of pristine and oxidized AMQDs at 300 K. For oxidized AMQD, the NAC is 2.3 meV, which is obviously larger than that of pristine AMQD (around 1.1 meV).

ACS Paragon Plus Environment

Page 11 of 20 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Applied Materials & Interfaces

According to eq.1, the NAC elements are strongly dependent on the energy difference

 k   j , the electron-phonon (e-p) coupling term  j |  R H | k  and the

nuclear velocity Ṙ.30, 31, 52 As displayed in Figure 4a,d, the averaged energy difference of LUMO and HOMO in pristine AMQD is ~1.7 eV, which is about 1.4 times larger than that of oxidized AMQD (~1.2 eV). Thereby, the energy difference of the interacting states is only one reason for the different NAC in pristine and oxidized AMQDs. On the other hand, the other two factors  j |  R H | k  and Ṙ are also crucial which are closely related with the phonon excitation and e-p coupling. In fact, the impurity in nanomaterials can induce impurity phonon excitation which have a chance to scatter and couple with the intrinsic phonon modes. Meanwhile, the electronic states induced by the impurity usually have strong e-p coupling with the phonon modes of materials.53, 54 In order to analyze the impurity phonon excitation modes, we compute the phonon spatial localization of pristine and oxidized AMQDs (similar to ref 51, 52) and project them onto the Sb and O atoms, respectively. As shown in Figure 4c, f, O atoms have not only the intrinsic phonon modes around 750 cm-1, but also the coupling phonon modes with AMQD (around 0 ~250 cm-1) within a wide range. This indicates the strong coherent vibration of O and Sb atoms, which enhances the e-p coupling and nuclear velocity around the doping region and promotes the non-radiative transitions.

ACS Paragon Plus Environment

ACS Applied Materials & Interfaces 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Figure 4. Time-dependent evolution of frontier orbital energy, the corresponding FT spectra of HOMO and LUMO energy fluctuation and the spatial localization of phonon modes for (a, b, c) pristine and (d, e, f) oxidized AMQDs, respectively. The spatial localization of phonon modes of oxygen are magnified by ten times for clarity. The Fermi level is set as zero. The temperature is set to be 300K. Moreover, to understand the e-p coupling between the electronic states and impurity phonon modes or other phonon modes involved in e-h recombination, we investigate the time-dependent evolution of frontier orbitals and their Fourier transform (FT) spectra.55 Actually, the strength of e-p coupling is correlated with the strength of molecular orbital energy fluctuation amplitude.53,

56

Obviously, compared with

electronic states in pristine AMQD, the band edge states induced by oxidation present more prominent fluctuations as shown in Figure 4a&d, suggesting stronger e-p coupling in oxidized AMQDs. The fluctuations of state energies are dominated by some specific phonon vibrational modes. The predominant vibrational frequency can be identified from the FT spectra.57, 58 As seen from the FT spectra, the vibrational frequency around

ACS Paragon Plus Environment

Page 12 of 20

Page 13 of 20 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Applied Materials & Interfaces

130 and 260 cm-1 driving the fluctuation of band edge states (LUMO of oxidized AMQD) is obviously larger than the frequency around 100 cm-1 controlling the fluctuation of LUMO energy in pristine AMQD. This indicates oxidized AMQDs possess stronger phonon excitation and e-p coupling to promote the release of photoenergy than pristine AMQD. To further illustrate the average release of photo-energy clearly, we define Ee(0) as the initially specific energy of photo-generated electrons of AMQDs, and Ee(t) as the average electron energy during relaxation. Ee(t) as a function of time for pristine and oxidized AMQDs is displayed in Figure 3b. The oxidized AMQD indeed releases more energy than pristine AMQD within the same time scale. The energy released via nonradiative transitions turns into the thermal form. Together with the narrow and weak photoabsorption and the slow release of photo-energy in pristine AMQD, AMQDs exhibiting superior PTT performance in experiment should be ascribed to the partial oxidation in AMQDs rather than pristine AMQDs. Previous theoretical study showed that two-dimensional antimonene with partial oxidation was also accompanied with similar band edge states.44 This indicates that large antimonene nanoflakes with spontaneously partial oxidation have similar band edge states with AMQDs. Therefore, we believe the antimonene nanoflakes should also possess good photothermal conversion performance. In fact, the antimonene nanoflakes with an average size of ~ 140 nm showed an excellent photothermal conversion efficiency of 41.8 % in experiment, 17 similar to AMQDs (the average size is ~ 3.9 nm) ~ 45.5 %. 15

