Enhanced Photovoltage Response of Hematite-X-Ferrite Interfaces (X = Cr, Mn, Co, or Ni)

High-fluorescent p-X-ferrites (XFe2O4; XFO; X = Fe, Cr, Mn, Co, or Ni) embedded in n-hematite (Fe2O3) surfaces were successfully fabricated via a facile bio-approach using Shewanella oneidensis MR-1. The results revealed that the X ions with high/low work functions modify the unpaired spin Fe2+–O2− orbitals in the XFe2O4 lattices to become localized paired spin orbitals at the bottom of conduction band, separating the photovoltage response signals (73.36~455.16/−72.63~−32.43 meV). These (Fe2O3)–O–O–(XFe2O4) interfacial coupling behaviors at two fluorescence emission peaks (785/795 nm) are explained via calculating electron-hole effective masses (Fe2O3–FeFe2O4 17.23 × 10−31 kg; Fe2O3–CoFe2O4 3.93 × 10−31 kg; Fe2O3–NiFe2O4 11.59 × 10−31 kg; Fe2O3–CrFe2O4 −4.2 × 10−31 kg; Fe2O3–MnFe2O4 −11.73 × 10−31 kg). Such a system could open up a new idea in the design of photovoltage response biosensors.


Background
As a n-type semiconductor, hematite (Fe 2 O 3 ) is an important semiconductor in the fields of photoluminescence and electron paramagnetic imaging due to its chemical stability and band gap (2 eV) [1]. However, poor minority charge carrier mobility (0.2 cm 2 V −1 s −1 ) and ultrafast recombination of photogenerated carriers (~10 ps) limit its application as a high-photostability fluorescent material [2]. Recently, an interesting option is the conjugation of Fe 2 O 3 with a p-type ferrite (band gaps 1.9~2.7 eV) with a lower but similar conduction band level and an appropriate valence band level [3]. It has two advantages, e.g., unpaired-paired spin change and electron-hole recombination [4]. For example, Sun et al. [5] confirmed that the electrons flow through the energy barrier between the Fe 2 O 3 and Fe 3 O 4 phases, according to spin-dependent tunneling mode. Higher void fraction of cubic Fe 3 O 4 provides more transfer channels for tetrahedral ion diffusion and charge transfer. To enhance separation rate of photoinduced charge carriers, Shen et al. [6] used Mg to modify the surface photovoltage of Fe 3 O 4 /Fe 2 O 3 heterostructured hollow nanospheres. A remarkable surface photovoltage response in UV and visible spectral region (320~570 nm) was attributed to the 2p(O 2− )→3d(Fe 3+ ) charge transfer and Fe 3+ (3d 5 ) crystal field transitions of the MgFe 2 O 4 and Fe 2 O 3 interface. Therefore, the incorporation of the magnetic nanocrystals associated with heavy metal ion (X)-modified Fe 3 O 4 on the Fe 2 O 3 surface can not only improve fluorescence intensity but also recycle the fluorescence by magnetic separation under modest magnetic fields [7].

