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. 2022 Nov 1;7(45):41594–41605. doi: 10.1021/acsomega.2c05580

Nickel–Cobalt Oxide Nanoparticle-Induced Biohydrogen Production

Zhenmin Li †, Jiangmei Wang ‡, Kexin Tian †, Chen Zhou †, Yong Pei †, Jishi Zhang †,*, Lihua Zang †
PMCID: PMC9670286  PMID: 36406540

Abstract

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The positive effects of metal oxide nanoparticles (NPs) on dark fermentation (DF) for biohydrogen synthesis have been increased, and the mechanism still needs to be further revealed. In this study, nickel–cobalt oxide (NiCo2O4) NPs were prepared to increase H2 yield via DF. The highest (259.67 mL/g glucose) and the lowest (188.14 mL/g glucose) yields were achieved at 400 and 800 mg/L NiCo2O4 NPs added, respectively, with their corresponding 33.97% increase and 2.93% decrease compared with the control yield (193.82 mL/g glucose). Meanwhile, the microbial community further confirmed that NiCo2O4 NPs increased the abundance of the dominant H2-producing Clostridium sensu stricto1 by 23.05%. The gene prediction also showed that NiCo2O4 NPs increased the abundance of genes encoding the rate-limiting enzyme pyruvate kinase in glycolysis, thus increasing the substrate conversion. Moreover, the gene abundance of key enzymes directly related to H2 evolution was also increased at different levels.

1. Introduction

As more and more machines gradually replace human labor, the increasing level of mechanization and industrialization inevitably leads to environmental pollution and other problems.1 In particular, the CO2 produced from the use of coal, oil, and natural gas has led to global warming, increased sea levels, and even the extinction of some species.2 The emergence of extreme weather may occur, which threatens the normal life and production of human beings.3 Moreover, the increasing requirement for energy from a growing world population increases the pressure on the environment and energy. The above serious situation has forced people to accelerate the development of new energy sources for the eco-friendly and sustainable development of humans. Considering the cleanliness and sustainability of H2 consumption, H2 yield and storage technology have received widespread attention.4

H2 can be produced by electrolysis of water, photosynthetic H2 evolution, industrial by-product reforming, and biofermentation.5 The sophisticated types of equipment and high capital investment that are required for the previous three methods limited the possibility of industrial application. Researchers have been looking for a low-cost and easy-to-operate process to produce H2.6 Biofermentation for H2 production includes dark fermentation (DF), photo-assisted process, and their combination. Although the latter two processes are faster in H2 synthesis and have higher substrate conversion rates, both involve the use of light sources, likely causing light pollution to the environment.7,8 In contrast, the DF is not only rapid and efficient in the substrate conversion to H2 and volatile fatty acids (VFAs) but also employs kitchen residue, agricultural waste, and organic wastewater to obtain H2.9 This measure alleviates environmental pollution, recovers some energy, and reduces the exploitation of nonrenewable energy sources.

Nonetheless, the actual H2 yield from DF was much lower than its theoretical value of 4 mol/mol glucose.10 This is due to the fact that (a) glucose may not be metabolized by the biochemical process of H2 evolution; (b) a part of glucose is consumed by the bacteria of assimilating microbes; and (c) the produced H2 is likely employed by the H2-consuming microbes. The high yield of H2 from DF can be improved by boosting the activity of relevant microbes. For example, by adding microelements (e.g., Co, Ni, Fe, Mn, Zn) essential for germs to the DF reactor.11 In addition, it has been revealed that metal NPs can not only interact with enzymes or membrane proteins on cells but also act as extracellular electron acceptors in cellular metabolic processes.12 Previous reports revealed that NPs had the quantum size effect (QSE) and high surface area (HSA), and conductive NPs could quicken the electron transfer (ET) between cells, within microbes and between enzymes at lower concentration levels.13,14

Based on the aforementioned factors, many researches were conducted to explore the influence of monometallic trace element-induced NPs on H2 evolution in DF reactors and found that the H2 generation was significantly enhanced. For example, some NPs released Ni2+, Fe0, and Fe2+ and increased H2 yields by 55, 37, and 15%, respectively, in contrast with the control yield.15 Cobalt (Co) is the vital element of coenzyme B12 (C72H100CoN18O17P), and its adequate dosage can evidently alleviate the accumulation of VFAs in DF, indicating that the appropriate Co-induced DF reaction favors microbial activity.16 Zhang et al.17 discovered that NiO NPs extracted from Eichhornia crassipes increased the H2 production rate (HPR) by 47.29% compared with the control yield of mesophilic DF.17 In addition, ferredoxin hydrogenase was extremely crucial in the DF for producing H2, and Yang et al.18 revealed that an appropriate dosage of lanthanum–iron oxide NPs was favorable for the synthesis of ferredoxin hydrogenase via DF.18 Hydrogenase is the key enzyme in catalytic DF that converts the NADH produced along with the decomposition of glucose into H2 and NAD+.19 They are mainly divided into [Ni–Fe] and [Fe–Fe] hydrogenase in view of the central active metal, and the former was more frequently found in microbes than the latter.15,20 It has been reported that the addition of alkali-based magnetic nanosheets to the DF reactor at mesophilic and thermophilic conditions increased the activities of hydrogenase by 10.5 and 42.8% and their H2 yields by 65.4 and 43.3%, respectively.21 The reason for the promoting effect of nickel on bioH2 production was described as the metal cofactor of the active center of [Ni–Fe] hydrogenase.22 Also, the work illustrated that the addition of Ni NPs and Ni–graphene nanocomposite to industrial wastewater could increase H2 yield by 23 and 105%, respectively.22 Nanoscale metal oxides are less toxic to microbess than pure metal NPs.23 The related study on the DF for H2 generation amended with TiO2 was performed by Hsieh et al.,24 where the stimulation mechanism attributed to the ET within the H2–DF of Clostridium pasteurianum.24