ACS Paragon Plus Environment

ACS Applied Materials & Interfaces 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 14 of 20

Compared with AMQDs, the photothermal conversion performance of BPQDs is generally low in experiments. (BPQDs 28.4%,16 AMQDs 45.5 %,15 AM nanosheets 41.8 % 17). The high photothermal conversion efficiency generally needs large non-radiative transitions, which is a positive correlation with the nonadiabatic coupling. According to Equation (1), the energy difference

k   j

in AMQDs is obviously reduced by the

partial oxidation generated band edge states. For BPQDs, they possess good defecttolerant for partial oxidation,47 the energy difference

k   j

does not show obvious

change. In addition, the fluctuation of initial (j) and final (k) electronic states is directly correlated with the strength of the e-p coupling, which is closely related with the  j |  R H |  k 

term. The fluctuation of the new emerged band edge states is stronger

than that of the intrinsic electronic states. For BPQDs, the initial and final electronic states are all the intrinsic electronic states of BPQDs, and the fluctuation has no obvious change under partial oxidation. Moreover, for BPQD, it has two pathways to release the photo-energy. The radiative transitions generate the fluorescence, and the nonradiative transitions produce the heat. As a result, BPQDs not only possess fluorescence bioimaging property,59, 60 but also photothermal therapy performance.59, 61 For AMQDs, only photo-energy can be transferred to heat via non-radiative transitions due to the emergence of the band edge states. That is, the PTCE of AMQDs will be higher than BPQDs.Conclusions In summary, we provide the first excited state dynamics to the superior PTT performance of AMQDs observed experimentally. In fact, the good PTT property does not derive from pristine AMQDs themselves on account of the weak photoabsorption

ACS Paragon Plus Environment

Page 15 of 20 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Applied Materials & Interfaces

and low photothermal conversion. Interestingly, the spontaneously partial oxidation in AMQDs plays a key role to optimize the photoabsorption and photothermal conversion. Specifically, the partial oxidation introduces the band edge states near the unoccupied molecular orbital, which not only strengthens the transition dipole moment, but also broadens the optical absorption range in NIR region. Meanwhile, the oxidation speeds up the release of photo-energy through accelerating the non-radiative transition rate, which further improves the photothermal conversion. This work may open a feasible route to efficient utilization of oxidative 2DQDs in biomedical field, and trigger intensive research in other related 2DQDs.

Supporting Information The geometric structure, absorption spectrum and DOSs of triangular AMQDs in Figure S1. The real space distribution of HOMO and LUMO of hexangular and triangular AMQDs. (PDF)

Conflicts of interest The authors declare no competing financial interests.

Acknowledgments This work is supported by the National Key R&D Program of China (Grant No. 2017YFA0204800), Natural Science Foundation of China (21525311, 21773027, 21703032, 21803032), Natural Science Foundation of Jiangsu Province (BK20180735) and NUPTSF (Grant No.NY219025). We thank the Big Data Center of Southeast University for providing the facility support on the numerical calculations in this paper.

