Improvement of Biohydrogen Production from Dark Fermentation by

Oct 11, 2017 - In several types of immobilization carriers, activated carbon (AC) has been well-documented as a support matrix in dark fermentation. ...
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Improvement of Biohydrogen Production from Dark Fermentation by Cocultures and Activated Carbon Immobilization Cunsheng Zhang,*,†,‡ Xinxin Kang,† Nini Liang,† and Abdumutalip Abdullah† †

School of Food and Biological Engineering, Jiangsu University, Zhenjiang 212013, China Key Laboratory for Solid Waste Management and Environment Safety (Tsinghua University), Ministry of Education of China, Beijing 100084, China

‡

ABSTRACT: To improve biohydrogen production, the performance of dark fermentation by cocultures and the immobilization system with activated carbon (AC) were investigated. Results of batch tests illustrated that lower yield was obtained by monoculture Enterobacter cancerogeous HG6 2A (A) and Enterobacter homaechei 83 (B). The defects of monocultures could be overcome by cocultures in dark fermentation. The optimum A:B number ratio of 0.9:1 was recommended. The optimum loading rate of AC was 200 g/L in the immobilization system, corresponding to the biohydrogen yield of 1.203 mol/mol-glucose. The biohydrogen production of the immobilization system increased 259% in comparison to that of the suspension cell system, indicating that immobilization was an effective method of improving biohydrogen production. The surface attachment and the synergistic effect explained the higher performance of the cell immobilization system.

1. INTRODUCTION The increasing energy demand and environmental pollution issues have impelled researchers to develop renewable energy.1 Currently, much attention has been paid to biohydrogen because its energy content (122 kJ/g) is greater than that of fossil fuels and because it combusts without greenhouse gas emissions (such as NOx). Moreover, biohydrogen is a source that could be stored easily and safely in alloys and metals that can form hydrides.2 Because of these advantages, biohydrogen production from dark and photo fermentation has been extensively studied by researchers. Dark fermentation was considered to be a more promising approach for hydrogen production than photo fermentation because expensive and large surface area photo bioreactors are required for photo fermentation.3 Dark fermentation for hydrogen production is a microbial conversion process in which organic substrates such as starch, protein, lipid, cellulose, and glucose are decomposed by a series of biochemical reactions with the function of enzymes. According to the metabolic pathway, hydrogen dark fermentation can be divided into three types: propionate type, butyrate type, and ethanol type.4,5 For different types, the biohydrogen yield and the type and amount of volatile fatty acid (VFA) were obviously distinct.6 Thus, the components of VFA could be used as an indicator to identify the fermentation type. Currently, several categories of hydrogenogen, such as Clostridium sp., Bacillus sp., Brevumdimonas sp., and Enterobacter aerogenes, have been applied for biohydrogen production, and the values of their optimum hydrogen yield are between 1.0 and 2.8 mol H2/mol glucose depending on the microbes’ species.3,6−8 In addition to the metabolic pathway, biohydrogen production can also be influenced by several other factors such as pH, substrate type, organic loading rates, and microbial competition.9 It is extremely important to control the fermentation conditions at the optimum level for higher biohydrogen yield. © XXXX American Chemical Society