Methods
Here, S. oneidensis MR-1 was cultured in a chemically defined minimal medium as described previously [11]. MR-1 cells were cultured aerobically on TSB (without dextrose) for 16 h at 30°C with shaking at 100 rpm. Cells were washed twice and centrifuged at 6000 rpm for 10 min in sterile PIPES/AQDS buffer at pH 7, followed by one wash and re-suspension to~10 9 cells ml −1 in M1 medium. Anaerobically grown cells of MR-1 were added to the tubes containing the magnetite and M1 medium to obtain a final concentration of 2.3 × 10 8 cells ml −1 . The total volume of medium in each tube, including X(Cr, Mn, Co, or Ni)-modified goethite (FeOOH) and cells, was 250 ml. The X-modified Fe 3 O 4 in the medium had a final concentration of 90 mM [12]. All treatment tubes were incubated in the dark at 30°C until the end of the experiment. All treatments with anaerobically cultured cells were incubated for 45 days.
The size of the laser spot was less than 2 μm, and the acquisition time for all spectra was 20 s. Scanning electron microscopy (SEM) and energy-dispersive X-ray spectroscopy (EDS) were performed on a Cu plate with a Hitachi S-4800 field emission machine with an accelerating voltage of 5 KeV [13]. The X-ray diffraction data were collected for all Fe 2 O 3 -XFe 2 O 4 heterostructures using an X-ray diffractometer (Bryke D8-Advance, Germany, Cu K α radiation, λ = 0.154 nm, 40 kV, 40 mA) [14]. Raman scattering measurements (Labram HR evolution, Horiba Scientific, France) were conducted at room temperature under a backscattering geometric configuration using a WITec-Alpha confocal micro-Raman system [15]. The light absorption properties of the heterostructures were tested by UV-Vis diffuse reflectance spectroscopy (DRS) (Evolution 220, USA) [16]. Atomic force microscope (AFM) and Kelvin probe force microscopy (KPFM) measurements were performed on an atomic force microscope (Asylum Research MFP-3D, USA) [17]. Photoluminescence (PL) emission at room temperature was obtained at 420~900 nm with an excitation wavelength at 400 nm. The slit widths for both the excitation and emission were 5.0 nm. A fiber-based fluorescence spectrometer (USB 4000, Ocean Optics, USA) was used to record the in situ PL spectra [18].
Besides, we simulated the effective masses of electronhole pairs, dielectric functions (ε), and spin-partial densities of states (spin-PDOSs) via Kramers-Kronig transform to give an insight into the electron transfer process at the atomic level and to contribute to the interpretation of experimental results from techniques such as DRS, KPFM-AFM, or PL, based on the generalized gradient-corrected Perdew-Burke-Ernzerhof functional + U (GGA-PBE) (Castep, Materials studio, Accelrys, USA) [19], where the Coulomb and screened exchange parameters (U, J) were set 5 and 1 eV, respectively. A kinetic energy cutoff of 300 eV for the electrons was used, well within the convergence of a total-energy calculation. A 2 × 2 × 2 super cell was introduced for the interstitial plane-wave, and a 5 × 5 × 5 k-point mesh for integration over the Brillouin zone.

Structural Characterization
In Burns' opinion [20]  To further identify the interactions of iron oxides, we used lines in Fig. 1c to depict the typical Raman spectrum of Fe 2 O 3 -XFe 2 O 4 heterostructures. The Raman band at the F 2g , E g , and E 2g modes reflect translational movement of the tetrahedron, symmetric bending of oxygen with respect to the metal ion, and asymmetric stretching of Fe(X) and O, respectively. These bands reflect that Fe 2 O 3 comprises hexagonal close-packed layers of O 2− and that Fe 3+ ions fill two thirds of the octahedral voids, forming a FeO 6 octahedral layer. XFe 2 O 4 is a normal spinel, with X 2+ ions at tetrahedral sites and Fe 3+ ions at octahedral sites. On another side, we can see that a broad asymmetric D peak at 915~970 cm −1 as the phonon scattering near the Brillouin zone boundary is attributed to the long-range (Fe 2 O 3 )-O-O-(XFe 2 O 4 ) interface. These results confirm that the surface Fe 2 O 3 has been successfully reduced as a XFe 2 O 4 and that they are bonded to each other with the shared oxygen atoms of the octahedron-tetrahedron.