ACS Paragon Plus Environment

ACS Applied Materials & Interfaces 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

References (1) Vanparijs, N.; Nuhn, L.; De Geest, B. G. Transiently Thermoresponsive Polymers and Their Applications in Biomedicine. Chem. Soc. Rev. 2017, 46, 1193-1239. (2) Li, Z.; Yu, X.-F.; Chu, P. K. Recent Advances in Cell-Mediated Nanomaterial Delivery Systems for Photothermal Therapy. J. Mater. Chem. B 2018, 6, 1296-1311. (3) Meng, D.; Yang, S.; Guo, L.; Li, G.; Ge, J.; Huang, Y.; Bielawski, C. W.; Geng, J. The Enhanced Photothermal Effect of Graphene/Conjugated Polymer Composites: Photoinduced Energy Transfer and Applications in Photocontrolled Switches. Chem. Commun. 2014, 50, 14345-14348. (4) Liu, X.; Wang, Q.; Li, C.; Zou, R.; Li, B.; Song, G.; Xu, K.; Zheng, Y.; Hu, J. Cu(2)-Xse@Msio(2)-Peg CoreShell Nanoparticles: A Low-Toxic and Efficient Difunctional Nanoplatform for Chemo-Photothermal Therapy under near Infrared Light Radiation with a Safe Power Density. Nanoscale 2014, 6, 4361-4370. (5) Liang, C.; Xu, L.; Song, G.; Liu, Z. Emerging Nanomedicine Approaches Fighting Tumor Metastasis: Animal Models, Metastasis-Targeted Drug Delivery, Phototherapy, and Immunotherapy. Chem. Soc. Rev. 2016, 45, 6250-6269. (6) Cheng, L.; Wang, C.; Feng, L.; Yang, K.; Liu, Z. Functional Nanomaterials for Phototherapies of Cancer. Chem. Rev. 2014, 114, 10869-10939. (7) Tian, Q.; Tang, M.; Sun, Y.; Zou, R.; Chen, Z.; Zhu, M.; Yang, S.; Wang, J.; Wang, J.; Hu, J. Hydrophilic Flower-Like Cus Superstructures as an Efficient 980 Nm Laser-Driven Photothermal Agent for Ablation of Cancer Cells. Adv. Mater. 2011, 23, 3542-3547. (8) Jain, P. K.; Huang, X. H.; El-Sayed, I. H.; El-Sayed, M. A. Noble Metals on the Nanoscale: Optical and Photothermal Properties and Some Applications in Imaging, Sensing, Biology, and Medicine. Acc. Chem. Res. 2008, 41, 1578-1586. (9) Zou, Q.; Abbas, M.; Zhao, L.; Li, S.; Shen, G.; Yan, X. Biological Photothermal Nanodots Based on SelfAssembly of Peptide-Porphyrin Conjugates for Antitumor Therapy. J. Am. Chem. Soc. 2017, 139, 19211927. (10) Park, J. E.; Kim, M.-J.; Lim, M. S.; Kang, S. Y.; Kim, J. K.; Oh, S.-H.; Her, M.; Cho, Y.-H.; Sung, Y.-E. Graphitic Carbon Nitride-Carbon Nanofiber as Oxygen Catalyst in Anion-Exchange Membrane Water Electrolyzer and Rechargeable Metal–Air Cells. Appl. Catal. B-Environ 2018, 237, 140-148. (11) Zheng, X. T.; Ananthanarayanan, A.; Luo, K. Q.; Chen, P. Glowing Graphene Quantum Dots and Carbon Dots: Properties, Syntheses, and Biological Applications. Small 2015, 11, 1620-1636. (12) Lee, H. U.; Park, S. Y.; Lee, S. C.; Choi, S.; Seo, S.; Kim, H.; Won, J.; Choi, K.; Kang, K. S.; Park, H. G.; Kim, H. S.; An, H. R.; Jeong, K. H.; Lee, Y. C.; Lee, J. Black Phosphorus (Bp) Nanodots for Potential Biomedical Applications. Small 2016, 12, 214-219. (13) Yang, G.; Wan, X.; Gu, Z.; Zeng, X.; Tang, J. Near Infrared Photothermal-Responsive Poly(Vinyl Alcohol)/Black Phosphorus Composite Hydrogels with Excellent on-Demand Drug Release Capacity. J. Mater. Chem. B 2018, 6, 1622-1632. (14) Qu, G.; Liu, W.; Zhao, Y.; Gao, J.; Xia, T.; Shi, J.; Hu, L.; Zhou, W.; Gao, J.; Wang, H.; Luo, Q.; Zhou, Q.; Liu, S.; Yu, X.-F.; Jiang, G. Improved Biocompatibility of Black Phosphorus Nanosheets by Chemical Modification. Angew. Chem. 2017, 129, 14680-14685. (15) Tao, W.; Ji, X.; Xu, X.; Islam, M. A.; Li, Z.; Chen, S.; Saw, P. E.; Zhang, H.; Bharwani, Z.; Guo, Z.; Shi, J.; Farokhzad, O. C. Antimonene Quantum Dots: Synthesis and Application as near-Infrared Photothermal Agents for Effective Cancer Therapy. Angew. Chem. Int. Ed. 2017, 56, 11896–11900.