Previously many researches focused on pure culture fermentation, because the feedstock was consumed by only a single microbe without extra loss.10−12 Nevertheless, plenty of disadvantages of pure culture fermentation could be observed. First, the degradation of macromolecular substrates requires a series of enzymes. For pure culture fermentation, the fermentation efficiency was usually lower because of its lower production rate of enzymes which are required in substrate degradation. Second, bacteria growth needs a stable pH environment to maintain the activity of enzymes. Fermentation by pure culture which is sensitive to pH variation is prone to experience failure, leading to a lower conversion ratio of feedstock to biohydrogen as well as lower biohydrogen yield. Recently more and more studies have focused on cocultures because a higher biohydrogen yield could be obtained when two or more microbes ferment together.13−15 From the point of view of industrial application, cocultures are easier to operate and control, and they could also be applied in degrading a wide range of complex feedstocks without sterilization.16 The bacteria needs a stable environment for its rapid growth and metabolism. Many research efforts have been made to create a stable environment by immobilization. The immobilized cell systems can be classified into three types: surface attachment, self-flocculation, and gel entrapment approaches.17−19 Of all the methods, the surface attachment approach has attracted more and more attention because of its advantages: higher tolerance to environment perturbation, process stability, and higher biological activity. In several types of immobilization carriers, activated carbon (AC) has been well-documented as a support matrix in dark fermentation. AC has higher specific surface area and lower toxicity properties. Its highly porous structure and the surface, where the bacteria Received: July 13, 2017 Revised: September 17, 2017 Published: October 11, 2017 A

DOI: 10.1021/acs.energyfuels.7b02035 Energy Fuels XXXX, XXX, XXX−XXX

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Energy & Fuels

detector were 160, 180, and 180 °C, respectively. Argon was utilized as carrier gas with pressure of 0.08 MPa and a flow rate of 25 mL/min. To determine the concentrations of glucose and VFAs and pH of dark fermentation, liquid samples were collected. The pH was detected by a pH meter (Shanghai Sanxin, pHB-1). The concentration of glucose was determined by the 3,5-dinitrosalicylic acid (DNS) method.6 The VFAs of the liquid samples were measured by GC (GC2010 plus, Shimadzu, Japan), using a hydrogen flame ionization detector (FID) and a capillary column (Agilent 1909/N-133HP-INNOWAX 30 m × 0.25 mm). The temperature program of the column was 60 °C for 3.0 min; increased to 90 °C at a rate of 30 °C/min, maintained for 1.0 min; increased to 165 °C at a rate of 15 °C/min, maintained for 2.0 min; and increased to 230 °C at a rate of 15 °C/min, maintained for 2.0 min. The temperatures of the injection port and FID were 240 and 250 °C respectively. Nitrogen was used as carrier gas. The flow rates of nitrogen, hydrogen, and air were 35, 40, and 400 mL/min, respectively. 2.6. Kinetic Modeling. In order to determine the performance of hydrogen production by cultures A and B and their mixed cultures, the cumulative hydrogen production of each test was fitted to the modified Gompertz equation.25 The cumulative hydrogen production values were used to fit the modified Gompertz model using the software Origin 8.0.

could grow freely, help to sustain cell viability and enhance cell density.20,21 To the best knowledge of the authors, the reports on immobilization by AC for higher hydrogen production are quite limited.21−23 In our previous research, two cultures were screened from anaerobic sludge pretreated by alkali.24 The two cultures of A and B were indentified to be Enterobacter cancerogeous HG6 2A (A) and Enterobacter homaechei 83 (B), respectively. No report has been found in the literature that hydrogen could be produced from the two strains. To enhance the performance of biohydrogen production by cultures A and B, fermentation by cocultures and cell immobilization were investigated. Consequently, the purpose of this study was twofold: (i) assess the performance of fermentation by cocultures and (ii) examine the characteristics of immobilized system by cocultures.