Unpaired-Paired Spin Change in the Lattice
In the literature [3], the enhanced photovoltage response performances can be attributed to intra-or inter-electronic transition in the UV and visible region. The origin of electron transfer enhancement of Fe 2 O 3 -XFe 2 O 4 can be summarized by (i) unpairedpaired spin change in the lattice and (ii) electron-hole recombination in the interface. Figure 2a verifies that the X ions enhance the average fluorescence intensities by 3.13~6.35 multiples than that of Fe 2 O 3 -Fe 3 O 4 , where the band gap differences in Fig. 2b are close to the Fermi point, providing high electron transfer ratios. In the octahedral Fe 3+ -O 2− orbital at an intrinsic main fluorescence emission peak of 390 nm, the absorption bands can be attributed to two charge transfers as the oxygen-to-metal 2p(O 2− )→3d(Fe 3+ ) (left region: Fe 2 O 3 ; and middle region: XFe 2 O 4 ) intra-atomic transitions, reflecting the non-degeneracy ( 6 A 1 )→three orbital degeneracy (T 2g ) inter-atomic transition [23]. This corresponds to the T 2g -T 2g orbital degeneracy, as shown in Fig. 2c.
On another side, the spin parity of the iron pairs can remain the same in the excited state, showing the spindown PDOSs. To modify the electron transfer behaviors in tetrahedral Fe 2+ -O 2− orbitals at two broad blue fluorescence emission peaks at 450 and 473 nm, we used X 2+ as an acceptor to occupy the tetrahedral sites at the bottom of the conduction band, and thus, the electronic transitions implying Fe 2+ (or X 2+ )-O 2− orbitals are known to be only at the origin of charge transfers between the bottom of the conduction band and the top of the valence band. The unpaired spin orbitals change into paired spin orbitals; therefore, the paired spin orbitals enhance the spin quantum number (S) to 1, changing the multiplicity of the excited state (M = 2S + 1) into 3. This unpaired-paired spin change provides more active electron gas in the Fe 2 O 3 -XFe 2 O 4 interface to enhance the average luminous intensities as 3.31~8.18 multiples than that of Fe 2 O 3 -Fe 3 O 4 by the excitation of 488 nm, as presented in Fig. 3a. The accelerated electron-hole recombination [24] at the near-infrared photoresponse region is beneficial for transferring long-range electrons to separate the photovoltage response signal.

Electron-Hole Recombination in the Interface
Ultimately, we found that Fe 3 O 4 has a significant photovoltage response red shifted to 257.7 meV from  Fig. 3b, which allows for the efficient separation of electron-hole pairs at the Fe 2 O 3 -Fe 3 O 4 interface, which will be higher than that (200 meV) of the reported Fe 2 O 3 -ZnFe 2 O 4 interface [25][26][27]. The origin of the high/low photovoltage response region (theoretical difference data~200 meV; experimental difference data 45~160 meV) is attributed to the surface potential difference (270 meV/ 3~70 meV) of Fe 2 O 3 and XFe 2 O 4 , according to the theoretical potential images (see Fig. 3c). The photovoltage response signal in the low photovoltage response region is modified via the X-Fe-O orbital degeneracy.
To our knowledge, the crystal field theory indicates that the Fe-d orbital will split into the doubly degenerate e g orbital (d z2 and d x2-y2 ) and triple degenerate t 2g orbital (d xy , d yz , and d xz ) [28]. On the one hand, the high-energy Fe-d x2-y2 orbital (work function 4.5 eV) can be modified by the X-d x2-y2 orbital with the higher work functions (Co 4.7 eV and Ni 4.6 eV) [29]. The X ions reduce both octahedral and tetrahedral surface potentials (~0.7 and 10 meV); because of that, the down-spin Co 2+ (or Ni 2+ )-Fe 3+ interfacial coupling degenerates with the down-spin d x2-y2 orbital of Fe 2+ -3d 6 4s 2 (Fig. 2c)  Consequently, the different photovoltage response behaviors above can be used for the design of highmobility electronic devices and fluorescent probes for different heavy metal ion imaging, oxygen evolution catalysts [30], and biomolecules [31], etc.

Conclusions
In summary, a novel bio-induced phase transition method for the growth of XFe 2 O 4 embedded in a Fe 2 O 3 is proposed here using S. oneidensis MR-1. We explained the mechanism of surface photovoltage response and high-photostability fluorescence. The present work demonstrates that the calculated unpaired-paired spin X 2+ -Fe 2+ -O 2-orbitals verify the enhanced photovoltage response signal (theoretical data~200 meV; experimental data 45~160 meV) and separate the high/ low surface potential regions (270 meV/3~70 meV) based on the calculated electron-hole effective masses. As a consequence, our works provide a reference for designing new photoluminescence and electron paramagnetic imaging biosensors. Further investigation will be focused on the electron transfer process between interfaces and heavy metal ions in an aquatic environment to garner a better understanding of the selective fluorescence probe application.  [26] and 5.52 eV [27], respectively, and the charges transfer between the different work functions of two materials for their Fermi levels to equilibrate. The corresponding theoretical surface potential images are shown in (c). d means the calculated effective masses of electron-hole pairs and surface potential illustration