ACS Paragon Plus Environment

Page 16 of 20

Page 17 of 20 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Applied Materials & Interfaces

(16) Sun, Z.; Xie, H.; Tang, S.; Yu, X. F.; Guo, Z.; Shao, J.; Zhang, H.; Huang, H.; Wang, H.; Chu, P. K. Ultrasmall Black Phosphorus Quantum Dots: Synthesis and Use as Photothermal Agents. Angew. Chem. 2015, 127, 11688-11692. (17) Tao, W.; Ji, X.; Zhu, X.; Li, L.; Wang, J.; Zhang, Y.; Saw, P. E.; Li, W.; Kong, N.; Islam, M. A.; Gan, T.; Zeng, X.; Zhang, H.; Mahmoudi, M.; Tearney, G. J.; Farokhzad, O. C. Two-Dimensional AntimoneneBased Photonic Nanomedicine for Cancer Theranostics. Adv. Mater. 2018, 30, 1802061. (18) Xue, T.; Liang, W.; Li, Y.; Sun, Y.; Xiang, Y.; Zhang, Y.; Dai, Z.; Duo, Y.; Wu, L.; Qi, K.; Shivananju, B. N.; Zhang, L.; Cui, X.; Zhang, H.; Bao, Q. Ultrasensitive Detection of Mirna with an Antimonene-Based Surface Plasmon Resonance Sensor. Nat. Commun. 2019, 10, 28. (19) Xing, C.; Chen, S.; Qiu, M.; Liang, X.; Liu, Q.; Zou, Q.; Li, Z.; Xie, Z.; Wang, D.; Dong, B.; Liu, L.; Fan, D.; Zhang, H. Conceptually Novel Black Phosphorus/Cellulose Hydrogels as Promising Photothermal Agents for Effective Cancer Therapy. Adv. Healthc. Mater. 2018, 7, e1701510. (20) Frezard, F.; Demicheli, C.; Ribeiro, R. R. Pentavalent Antimonials: New Perspectives for Old Drugs. Molecules 2009, 14, 2317-2336. (21) Yang, X.; Liu, G.; Shi, Y.; Huang, W.; Shao, J.; Dong, X. Nano-Black Phosphorus for Combined Cancer Phototherapy: Recent Advances and Prospects. Nanotechnology 2018, 29, 222001. (22) Choi, J. R.; Yong, K. W.; Choi, J. Y.; Nilghaz, A.; Lin, Y.; Xu, J.; Lu, X. Black Phosphorus and Its Biomedical Applications. Theranostics 2018, 8, 1005-1026. (23) Ares, P.; Aguilar-Galindo, F.; Rodriguez-San-Miguel, D.; Aldave, D. A.; Diaz-Tendero, S.; Alcami, M.; Martin, F.; Gomez-Herrero, J.; Zamora, F. Mechanical Isolation of Highly Stable Antimonene under Ambient Conditions. Adv. Mater. 