Nevertheless, to our knowledge, NiCo2O4 NPs not have been reported for bioH2 production by the DF reaction. Therefore, the main tasks in this work are (a) to synthesize NiCo2O4 NPs and characterize them; (b) to reveal the influence on bioH2 production by DF under 37 °C conditions in different dosages of NiCo2O4 NPs; (c) to detect and analyze the intermediate products in the DF process; (d) to uncover the microbial community variation at different doses of NiCo2O4 NPs; and (e) to predict the functional genes for bacteria after the DF procedure.

2. Materials and Methods

2.1. Inoculums Production

The inoculums used for this work were obtained from the wastewater-containing citric acid treatment plant in Shandong of China. To breed H2-producing bacteria (HPB), the inoculated sludge needs to be domesticated and cultured in anaerobic condition at 37 °C without nutrients for 20 days and then an oil bath for 45 min at 90 °C for enriching HPB and restraining methanogens. Then, the preheated sludge was cooled to 37 °C, and 1.0 g/L of glucose was added followed by DF at 37 °C for 48 h. Thus, the inoculums of H2–DF were obtained and then characterized for its physicochemical properties based on the methods of Sun et al.25 and the results are presented in Table 1.

Table 1. Physicochemical Properties of Inoculated Sludge.

physical and chemical indexes seed sludge
pH 7.0 ± 0.1
total solid (TS, wt.%) 12.5 ± 0.3
volatile solid (VS, wt.% of TS) 52 ± 0.8
chemical oxygen demand (COD, mg/L) 7289 ± 55
total organic carbon (TOC, mg/L) 2569 ± 60
total carbon (TC, mg/L) 3074 ± 70
inoraganic carbon (IC, mg/L) 505 ± 25
ammonium (NH4+–N, mg/L) 476 ± 15
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2.2. NiCo2O4 NPs Preparation

The NiCo2O4 NPs used in this work were fabricated by sol–gel means. The specific process was as follows: (a) Ni(NO3)2·6 H2O (0.01 mol, 2.91 g) and Co (NO3)2·6 H2O (0.02 mol, 5.83 g) were fully dissolved in 60 mL of deionized water. (b) Citric acid monohydrate (0.045 mol, 9.46 g) was mixed with the above solution and stirred to form a stable and clear liquid. (c) Ammonia was added slowly dropwise to regulate the pH to 2.0, and the liquid was stirred at 80 °C for 120 min to produce a gel and then dried in a drying cabinet at 115 °C for 300 min. (d) The intermediate was incinerated at 700 °C for 4.5 h; subsequently, the calcined sample was cooled to room temperature and purified with deionized water and ethanol alternately 2 times. (e) The purified product was dried under vacuum conditions at 60 °C, and then NiCo2O4 NPs were obtained, which were milled into powder and stored in an airtight condition.

2.3. Batch Fermentation Process

Three sets of parallel experiments were designed for this study. All DF tests were conducted in the 500 mL DF reactor with a remaining volume of 125 mL for reducing the DF H2 partial pressure. Then, inoculum (150 mL) and substrate (glucose 10 g/L, peptone 0.3 g/L) were added to each DF reactor. In addition, seven concentration gradients of NiCo2O4 NPs (0, 50, 100, 200, 400, 600, and 800 mg/L) were added to the above reactor to evaluate the effect on bioH2 yield from DF at 37 °C. The initial pH values of all reactors were near neutral (7.0) without regulation. To provide an anaerobic environment for microbes, all reactors were purged with nitrogen for 3 min and sealed quickly, and then they began to produce H2 under mesophilic conditions (37 °C) and lasted for 36 h. Finally, the generated H2 was collected by the saturated NaOH solution to remove the interference of acidic gases such as CO2 and H2S. The H2 yields were determined every 3 h, while fermentation liquids were sampled every 6 h for chemical characterization. Moreover, H2 measurement and determination need to follow a previous work.26