2. MATERIALS AND METHODS 2.1. Enrichment of Hydrogenogen Bacteria. Cultures A and B were screened from anaerobic sludge pretreated by NaOH in our previous research.24 Prior to dark fermentation, the two cultures were enriched in different bottles with liquid medium for 12 h at 37 °C, forming bacterial liquid suspensions of A and B. The enriched bacteria number was calculated based on microscope measurements. The numbers of cultures A and B in liquid suspensions were 3.2 × 107 /L and 3.7 × 107 /L, respectively. 2.2. Medium Composition. The liquid medium composition was composed of glucose (20.0 g/L), tryptone (4.0 g/L), yeast juice (1.0 g/L), cysteine (0.5 g/L), NaCl (3.0 g/L), FeSO4·7H2O (0.1 g/L), MgCl2 (0.1 g/L), K2HPO4 (1.5 g/L), and trace element solution (10 mL/L). The composition of the trace element solution was ascorbic acid (0.025 g/L), citric acid (0.02 g/L), p-aminobenzoic acid (0.01 g/ L), MnSO4·7H2O (0.01 g/L), ZnSO4·7H2O (0.05 g/L), H3PO4 (0.01 g/L), CaCl2 (0.01 g/L), and CoCl2·6H2O (0.2 g/L). The medium was sterilized at 121 °C for 20 min. 2.3. AC Selection and Pretreatment. The particular AC was screened by a sieve, and the AC with particular size of 0.18−0.25 mm was selected for immobilization. The selected AC was first washed 5 times by distilled water, and then it was dried in a drying cabinet at 105 °C for 24 h. Finally, the selected AC was sterilized at 121 °C for 20 min before fermentation. 2.4. Experimental Design. 2.4.1. Dark Fermentation by Cocultures of A and B. Five groups (1−5) were designed to determine the influence of cocultures on biohydrogen production. Each group was added with 200 mL liquid medium, and 20 mL bacterial liquid was inoculated into each group at aseptic conditions. For groups 1, 2, and 3, the ratios of liquid suspensions A to B were designed to be 1:3, 1:1, and 3:1, respectively, corresponding to bacterial number ratios of 0.3:1, 0.9:1, and 2.6:1. The bacterial liquid suspensions of A and B were added into groups 4 and 5, respectively. After inoculum was mixed with the medium, each bottle was flushed with argon for 5 min to ensure an anaerobic environment. Dark fermentation was carried out at 37 °C in the 250 mL bottles with the effective volume of 220 mL. The fermentation gas was calculated by water displacement method with saturated salt water. 2.4.2. Immobilization of Dark Fermentative Bacteria by AC. Four groups were designed to measure the performance of dark fermentation immobilized by AC. The AC loading rates for groups 1, 2, 3, and 4 were 100, 200, 300, and 400 g/L, respectively. The adopted optimum A:B ratio was determined to be 0.9:1 (section 3.1). The other fermentation conditions were the same as those described in section 2.4.1. 2.5. Analytical Methods. The gas samples were collected during dark fermentation to detect hydrogen content. The composition of gas was measured using a gas chromatograph (GC7890B, Agilent, United States) equipped with a thermal conductivity detector (TCD) and a stainless steel column of TDX-01 (packed with carbon molecular sieve, 2 m × 3 mm). The temperatures of injection port, column, and TCD

3. RESULTS AND DISCUSSION 3.1. Dark Fermentation by Cocultures of A and B. Figure 1 shows the cumulative biohydrogen production from

Figure 1. Cumulative hydrogen production fermentation by cultures of A and B in suspension cell system.

cofermentation by cultures A and B and single fermentation by A and B. For single fermentation, biohydrogen production from dark fermentation by culture A could be finished quickly in 24 h. An obvious lag-phase time of 40 h (hour 20−60) was observed on culture B, resulting in a lower biohydrogen production rate of culture B in comparison to that of culture A. However, the total biohydrogen production of B (187 mL) was 57.1% higher than the production of A (119 mL), indicating that culture B had a higher hydrogen production potential than culture A. The order of biohydrogen production was: B > A:B (0.3:1) > A:B (0.9:1) > A:B (2.6:1) > A. This order illustrated that the greater the amount of culture B the greater the biohydrogen production was. However, a long fermentation time was required when A:B exceeded 0.9:1. From Figure 1 and the data of R2 in Table 1, it could be observed that the cumulative biohydrogen production fit well with the Gompertz B

DOI: 10.1021/acs.energyfuels.7b02035 Energy Fuels XXXX, XXX, XXX−XXX

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Energy & Fuels Table 1. Results from Dark Fermentation by Cultures of A and B group