2016, 28, 6332-6336. (24) Gibaja, C.; Rodriguez-San-Miguel, D.; Ares, P.; Gómez-Herrero, J.; Varela, M.; Gillen, R.; Maultzsch, J.; Hauke, F.; Hirsch, A.; Abellán, G.; Zamora, F. Few-Layer Antimonene by Liquid-Phase Exfoliation. Angew. Chem. Int. Ed. 2016, 55, 14345-14349. (25) Gusmão, R.; Sofer, Z.; Bouša, D.; Pumera, M. Pnictogens (as, Sb, Bi) Nanosheets by Shear Exfoliation Using Kitchen Blenders for Electrochemical Applications. Angew. Chem. Int. Ed. 2017, 129, 14609-14614. (26) te Velde, G.; Bickelhaupt, F. M.; Baerends, E. J.; Fonseca Guerra, C.; Van Gisbergen, S. J. A.; Snijders, J. G.; Ziegler, T. Chemistry with Adf. J. Comput. Chem. 2001, 22, 931-967. (27) Guerra, C. F.; Snijders, J. G.; te Velde, G.; Baerends, E. J. Towards an Order-N Dft Method. Theor. Chem. Acc. 1998, 99, 391-403. (28) Perdew, J. P.; Burke, K.; Ernzerhof, M. Generalized Gradient Approximation Made Simple. Phys. Rev. Lett. 1996, 77, 3865-3868. (29) Lenthe, E. V.; Baerends, E. J. Optimized Slater-Type Basis Sets for the Elements 1-118. J. Comput. Chem. 2003, 24, 1142-1156. (30) Chu, W.; Saidi, W. A.; Zheng, Q.; Xie, Y.; Lan, Z.; Prezhdo, O. V.; Petek, H.; Zhao, J. Ultrafast Dynamics of Photongenerated Holes at a CH3OH/TiO2 Rutile Interface. J. Am. Chem. Soc. 2016, 138, 13740-13749. (31) Zheng, Q.; Saidi, W. A.; Xie, Y.; Lan, Z.; Prezhdo, O. V.; Petek, H.; Zhao, J. Phonon-Assisted Ultrafast Charge Transfer at Van Der Waals Heterostructure Interface. Nano Lett. 2017, 17, 6435-6442. (32) Craig, C. F.; Duncan, W. R.; Prezhdo, O. V. Trajectory Surface Hopping in the Time-Dependent KohnSham Approach for Electron-Nuclear Dynamics. Phys. Rev. Lett. 2005, 95, 163001. (33) Akimov, A. V.; Prezhdo, O. V. The Pyxaid Program for Non-Adiabatic Molecular Dynamics in Condensed Matter Systems. J. Chem. Theory Comput. 2013, 9, 4959-4972.

ACS Paragon Plus Environment

ACS Applied Materials & Interfaces 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

