Mitigation of N2O Emission from Aquaponics by Optimizing the

Sep 18, 2017 - Mitigation of N2O Emission from Aquaponics by Optimizing the Nitrogen Transformation Process: Aeration Management and Exogenous Carbon ...
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Mitigation of N2O Emission from Aquaponics by Optimizing the Nitrogen Transformation Process: Aeration Management and Exogenous Carbon (PLA) Addition Yina Zou,†,‡ Zhen Hu,*,† Jian Zhang,† Yingke Fang,† Minying Li,† and Jianda Zhang§ †

School of Environmental Science and Engineering, Shandong University, Jinan, 250100, China School of Environment, Tsinghua University, Beijing, 100084, China § College of Resources and Environment Science, Hebei Normal University, Shijiazhuang, 050024, China ‡

S Supporting Information *

ABSTRACT: N2O production in aquaponics is an inevitable concern when aquaponics is developed as a future production system. In the present study, two attempts were applied to mitigate N2O emission from aquaponics, i.e., aeration in hydroponic bed (HA) and addition of polylactic acid (PLA) into fillers (PA). Results showed that N2O emission from HA and PA was decreased by 47.1−58.1% and 43.2−74.9% respectively compared with that in control. Denitrification was proved to be the main emission pathway in all treatments, representing 62.4%, 86.4%, and 75.8% of the total N2O emission in HA, PA, and control, respectively. However, production of plants in HA was severely impaired, which was only 3.04 ± 0.39 kg/m2, while in PA and control, plants yields were 4.87 ± 0.56 kg/m2 and 4.33 ± 0.58 kg/m2. Combining the environmental and economic benefits, adding PLA in aquaponics may have a better future when developing and applying aquaponics systems. KEYWORDS: aquaponics, N2O emission, mitigation, polylactic acid, denitrification excreta. Ammonia (NH3) is the major form of fish excreta, and is also the primary control factor because it could cause the fish death at a very low concentration (average value: 2.79 mg NH3/L for 32 freshwater species).7 Nitrification in aquaponics is the way to eliminate this concern. A mature aquaponics system contains three main components: the fish, the plants, and the most importantly microbes from which the successful running of aquaponics benefits. In nitrification, toxic NH3 can be removed and eventually oxidized to nitrate (NO3−-N) by ammonia-oxidizing bacteria (AOB) and nitrite-oxidizing bacteria (NOB).8 NO3−-N only can be toxic to fish at a high concentration.9 Since there are anaerobic microenvironments in aquaponics, denitrification can also occur inevitably and then removes nitrogen from the system. Besides, growth of plants is another nitrogen removal pathway by absorption of the various nitrogen compounds existing in the water. Our previous studies demonstrated that changes in the operating conditions of aquaponics, i.e., physicochemical parameters controlled in water and construction structures of the system, have great influences on nitrogen transformations.10,11 The concentration of nitrogen compounds and the production of fish and plants would be changed under different operating conditions. A huge environmental concern involved in nitrogen transformation processes is the nitrous oxide (N2O) emission. N2O is the third greatest greenhouse gas and an important ozone depletion substance. About 30−45% of N2O emission was proved to be from anthropogenic sources in the world.12

1. INTRODUCTION The aquaculture industry has been thriving rapidly, and the production of aquatic product was up to 73.8 million tons in 2014.1 However, vigorous growth of aquaculture has resulted in many problems. Water eutrophication and biota damage are always caused when aquaculture wastewater containing numerous nutrients is dumped into the environment, and discharging this kind of wastewater is also a waste of nutrients. Aquaponics, which combines hydroponics with the aquaculture process, is a novel recirculating aquaculture production system.2 It is attracting the attention of scientists and fishermen because of the potential for recovering nitrogen in aquaculture wastewater, and elevated nitrogen utilization efficiency could reduce its environmental impacts.3 In addition, aquaponics is an option to future agriculture because hydroponics is believed to be an alternative to growing plants with soil. In recent years, the increasing reduction of water resources and arable land has restricted the development of agriculture, and aquaponics which meets the definition of sustainable agriculture is considered to be a promising production system for the areas where soil is poor and water is scarce.4 So far, there have been many successful cases of aquaponics in the world.2,5 Once aquaponics is operated properly, it acts like a stable ecosystem. Toxic and harmful substances could be cleared up within aquaponics, and the system is also less susceptible to attacks from plants and fish diseases.6 Nitrogen is one of the most important elements in aquaponics. It is the substance constructing cells and supports the growth of all organisms in aquaponics. Nitrogen transformations in aquaponics are the core biochemical reactions. The nitrogen transformations start with the digestion of fish feed by fish, and then the nitrogen enters the water as the fish © XXXX American Chemical Society