2.4. Determination of NiCo2O4 NP Characteristics

The crystal structure and phase component of NiCo2O4 NPs were revealed with an X-ray diffraction (XRD, AXS, Bruker, Germany) at an angle of 2θ in the range of 10–80°, maintaining a scanning rate of 20°/min. NiCo2O4 NPs were analyzed by the versatile scanning electron microscopy (SEM) (S4800, Hitachi, Japan) with an energy dispersive spectrometer (EDS) (X-MAX80, Oxford, UK) for their morphological and elemental composition, where the EDS model was Xplore, and the gold spray target was a platinum target. The surface area of NiCo2O4 NPs was estimated by the Brunauer–Emmett–Teller detector (BET, ASAP2460, Micromeritics, USA). In addition, the elemental composition and chemical states of NiCo2O4 NPs were revealed through an X-ray photoelectron spectrometer (XPS, ESCALAB 250Xi, Thermo Scientific, USA) using Al Kα X-rays as the excitation source.

2.5. Liquid Analysis

The key physicochemical indicators of seed sludge, such as total organic carbon (TOC), inorganic carbon (IC), total solids (TS), volatile solids (VS), ammonium (NH4+–N), pH, and chemical oxygen demand (COD) were gauged consistent with the former methods.21 First of all, the collected samples of fermentation broth were centrifuged at 7000 r/min for 5 min and then filtrated with a filter membrane with a pore size of 0.45 μm. The SMPs such as HAc (acetate), HPr (propionate), HBu (butyrate), EtOH (ethanol), and glucose were evaluated by high-performance liquid chromatography (HPLC, LC-20AT, Shimadzu, Japan) with a detector of refractive index. Sulfuric acid (0.005 M, 0.5 mL/min) was utilized as the mobile phase, which was equipped with an Aminex HPX-87H column and Cation-H cartridge microguard. The contents of nickel and cobalt ions in the zymotic fluid were determined by an inductively coupled plasma emission spectrometer (ICP–OES, Optima 7000DV, Perkin Elmer, MA, USA).

2.6. Three-Dimensional Fluorescence Assay and 16S rRNA Gene Amplicon Sequencing

The extracellular polymers (EPS) were extracted from the final sludge after DF and based on previous techniques,27 which were obtained from the control, the highest, and the lowest H2 yield samples. To determine the EPS characteristics, these sludge samples (15 mL) were centrifuged (6000 r/min, 10 min), and they were dissolved in Ringer solution (150 mmol/L NaCl, 2.5 mmol/L CaCl2, 4.0 mmol/L KCl), and then heated for 35 min at 60 °C. Subsequently, the suspension fluids were concentrated (9000 r/min, 3 °C, 15 min), and then each supernatant liquid was collected to filter via a 0.22 μm filter membrane. Finally, the filtrates were scanned at 2400 nm/min through a fluorescence spectrometer (F-7100, Hitachi, Japan) with excitation (EX) and emission (EM) wavelengths in the range of 200–600 nm at an interval of 5 nm, for obtaining their spectrograms of three-dimensional excitation–emission matrixes (EEM). Also, the paired-end sequencing of community DNA fragments was revealed through 16S rRNA gene pyrophosphate sequencing to evaluate structural changes in microbial communities. The total DNA was extracted and quantified using the Qubit dsDNA HS. Moreover, the V3 and V4 areas of the 16S rRNA gene were obtained by amplification of 30 ng of DNA as a template where they employed the upstream and downstream primers of ACTCCTACGGGAGGCAGCA and CGGACTACHVGGGTWTCTAAT, respectively. After completing these gene sequence tests, the amplified products were purged and reclaimed by small magnetic beads and quantified by fluorescence with a microplate reader (BioTek, FLx800, Agilent, America). Finally, high-throughput sequencing and gene libraries were prepared using the Illumina TruSeq Nano DNA LT Library Prep Kit.26

2.7. Analysis of Variance and Kinetic Modeling

To investigate whether the effects of NiCo2O4 NPs added in the DF on the amount of bioH2 was statistically significant, the average with standard deviations of the three parallel experiments were calculated and analyzed by one-way ANOVA using Origin 2021 software to calculate P values, where P < 0.05 was significant. The average values were fitted by the modified Gomperz model (eq 1) for evaluating the kinetic process of H2 generation via DF. Thus, the kinetic values such as the lag phase, maximum H2 yield, and maximum H2 production rate (HPR) were used to evaluate the correlation coefficient (R2).18

2.7. 1

where t (h) = DF time, P(t) = H2 yield (mL/g glucose), Pm = maximum H2 yield (mL/g glucose), e = 2.72, Rm = maximum HPR (mL/g glucose·h), and λ = lag phase (h).

3. Results and Discussion

3.1. Characterization of NiCo2O4 NPs

The morphology, crystal texture, elemental composition, and surface area were detected to explore the effect of NiCo2O4 NPs on H2 generation on DF, which are revealed in Figure 1.

Figure 1.

Figure 1

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NiCo2O4 NPs XRD graphic (a); SEM–EDS graphic of NiCo2O4 NPs (b); SEM graphic of NiCo2O4 NPs at 1 μm (c); element distribution of SEM mapping (d–h).