A:B

1 2 3 4 5

0.3:1 0.9:1 2.6:1 1:0 0:1

H2 production (mL) 172 167 129 119 187

± ± ± ± ±

8.2 9.5 6.5 4.3 7.8

H2 content (%) 60.0 61.6 60.5 60.8 61.0

± ± ± ± ±

0.2 0.2 0.3 0.2 0.1

VFA (g/L) 3.4 4.0 3.0 2.7 4.2

± ± ± ± ±

0.3 0.4 0.3 0.2 0.4

final pH

P (mL)

Rm (mL/g-VS/h)

λ (h)

R2

± ± ± ± ±

172 168 129 120 −

6.3 9.3 11.0 9.1 −

12.5 9.7 9.5 9.6 −

0.9989 0.9988 0.9974 0.9980 −

4.7 4.9 4.8 4.8 4.7

0.2 0.1 0.1 0.1 0.2

equation except for culture B. The relative parameters of each group are shown in Table 1. The maximum cumulative hydrogen production (P) and the lag-phase time of groups 1, 2, and 3 were 172, 168, and 129 mL and 12.5, 9.7, and 9.5 h, respectively. Taking the maximum biohydrogen production and the lag-phase time into consideration, the optimum number ratio of A:B was determined to be 0.9:1 for fermentation by cocultures. The biohydrogen content shown in Table 1 illustrates the highest value (61.6%) was obtained at the A:B ratio of 0.9:1 (group 2). Moreover, the final VFA of group 2 was 4.0 g/L, which was higher than that of the other groups. However, a higher final pH value was observed in group 2, indicating a higher buffer capacity could be formed when A:B ratio was 0.9:1. As shown in Figure 2, the pH of group 5 (monoculture

Figure 3. Cumulative biohydrogen production of dark fermentation immobilized by AC.

the AC loading rate, while it decreased when the AC loading rate exceeded 200 g/L. These results showed that the optimum AC loading rate is 200 g/L, corresponding to the biohydrogen production of 599 mL. Compared with the control group shown in Figure 1 (A:B = 0.9:1), the biohydrogen production of dark fermentation immobilized by AC increased 2.59 times, indicating that cell immobilization was an effective approach for improving the biohydrogen production. Results of Figure 3 (fitting curves) and Table 2 (R2) illustrated that the biohydrogen production fitted well with the Gompertz equation at the AC loading rates of 100, 200, and 300 g/L. The highest P value and the lowest λ value were all obtained at the AC loading rate of 200 g/L. Moreover, the corresponding biohydrogen yield and the biohydrogen content were 1.203 mol/mol-glucose and 63.1%, respectively. These values were all higher than the values of the other groups, further illustrating that the AC loading rate of 200 g/L is the optimum condition for immobilization. It was worth noting that nearly all of the liquid in the fermentation system was adsorbed by the AC after 10 h. In this condition, no more biohydrogen was produced and no liquid sample could be collected in the system. Mass transfer strongly influences hydrogen production. Beckers et al. found that the hydrogen production rate of immobilization reactor could be affected by exchange surface area, stirring speed, and gas stripping.26 Addition of AC could limit the transfer coefficient of nutrients and metabolites by inhibition of fermentative microorganism. Nevertheless, AC could also provide a suitable matrix for cell adherence and colonization which helped hydrogen production. Consequently, both positive and negative effects could be caused by AC in the immobilization system, and the improvement of hydrogen production depends on the dosage of AC. In this research, an optimum AC dosage of 200 g/L was recommended. Lower dosage of AC could not provide ample

Figure 2. Variation of pH during fermentation process in suspension cell system.