(34) Akimov, A. V.; Prezhdo, O. V. Advanced Capabilities of the Pyxaid Program: Integration Schemes, Decoherence Effects, Multiexcitonic States, and Field-Matter Interaction. J. Chem. Theory Comput. 2014, 10, 789-804. (35) Zheng, Q.; Zhao, J. Hefei NAMD. http://staff.ustc.edu.cn/∼zhaojin/code.html (Accessed Oct. 24, 2016). (36) Kresse, G.; Furthmüller, J. Efficient Iterative Schemes for Ab Initio Total-Energy Calculations Using a Plane-Wave Basis Set. Phys. Rev. B 1996, 54, 11169-11186. (37) Kresse, G.; Furthmüller, J. Efficiency of Ab-Initio Total Energy Calculations for Metals and Semiconductors Using a Plane-Wave Basis Set Comput. Mater. Sci. 1996, 6, 15-50. (38) Niu, X.; Yi, Y.; Bai, X.; Zhang, J.; Zhou, Z.; Chu, L.; Yang, J.; Li, X. a. Photocatalytic Performance of Few-Layer Graphitic C3n4: Enhanced by Interlayer Coupling. Nanoscale 2019, 11, 4101-4107. (39) Niu, X.; Li, Y.; Zhang, Y.; Zheng, Q.; Zhao, J.; Wang, J. Highly Efficient Photogenerated Electron Transfer at a Black Phosphorus/Indium Selenide Heterostructure Interface from Ultrafast Dynamics. J. Mater. Chem. C 2019, 7, 1864-1870. (40) Ji, J.; Song, X.; Liu, J.; Yan, Z.; Huo, C.; Zhang, S.; Su, M.; Liao, L.; Wang, W.; Ni, Z.; Hao, Y.; Zeng, H. Two-Dimensional Antimonene Single Crystals Grown by Van Der Waals Epitaxy. Nat. Commun. 2016, 7, 13352. (41) Fortin-Deschenes, M.; Waller, O.; Mentes, T. O.; Locatelli, A.; Mukherjee, S.; Genuzio, F.; Levesque, P. L.; Hebert, A.; Martel, R.; Moutanabbir, O. Synthesis of Antimonene on Germanium. Nano Lett. 2017, 17, 4970-4975. (42) Ares, P.; Palacios, J. J.; Abellan, G.; Gomez-Herrero, J.; Zamora, F. Recent Progress on Antimonene: A New Bidimensional Material. Adv. Mater. 2017, 30, 1703771. (43) Zhang, S.; Guo, S.; Chen, Z.; Wang, Y.; Gao, H.; Gomez-Herrero, J.; Ares, P.; Zamora, F.; Zhu, Z.; Zeng, H. Recent Progress in 2D Group-Va Semiconductors: From Theory to Experiment. Chem. Soc. Rev. 2017, 47, 982-1021. (44) Zhang, S.; Zhou, W.; Ma, Y.; Ji, J.; Cai, B.; Yang, S. A.; Zhu, Z.; Chen, Z.; Zeng, H. Antimonene Oxides: Emerging Tunable Direct Bandgap Semiconductor and Novel Topological Insulator. Nano Lett. 2017, 17, 3434-3440. (45) Zhang, S.; Xie, M.; Li, F.; Yan, Z.; Li, Y.; Kan, E.; Liu, W.; Chen, Z.; Zeng, H. Semiconducting Group 15 Monolayers:A Broad Range of Band Gaps and High Carrier Mobilities. Angew.Chem.Int. Ed. 2016, 55, 1666 –1669. (46) Ziletti, A.; Carvalho, A.; Campbell, D. K.; Coker, D. F.; Castro Neto, A. H. Oxygen Defects in Phosphorene. Phys. Rev. Lett. 2015, 114, 046801. (47) Niu, X.; Shu, H.; Li, Y.; Wang, J. Photoabsorption Tolerance of Intrinsic Point Defects and Oxidation in Black Phosphorus Quantum Dots. J. Phys. Chem. Lett. 2017, 8, 161-166. (48) Zhou, S.; Liu, N.; Zhao, J. Phosphorus Quantum Dots as Visible-Light Photocatalyst for Water Splitting. Computational Materials Science 2017, 130, 56-63. (49) Ziletti, A.; Carvalho, A.; Trevisanutto, P. E.; Campbell, D. K.; Coker, D. F.; Castro Neto, A. H. Phosphorene Oxides: Bandgap Engineering of Phosphorene by Oxidation. Phys. Rev. B 2015, 91, 085407. (50) Niu, X.; Li, Y.; Zhang, Y.; Li, Q.; Zhou, Q.; Zhao, J.; Wang, J. Photo-Oxidative Degradation and Protection Mechanism of Black Phosphorus: Insights from Ultrafast Dynamics J. Phys. Chem. Lett. 2018, 9 5034-5039.