In Figure 1a, the XRD spectra revealed the typical spinel structure: diffraction peaks at 2θ = 18.9, 31.1, 36.6, 38.4, 44.6, 53.8, 59.0, and 64.9° corresponded to the characteristic peaks of the standard spectrum of Joint Committee on Powder Diffraction Standards (JCPDS) with card number 20–0781. Also, there were no impurity peaks in the XRD spectra as a whole, which indicated the high purity of the prepared material. In addition, the narrow and sharp diffraction peaks illustrated that the NiCo2O4 NPs had a high proportion of crystalline regions, thus making the material less susceptible to damage.28,29 In addition, Figure 1b describes the EDS pattern; the mass percentages of Ni, Co, and O were 12.9, 62.8, and 19.0% respectively. Figure 1c exhibits the SEM images of NiCo2O4 NPs with a 20,000 magnification, which showed the appearance with a polyhedral shape. In addition, the particles were relatively uniform and smooth, where NiCo2O4 NPs were slightly agglomerated due to van der Waals forces.30 The elemental mapping (Figure 1d–h) revealed the distribution of Ni, Co, O, and C. Moreover, the BET surface area of NiCo2O4 NPs was 12.4249 m2/g, and the average pore diameter for adsorption and desorption was between 1 and 14 nm (Table 2).

Table 2. BET Test Data of NiCo2O4 NPs.

item data
surface area BET surface area 12.4249 m2/g
pore size adsorption average pore diameter (4 V/A by BET) 13.2636 nm
  desorption average pore diameter (4 V/A by BET) 1.7022 nm
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Furthermore, the XPS technique was used to acquire the elemental composition and chemical bonds of NiCo2O4 NPs. Figure 2a reveals the full spectrum map of NiCo2O4 NPs and demonstrates the existence of Ni, Co, and O. This was not only consistent with the XRD characterization but also indicated the high purity of the NiCo2O4 NPs.

Figure 2.

Figure 2

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XPS spectrogram of NiCo2O4 NPs: full spectrogram (a); XPS spectrogram of O 1s (b), XPS spectrogram of Ni 2p (c); XPS spectrogram of Co 2p (d).

The existence of element C in the sample was the corollary of the material preparation when XPS analysis was performed. The orbital peaks at 529, 780, and 855 eV confirmed the presence of O 1s, Co 2p3, and Ni 2p3, respectively. The curves of O 1s revealed different oxygen components and were labeled as O 1 and O 2, respectively (Figure 2b). Figure 2b shows that the peak of O 1 corresponded to the typical metal– oxygen bond in the oxide and the binding energy value was 529.6 eV, while the O 2 peak at 530.9 eV was oxygen vacancies.31,32 The vacancies play part in mitigating the resistance of H+ movement and accelerating its shuttling in the surface layer.33 The Ni 2p profiles with two peaks at 855.2 and 872.3 eV for 2p2/3 and 2p1/3, respectively, indicate the existence of Ni2+ (Figure 2c). The peak at 860.5 eV ascribed the appearance of Ni3+, and the peak at 879.8 eV was the coexistence of Ni2+ and Ni3+.34 The profile of Co 2p exhibited two peaks of 2p3/2 and 2p1/2 at 780.1 and 795.5 eV, respectively, which signified the existence of Co3+ (Figure 2d). Meanwhile, the satellite peaks at 783.2 and 802.9 eV demonstrated the presence of Co2+.35

3.2. Effect of NiCo2O4 NPs on BioH2 Yield

The influences of NiCo2O4 NPs at seven dosage levels on the bioH2 generation by DF are depicted in Figure 3, where Figure 3a shows the variation of H2 yield with DF time and Figure 3b represents the HPR.

Figure 3.

Figure 3

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Effect of different doses of NiCo2O4 NPs on bioH2 production by DF: (a) bioH2 yields; (b) rates of bioH2 yield; (c) effect of different dosages of NiCo2O4 NPs on SMPs and glucose; (d) change of glucose and SMPs with 400 mg/L NiCo2O4 NPs.

It can be found that H2 synthesis started at the 9th hour and almost completely ended at the 24th hour. The moderate amount of NiCo2O4 NPs (400 mg/L) could facilitate bioH2 generation, and the largest H2 production of 259.67 mL/g glucose was reached at the addition of 400 mg/L, which increased by 33.97%, matching with the control yield (193.82 mL/g glucose). Table 3 provides the increased value of different materials on the total bioH2 yield when DF was performed with glucose as substrate, indicating that this experiment was at a higher level of bioH2 synthesis.21,24,25,36

Table 3. Comparison of H2 Production by DF under Different Conditions.