B) was higher than group 4 (monoculture A), indicating that less VFA was produced during the lag-phase time by monoculture B. When cultures A and B were mixed, the long lag-phase time was conquered. Thus, it was concluded that culture B was lacking enzyme for glucose degradation at the initial fermentation time. For monoculture B, the hydrogen was mainly produced from hour 60 to hour 80 (Figure 1), and the corresponding pH range was 4.7−4.9 (Figure 2), indicating the optimum pH range for culture B was 4.7−4.9. In the cosystem, cultures A and B are mixed in different ratios. Glucose could be decomposed quickly by culture A, leading to a sharp decrease of pH. The lower pH might have motivated culture B to produce biohydrogen. Thus, the higher efficiency of the cosystem was attributed to the synergistic reaction of cultures A and B. 3.2. Immobilization of Dark Fermentative Bacteria by AC. 3.2.1. Biohydrogen Production. The results of biohydrogen production of dark fermentation immobilized by AC are shown in Figure 3. The biohydrogen production increased with C

DOI: 10.1021/acs.energyfuels.7b02035 Energy Fuels XXXX, XXX, XXX−XXX

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Energy & Fuels Table 2. Results of Dark Fermentation of AC Immobilization group

AC (g/L)

1 2 3 4

100 200 300 400

H2 yield (mol/mol-glucose) 0.934 1.203 0.753 0.301

± ± ± ±

0.03 0.04 0.02 0.01

H2 content (%)

P (mL)

Rm (mL/g-VS/h)

λ (h)

R2

± ± ± ±

476 611 382 −

25.6 49.5 28.1 −

9.76 9.52 9.62 −

0.9927 0.9939 0.9970 −

62.0 63.1 62.5 50.0

0.1 0.1 0.1 0.2

lowest pH was obtained at the AC loading rate of 100 g/L. These results indicated that the AC could play role of a buffer in weakening the acidity caused by VFA. The variation of VFA component during dark fermentation at the AC loading rate of 200 g/L is shown in Figure 5. VFA

matrix for higher cell density. Higher dosage of AC limited the transfer of nutrients and VFA, leading to a lower hydrogen yield (300 g/L AC) and even failure of fermentation (400 g/L AC). 3.2.2. VFA and pH. At the initiation of fermentation, no VFAs were detected in the culture medium. However, the accumulated VFA was observed as fermentation continued. The total VFA of each group increased to a stable level after 15 h. As shown in Figure 4A, the highest VFA was obtained at the AC

Figure 5. VFA component during dark fermentation with the AC loading rate of 200 g/L.

was mainly composed of acetate, propionate, butyrate, valerate, and caproate. Especially, the acetate and butyrate played the dominate role in VFAs. From Figure 3, the biohydrogen was mainly produced from hour 6 to 18 during which an obvious increase was observed on butyrate. Previous reports have verified that different fermentation types resulted in different amounts and components of VFA.6,27 The fermentation could be identified as butyrate type because the acetate and butyrate were the main products; the acetate and butyrate accounted for 41.2% and 51.4%, respectively.4 Wang et al. reported that the optimum pH range to achieve the maximum hydrogen yield was 4.5−6.0.28 Ren et al. revealed the highest hydrogen yield was obtained only when microbial reactions followed an ethanol fermentation type, which occurred at a pH of around 4.5.29,30 In our research, the final pH at the AC loading rate of 200 g/L was 4.3. It was inferred that the activity of microorganisms might have been inhibited by the accumulated VFAs, resulting in the cessastion of biohydrogen production. 3.2.3. Degradation of Glucose. In the culture medium, glucose was the sole carbon source which could be converted to biohydrogen. The initial glucose concentration was 20 g/L. As shown in Figure 6, the glucose decreased sharply during the initial 12 h. During this period, most of the glucose was degraded into VFA by cultures A and B. These results agreed with the sharp increase of VFA shown in Figure 4A. Figure 6 also shows that the highest decreasing rate of glucose was obtained at the AC loading rate of 200 g/L, corresponding to the glucose utilization rate of 86%. These results indicated that the mixed culture achieved the highest activity in degrading

Figure 4. Variation of total VFA (A) and pH (B) during the immobilization fermentation process.