ACS Paragon Plus Environment

Page 18 of 20

Page 19 of 20 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Applied Materials & Interfaces

(51) Reeves, K. G.; Schleife, A.; Correa, A. A.; Kanai, Y. Role of Surface Termination on Hot Electron Relaxation in Silicon Quantum Dots: A First-Principles Dynamics Simulation Study. Nano Lett. 2015, 15, 6429-6433. (52) Zhao, C.; Zheng, Q.; Wu, J.; Zhao, J. Ab Initio Nonadiabatic Molecular Dynamics Investigation on the Dynamics of Photogenerated Spin Hole Current in Cu-Doped MoS2. Phys. Rev. B 2017, 96, 134308. (53) Zhang, L.; Zheng, Q.; Xie, Y.; Lan, Z.; Prezhdo, O. V.; Saidi, W. A.; Zhao, J. Delocalized Impurity Phonon Induced Electron-Hole Recombination in Doped Semiconductors. Nano Lett. 2018, 18, 1592– 1599. (54) Estreicher, S. K.; Gibbons, T. M.; Kang, B.; Bebek, M. B. Phonons and Defects in Semiconductors and Nanostructures: Phonon Trapping, Phonon Scattering, and Heat Flow at Heterojunctions. J. Appl. Phys. 2014, 115, 012012. (55) Zhang, R.; Zhang, L.; Zheng, Q.; Gao, P.; Zhao, J.; Yan, J. Direct Z-Scheme Water Splitting Photocatalyst Based on Two-Dimensional Van Der Waals Heterostructures. J. Phys. Chem. Lett. 2018, 9, 5419-5242. (56) Long, R.; Guo, M.; Liu, L.; Fang, W. Nonradiative Relaxation of Photoexcited Black Phosphorus Is Reduced by Stacking with MoS2: A Time Domain Ab Initio Study. J. Phys. Chem. Lett. 2016, 7, 18301835. (57) Long, R.; Fang, W.; Akimov, A. V. Nonradiative Electron-Hole Recombination Rate Is Greatly Reduced by Defects in Monolayer Black Phosphorus: Ab Initio Time Domain Study. J. Phys. Chem. Lett. 2016, 7, 653-659. (58) Long, R.; Fang, W.; Prezhdo, O. V. Moderate Humidity Delays Electron-Hole Recombination in Hybrid Organic-Inorganic Perovskites: Time-Domain Ab Initio Simulations Rationalize Experiments. J. Phys. Chem. Lett. 2016, 7, 3215-3222. (59) Qiu, M.; Ren, W. X.; Jeong, T.; Won, M.; Park, G. Y.; Sang, D. K.; Liu, L. P.; Zhang, H.; Kim, J. S. Omnipotent Phosphorene: A Next-Generation, Two-Dimensional Nanoplatform for Multidisciplinary Biomedical Applications. Chem. Soc. Rev. 2018, 47, 5588-5601. (60) Long, L.; Niu, X.; Yan, K.; Zhou, G.; Wang, J.; Wu, X.; Chu, P. K. Highly Fluorescent and Stable Black Phosphorous Quantum Dots in Water. Small 2018, 14, 1803132. (61) Qiu, M.; Wang, D.; Liang, W.; Liu, L.; Zhang, Y.; Chen, X.; Sang, D. K.; Xing, C.; Li, Z.; Dong, B.; Xing, F.; Fan, D.; Bao, S.; Zhang, H.; Cao, Y. Novel Concept of the Smart Nir-Light-Controlled Drug Release of Black Phosphorus Nanostructure for Cancer Therapy. Proceedings of the National Academy of Sciences of the United States of America 2018, 115, 501-506.

ACS Paragon Plus Environment

ACS Applied Materials & Interfaces 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Partially oxidized antimonene quantum dots: remarkably enhanced photothermal cancer therapy efficiency by improving photoabsorption and photothermal conversion.

ACS Paragon Plus Environment

Page 20 of 20