substrate inoculum initial pH/ DF temp. additives/dosage (mg/L) H2 yield(mL/g) reference
glucose anaerobic sludge 6.9, 37 °C AMNSs/100 232.8 Cao et al.21
glucose anaerobic sludge 7.0, 55 °C AMNSs/400 150.3 Cao et al.21
glucose C. pasteurianum 7.0, 35 °C Fe/50 255.7 Hsieh et al.24
glucose anaerobic sludge 7.0, 37 °C MnFe2O4/400 272.7 Sun et al.25
glucose anaerobic sludge 7.0, 37 °C Fe3O4/100 198.30 Sun et al.36
glucose anaerobic sludge 7.0, 37 °C Fe3O4-rGO NCs/100 225.60 Sun et al.36
glucose anaerobic sludge 6.9, 37 °C NiCo2O4/400 259.67 this work
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Cao et al.21 used alkali-based magnetic nanosheets (AMNSs) (100 mg/L) to increase H2 yield via DF and obtained the highest yield of 232.8 mL/g glucose, being lower than that (259.67 mL/g glucose) from this work.21 Similarly, Sun et al.25 obtained the largest H2 yield of 272.2 mL/g glucose amended by 400 mg/L manganese ferrite NPs, which was slightly higher than that of this study.25 Moreover, NPs entered the cell and increase intracellular ET, thereby accelerating the synthesis of bioH2.36 Nonetheless, there are still some difficulties in comparison to the H2 yields, mainly due to their different additives and anaerobes in DF systems. A previous work reported that NPs may attach to bacteria and interact with structural proteins on the membrane in bioH2 synthesis via DF.21,36 A further increase in NiCo2O4 NPs (more than 400 mg/L) resulted in a decrease in H2 yield. The production of H2 was 188.14 mL/g glucose when the dosage of NiCo2O4 NPs up to 800 mg/L, which reduced to 97% of the control yield. A study about DF utilizing potato peel as substrate had similarly concluded that excess Fe3O4 NPs led to the death of anaerobes due to oxidative stress.37 Other studies showed that cell membranes acted as transport channels for metal ions, but excess metal ions could lead to impaired membrane due to problems with protein. The above reasons inhibit the activity of microbial and even lead to their death, likely causing a decline in the H2 yield when the dosage of NiCo2O4 NPs exceeded 400 mg/L. Figure 3b reveals the variation of HPR with DF time. The trend of HPR over time was approximately the same in all groups, with bioH2 synthesis after the 9th hour and peak period at 12–15 h. The highest HPR value of all DF groups was 48.74 mL/g/h and reached 400 mg/L NiCo2O4 NPs, which was increased by 64.77% with the control HPR (29.58 mL/g/h), providing evidence for the ability of NiCo2O4 NPs to promote DF for H2 yield.

3.3. Dynamical Analysis and Mathematical Statistics

The H2 generation via DF was conformed to the modified Gompertz equation; the detailed records are presented in Table 4. The kinetic fitting study illustrated that the lag phase (λ) was between 11 and 12 h for all DF groups, and the maximum H2 yield and HPR were also in general agreement with the experiment data. In addition, the fitted correlation R2 was greater than 99%, which not only indicated a successful fit of datas but was also consistent with the results of Figure 3. A slight drop of trend showed in λ with the increasing doses of NiCo2O4 NPs, but when NiCo2O4 NPs outnumbered 400 mg/L, the λ increased instead. Interestingly, even at 400 mg/L of NiCo2O4 NPs dosing, its λ (11.42 h) was a little greater than that of the control group (11.31 h). This showed that NiCo2O4 NPs prolonged the DF lag period slightly. Also, this may be related to the inhibition of HPB by NiCo2O4 NPs at the start of DF, similarly found by Zhang et al.38 In this study, the lag phase with the highest H2 yield was 0.11 h longer than that of the control group. Moreover, one-way ANOVA was performed by Origin 2021 software for SMPs, HBu and H2 yields at seven dosage levels of NiCo2O4 NPs, and the results are described in Table 5. There was a correlation between NiCo2O4 NP dosage and SMP, HBu, and H2 yield, as the p-values were all below 0.005. In addition, the final pH values of all DF were between 4.75 and 4.95, reaching the stable pH level at the end of DF (4.8–5.0).39

Table 4. Kinetic Parameters of bioH2 by DF and Final pH.

NiCO2O4(mg/L) Pm(mL/g) Rm(mL/(g·h)) λ (h) R2 (100%) final pH
0 194.09 28.94 11.31 99.89 4.81 ± 0.1
50 221.86 41.91 11.65 99.94 4.86 ± 0.1
100 229.95 42.11 11.60 99.96 4.93 ± 0.1
200 247.01 46.69 11.58 99.97 4.81 ± 0.1
400 259.81 50.91 11.42 99.96 4.76 ± 0.1
600 237.56 48.72 11.61 99.99 4.81 ± 0.1
800 188.52 33.54 11.82 99.93 4.95 ± 0.1
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Table 5. One-Way ANOVA in all Groups.

project p-H2 p-SMPs p-HBu p-Ni ions p-Co ions
value <0.05 <0.05 <0.05 <0.05 <0.05
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3.4. Impact of NiCo2O4 NPs on SMPs