loading rate of 200 g/L, corresponding to the final VFA of 5.9 g/L. Figure 4B shows the variation of pH during the fermentation process immobilized by AC. The pH decreased sharply at the initial fermentation process. After fermentation for 15 h, the pH value remained at a stable level. For the same group, the pH value agreed with the total VFA: the higher the total VFA, the lower the pH value. Moreover, it is worth noting that higher AC loading rate led to higher pH value, e.g., the D

DOI: 10.1021/acs.energyfuels.7b02035 Energy Fuels XXXX, XXX, XXX−XXX

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4. CONCLUSION Dark fermentation by cocultures was an effective way for biohydrogen improvement. The synergistic effect played an important role in improving the performance of dark fermentation. In the immobilized system, the optimum loading rate of AC was 200 g/L, corresponding to the glucose utilization rate and biohydrogen yield of 86% and 1.203 mol/ mol-glucose, respectively. The fermentation was identified to be butyrate type because of the dominant role of acetate and butyrate in VFA. The optimum biohydrogen yield of the immobilized cell system was 2.59 times higher than that of the suspension cell system. The stable environment provided by AC and the synergistic effect of cultures A and B were the main reasons for higher performance of the immobilized cell system.

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AUTHOR INFORMATION

Corresponding Author

Figure 6. Decline of glucose in immobilization cell system.

*Tel.: +86-511-88780201. Fax: +86-511-88780201. E-mail: [email protected]. ORCID

Cunsheng Zhang: 0000-0002-3523-6748

glucose at the AC loading rate of 200 g/L, and most of the glucose could be decomposed by the mixed cultures. 3.3. Discussion. Dark fermentation of organics for biohydrogen is a complex biochemical process in which macromolecular substrates are converted into hydrogen, CO2, VFAs, and other small molecule materials. It is difficult to carry out these steps by using a single pure monoculture.31 For different cultures, the rate of the same step is significantly different. Fermentation by cocultures was an effective way to enhance the hydrogen yield and shorten the fermentation time. Dark fermentation can be influenced by metabolic pathway and several environmental factors. The two strains utilized in this research belong to Enterobacter genus, and they have not yet been reported by others for biohydrogen production. Although the biohydrogen yield of the two strains was lower than the value obtained from the other strains such as Clostridium sp. and Bacillus sp., their potential capability of biohydrogen production requires further exploration by optimizing the fermentation conditions. AC provided a stable matrix to sustain cell viability as well as microbial colonization owing to its higher specific surface area and porous structure which enhance culture density.21 On the surface of AC, cultures A and B could grow freely. A steady biofilm which had a higher binding capacity especially for organic substrates might have been formed. Therefore, the surface attachment was one of the important reasons for higher biohydrogen yield.32,33 Prior to immobilization fermentation, the culture medium was brown (results not shown) because of the addition of tryptone and yeast juice. However, the brown color disappeared in about 30 min in the groups with AC addition. This phenomenon indicated that AC demonstrated a higher adsorption ability in the culture medium. Most of the cells as well as the nitrogen nutrients might have been adsorbed on AC at the initiation of fermentation, which was in favor of the forming of biofilm on AC. In this research, the performance of biohydrogen production was tested in only one batch. In the long term of biohydrogen production, however, the recycling of AC is required. On one hand, fermentation can be started without bacteria enrichment, and one the other hand the cost of immobilization carrier will be reduced.

Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The present work was supported by the Natural Science Foundation of Jiangsu Province, China (No. BK20150487), the National Natural Science Foundation of China (Grant No. 51608232), the Research Project for undergraduate of Jiangsu University (15A166, Y15A050), and the Open Fund of Key Laboratory for Solid Waste Management and Environment Safety (Tsinghua University) (SWMES 2015-11).

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REFERENCES

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DOI: 10.1021/acs.energyfuels.7b02035 Energy Fuels XXXX, XXX, XXX−XXX