To probe the influence of different doses of NiCo2O4 NPs on the DF, the SMP composition of the zymotic fluid was measured for all groups and the outcomes are exhibited in Figure 3c. The SMPs showed an increasing trend during the DF process with the proper NiCo2O4 NPs added (0–400 mg/L). When the NiCo2O4 NPs was injected at 400 mg/L, the SMPs reached the highest level of 5860 mg/L and was a 28.34% increase over the control SMPs (4570 mg/L). Figure 3d supplies the changing trends of glucose decomposition and SMPs yield from the 400 mg/L NiCo2O4 NPs (the highest H2 yield group), which changed rapidly during 6–18 h of DF. Whereas, the SMPs decreased to 97.4% when NiCo2O4 NPs was up to 800 mg/L. Different addition levels proved that NiCo2O4 NPs promoted the conversion rate of substrate within a certain range (0–400 mg/L), which coincided with H2 yield. SMPs decreased with increasing NiCo2O4 NPs (more than 400 mg/L) due to the irreversible damage about organelles and genetic material caused by excessive NPs crossing the cell membrane.40 The liquid phase products generated by DF were more favorable for H2 yield when HBu and HAc were predominant. Because the theoretical values of H2 evolution for different DF pathways were not equal, the theoretical H2 yields were 4 and 2 mol for 1 mol of glucose through the HAc and HBu metabolic pathways, respectively.41 As shown in Figure 3c, the HAc and HBu accounted for 26–31% and 58–62% of SMPs, respectively. They were much larger than the sum (10–16%) of HPr and EtOH from the SMPs in all DF groups, proving that the H2–DF was mainly HBu and HAc pathways.

3.5. Dissolution of NiCo2O4 NPs and the Effect on EPS

To investigate the effects of the NiCo2O4 NPs on the DF liquid phases, Ni and Co ions were detected and the outcomes are exhibited in Figure 4. NiCo2O4 NPs released trace amounts of Co and Ni ions in the H2–DF process, and their concentrations in DF broth was increased with the addition of NiCo2O4 NPs. Furthermore, the p-values for Ni and Co ions concentration calculated from the one-way ANOVA were not greater than 0.05, which indicated that the dosing of NiCo2O4 NPs at different levels had an obvious influence on the concentrations of Co and Ni ions in the DF liquid (Table 5). In addition, the Co ions in each group of zymotic fluid are slightly more than twice that of Ni ions, probably owing to the use of Ni2+ by the germs. Li et al.42 demonstrated that microbes utilized the element Ni when shrimp shell biochar loaded with nickel was applied for methanogenesis studies.42 Moreover, EPS was a gelatinous polymer secreted by microbes that existed outside the cell, and its function was to protect bacteria. The control (0 mg/L), highest (400 mg/L), and lowest (800 mg/L) H2 yield groups were measured for the identification of fluorescent dissolved organic compounds. Generally, EEM analysis was not precise because it was a semiquantitative technique.43 The five regions were divided according to the range of excitation (EX) and emission (EM) wavelengths and represented different substances; the specific partition method was referred to previous studies.18

Figure 4.

Figure 4

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Ni and Co ion concentrations in the final fermentation broth of each group.

In Figure 5, there were no significant differences in the regions of I (tyrosine-like proteins), II (tryptophan-like proteins), and III (fulvic acid-like organics) for three groups, while there were obvious discrepancies in IV (soluble microbial metabolites) and V (humic acid-like). The fluorescence intensity in region IV was evidently stronger in the highest H2 yield group than that of the others. This agreed with the detection results of SMPs, once more providing new evidence that a moderate amount of NiCo2O4 NPs (400 mg/L) played vital roles in the utilization of substrate and production of SMPs. Region V represented humic acid-like, whose structure included an amount of oxygen-containing functional groups that were difficult to biodegrade.44 Although its distribution on the outside of the cell played a role in protecting microbes, at high concentrations, it can also lead to a hindrance in the uptake of nutrients by the germs, as its gelatinous nature leads to an increase in viscosity on the outside of the cell.35 Furthermore, humic acid-like can also cause changes in the enzyme particle size and the structure of amino acids by binding to biological enzymes, thereby loosening the structure of protease and reducing its activity.45 Some metal ions can mitigate the inhibition of polysaccharides and relate enzymes by complexing with humic acid-like.46 The intensity of mitigation is related to the type and concentration of metal ions, and the alleviating of humic acid-like by bimetallic ions can obtain a synergistic effect of 1 + 1 > 2.47 The fluorescence responses of the control and the lowest H2 yield groups were not significantly different in region V, but they responded more strongly than that of the highest H2 yield DF group. This phenomenon was attributed to the better complexation of dissolved Ni2+ and Co3+ with humic acid-like via electrostatic force, cation exchange, and sweep flocculation in the DF reactor with 400 mg/L of NiCo2O4 NPs (the highest H2 yield), resulting in the reduced fluorescence intensity in region V (humic acid-like). This suggested that the moderate amounts of NiCo2O4 NPs could reduce humic acid-like. This was obviously favorable to high H2 yield, and the reason may be the shielding effects of Ni and Co ions released from NiCo2O4 NPs. While the enhanced fluorescence intensity of the lowest H2 yield group was likely attributed to the excessive release of Ni and Co ions from DF broth, the strong mutual repulsion between positive charges could hinder the mutual binding between metal ions and humic acid. Li et al.47 proved that the shielding effect on humic acid decreased with increasing Ca2+ and Al3+ at dosages higher than 100 and 70 mg/L, respectively.47

Figure 5.

Figure 5

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EEM spectra s of EPS from final DF: (a) 0, (b) 400, and (c) 800 mg/L.

3.6. Effect of NiCo2O4 NPs on Microorganisms

Since different bacteria have different tolerance toward NiCo2O4 NPs, the fermented sludge from the control group (0 mg/L), the highest (400 mg/L), and lowest (800 mg/L) H2 groups was taken for a microbiological assay by 16S rRNA gene sequencing technology.48 The reliability of the sequencing was confirmed by the valid sequence numbers of the three samples ranging from 70,400 to 76,684, and the good coverage were 0.999 in all cases. In addition, the Shannon index of germs in DF systems with 0, 400, and 800 mg/L NiCo2O4 NPs dosages were 6.31099, 6.00387, and 5.93574, respectively. This result corroborated that NiCo2O4 NPs reduced the microbial diversity because the Shannon index represented the level of biodiversity and they were positively correlated. Analogous phenomena were investigated by Zhang et al.14 who concluded that the Shannon indexes that matched with control samples in mesophilic and thermophilic conditions were decreased by 0.338 and 0.036, respectively.14Figure 6 illustrates the microbial profile of the three samples at the phylum and genus levels.

Figure 6.

Figure 6

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Microbial communities at different NiCo2O4 NPs additions: (a) phylum; (b) genus (top 5 of the samples).

The Firmicutes’ abundance was absolutely dominant in the grade of phylum (Figure 6a), which could form spores to resist harsh environments in very short periods, and break down substrates to obtain H2.49 The abundance of Firmicutes in the highest H2 yield group (400 mg/L, 84.04%) increased by 6.61% comparing with the control group (0 mg/L, 77.43%). Meanwhile, the relative abundance of Firmicutes in the lowest H2 yield group (800 mg/L, 74.90%) was reduced by 2.53%, matching the control abundance. A homologous phenomenon was that a moderate amount of Fe3O4 NPs could heighten the abundance of Firmicutes in DF confirmed by previous research.50 Interestingly, the relative abundance of Firmicutes in the previous studies was 35–49 and 29–42%, respectively, with or without the addition of NPs to the H2–DF system, being much lower than the proportion of Firmicutes in this work (74.90–84.04%).26,35 The reason why Firmicutes in this work was much greater than that in the previous two studies was probably due to the better sludge cultured. A similar finding was reported that the more Firmicutes in the H2–DF reactor, the more H2.51 The microbial structural distribution at the genus level is described in Figure 6b. Clostridium sensu stricto1 had absolute predominance, and there were no significant differences in the abundance of other bacteria. The proportions of Clostridium sensu stricto1 from the highest (400 mg/L, 71.48%) and lowest (800 mg/L, 50.95%) H2 yield groups were 1.23 and 0.88 times higher than that of the control (58.08%), respectively. H2 yield was positively correlated with Clostridium sensu stricto1, being attributed to the fact that such bacteria could convert glucose into H2.52 In addition,Clostridium sensu stricto1 pertained to Firmicutes, agreeing with the changes of microbial assays at the phylum level.53

Moreover, the effect of NiCo2O4 NPs on the microbes in the H2–DF system at the species level was demonstrated in Figure7a. It can be seen that Clostridium butyricum (C. butyricum) was absolutely dominant. The relative abundance of C. butyricum corresponding to the NiCo2O4 NPs supplemented with 0, 400, and 800 mg/L were 49.88, 62.51, and 43.90%, respectively. The C. butyricum of the latter two groups increased by 25.32% and decreased by 11.99% compared with the control sample. A moderate amount (400 mg/L) of NiCo2O4 NPs was instrumental in the multiplication of C. butyricum, while excess NiCo2O4 NPs led to the opposite result. These phenomena accorded with the microbial structure in genus levels. The C. butyricum is a typical dominant microbe in the HBu pathway of H2–DF. Fu et al.54 also illustrated that Raney nickel, nickel, and copper particles contribute to its growth and reproduction.54 This study confirmed that appropriate dosing of NiCo2O4 NPs (400 mg/L) promoted that the reproduction of C. butyricum dominated in Clostridium sensu stricto1, thereby facilitating the HBu–DF for more bioH2. However, a decrease in C. butyricum was revealed when the dose of NiCo2O4 NPs was greater than 400 mg/L, which was consistent with the total amount of SMPs and H2.

Figure 7.

Figure 7

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(a) Relative abundance of microbial species levels under different NiCo2O4 NPs addition conditions; (b) Predicted abundance of genes encoding key enzymes in different NiCo2O4 NPs addition groups.

3.7. Predicted Functional Analysis of Genes in HPB

For further comprehension of the pathways of substrate transformation by bacterial communities in DF systems, the 16S rRNA gene sequences of the microbial genome were compared with those of the Kyoto Encyclopedia of Genes and Genomes (KEGG) by PICRUSt software. Also, the predicted absolute abundance of key genes is exhibited in Figure 7b. Genetic predictions indicated that the DF processes enriched for gene expression that converted glucose to phosphoenolpyruvate: pyruvate kinase, the rate-limiting enzyme in the glycolytic phase.18 The H2–DF groups with NiCo2O4 NPs of 400 and 800 mg/L, elevated by 16.1% and reduced by 3.8%, respectively, compared with the control sample, indicating that adequate addition (400 mg/L) of NiCo2O4 NPs was profitable to the glycolytic process. More importantly, most of the H2 in the DF process is generated under the catalysis of ferredoxin hydrogenase: 2 H+ + 2 reduced ferredoxins < = > 2 oxidized ferredoxins + H2, which are the most significant H2-producing enzymes.55 In this work, the predicted absolute abundance of the gene encoding ferredoxin hydrogenase in the group of 400 mg/L NiCo2O4 NPs added was enhanced by 68.7% of the control one, but there was no obvious variation in the group supplemented with 800 mg/L NiCo2O4 NPs. In addition, pyruvate ferredoxin oxidoreductase participates in the reaction: 2 oxidized ferredoxin + CoA + pyruvate = 2 reduced ferredoxin + acetyl-CoA +2 H+ + CO2. The reduced ferredoxin catalyzes the proton to H2 by hydrogenase or ferredoxin hydrogenase. Interestingly, the predicted genes abundance of encoding pyruvate ferredoxin oxidoreductase and [Fe–Ni] hydrogenase in this work increased with the increasing doses of NiCo2O4 NPs and both being the highest at the dose of 800 mg/L, with an enhancement of 12.5 and 19.8% over the control, respectively. Gene prediction results proved that 400 mg/L of NiCo2O4 NPs in H2–DF increased the abundance of genes encoding glycolytic processes and other enzymes related to H2 yield. In addition, the predicted levels of genes encoding acetyl–CoA synthetase, acetate kinase, butyrate kinase, etc., were elevated to varying degrees when 400 mg/L NiCo2O4 NPs were added. This was in line with the changes of the SMP assay. In addition, the common strains in the DF-H2 generation pathway with HAc and HBu as products all belong to Clostridium, being in line with the results of the detection of microbes in this work.21,56−58

3.8. Mechanism of BioH2 Yield Improvement

The mechanisms of NPs in bioH2 production through DF in former works are summarized as follows: (a) optimizing microbial community structure; (b) changing EPS; (c) accelerating ET. Furthermore, Zhang et al.14 and Li et al.59 uncovered that NPs could attach to bacteria and interact with structural proteins on the membrane in a work about DF.14,59 In this work, more detailed probable H2 enhancing mechanisms were proposed: (a) By virtue of the QSE and HSA of NiCo2O4 NPs, not only the rate of ET between HPB can be accelerated but also the synthesis of hydrogenases. (b) Ni participates in the synthesis of [Fe–Ni] hydrogenase and acetyl–CoA synthase. The former facilitates the catalytic reduction of protons to H2, while the latter is a key intermediate in the yield of SMPs. (c) NiCo2O4 NPs can adhere to the cell surface or enter the cell, thus facilitating the ET process. (d) The Co and Ni ions released by NiCo2O4 NPs provide HPB with important trace elements required for multiplying, thus optimizing the community structure of bacteria. (e) Ni and Co ions released from NiCo2O4 NPs relieved the inhibitory effect of humic acid-like. (f) NiCo2O4 NPs promoted the expression of key genes in the DF process.

4. Conclusions

NiCo2O4 NPs was prepared to improve the H2 productivity by DF. The highest H2 production (259.67 mL/g glucose) was achieved at the NiCo2O4 NPs supplemented with 400 mg/L, which was enhanced by 33.97% compared to the control sample (193.82 mL/g glucose). In addition, the relative abundance of C. butyricum increased by 25.32%, promoting the HBu pathway. The inhibitory effect of humic acid-like in H2–DF was effectively alleviated. Gene predictions indicated that the abundance of genes encoding key enzymes related to H2 synthesis were enhanced by NiCo2O4. This work provides a theoretical basis for the achieve energy recovery of DF treating food processing wastewater.

Acknowledgments

This work is funded by the Natural Science Foundation of Shandong Province (ZR2016EEM33) and the Foundation (ZZ20210125) of State Key Laboratory of Biobased Material and Green Papermaking, China.

Author Contributions

Z.L: investigation, writing and editing, visualization, and methodology;J.W: writing and methodology; K.T: review and editing; C.Z: formal analysis and data curation; Y.P: formal analysis; J.Z: conceptualization, review and editing, funding acquisition and Supervision; L.Z: project administration.

The authors declare no competing financial interest.

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