Received: Revised: Accepted: Published: A

July 13, 2017 September 9, 2017 September 18, 2017 September 18, 2017 DOI: 10.1021/acs.jafc.7b03211 J. Agric. Food Chem. XXXX, XXX, XXX−XXX

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Journal of Agricultural and Food Chemistry

feeding ration was the same in three treatments. Fish feed was the floating pellets with nitrogen content of 23%. Two attempts were employed to reduce the N2O emission named as hydroponic aeration (HA) and PLA addition (PA). In HA, a concentric-circle aeration diffusor was fixed at the bottom of hydroponic bed, which can achieve uniform aeration. Aeration rate in the hydroponic bed was set at 0.6 L/min, and to not increase the cost of aeration, aeration rate in the fish tank was reduced to 0.4 L/ min, while in control and PA aeration rate in the fish tank was 1.0 L/ min. In PA, the gravel layer of the fillers in the hydroponic bed was reformed, and it was changed into a mixed layer of gravel and PLA (Hisun, Taizhou, China) at the volume ratio of 1:1. The size of PLA was similar to that of gravel with the density of 1.25 g/cm3. PLA is the polymer made of lactic acid and has good thermoplastic characteristic; the relative molecular mass of the PLA is about 2200 g/mol. 2.2. Water Quality and Nitrogen Measurement. Routine monitoring of water quality was carried out at around 10:00 a.m. every other day, and about 50 mL of water sample was collected from the middle of each fish tank and taken back to the laboratory. The pH and DO concentration were determined on site using a pH analyzer (Leici, Shanghai, China) and a DO analyzer (HACH, Loveland, Colorado), respectively; water temperature was also measured by a DO analyzer simultaneously. pH was measured only in the middle of the fish tank, but as to DO concentration, the hydroponic bed was also included and the measurement location was in the middle of fillers. Nitrogen compound measurements including TAN, NO2−, and NO3− were accomplished in 24 h according to the methods described in APHA.19 Organic nitrogen and total organic carbon (TOC) in water were also measured when the present study ended. Organic nitrogen was obtained by subtracting the above inorganic nitrogen from total nitrogen, which was measured using the persulfate digestion method.20 The TOC measurement was applied in a TOC analyzer (Shimadzu, Kyoto, Japan). Nitrogen in fish feed and nitrogen accumulated in fish body and plants were derived from their dry matter increase and corresponding nitrogen content concentration. Briefly, fish, plants, and fish feed were first dried to constant weight to calculate their moisture content, and then an elementary analyzer (Elementar, Langenselbold, Germany) was used to determine the nitrogen content concentration in dried samples. 2.3. N2O Emission Flux Determination. Closed chamber method was adopted to determine the N2O flux in the hydroponic bed. The chamber covered the whole hydroponic bed during the gas sampling period, and gas samples were drawn into air bags periodically at 0, 20, 40, 60, 80, 100, and 120 min using an aspirator pump. Gas samples were taken back to the lab, and subsequently a gas chromatograph (Agilent, Palo Alto, California) equipped with electron capture detector was used to detect N2O concentration in gas samples. N2O emission flux from the hydroponic bed was calculated by the linear increase of N2O concentration in the sampling period according to the equation described in our previous study.14 2.4. N2O Production Pathway Measurement. When the present study ended, an incubation study was conducted in the laboratory to figure out the N2O emission pathway, and previous methods were modified (Maag and Vinther;22 Stevens et al.21) to simulate the field conditions better. Before the incubation study, moisture content of the perlite in the hydroponic bed was measured. The incubation study was conducted in screw-topped glass bottles of 1000 mL, and there was a silicone tube in the cap for gas input and sampling. The air-dried perlite in bottles was 10 cm in diameter by 5 cm high, and synthetic aquaponics wastewater ((NH4)2SO4, KNO3, glucose, and tap water) was added to give a moisture content about 0.5 g H2O/mL perlite, the same moisture content as in field aquaponics. NH4+-N loading and NO3−-N loading were both 20 g N/m2, which were similar to the average nitrate loading in the late study stage of field aquaponics, and the glucose loading was 120 g/m2 so that the C/ N ratio was near the normal level. After the above preparation, the following procedures were repeated five times. Every treatment contained two sets of incubation bottles: C2H2 was added to one at 10 Pa, and another did not have C2H2 added. Then the bottles were

Of the anthropogenic sources, it is estimated that wastewater treatment and aquaculture account for 4.7%, and the main emission pathway is the biological nitrification and denitrification.13 These two sectors, i.e., aquaculture and wastewater treatment, are linked together in aquaponics, making it a potential N2O emission source. As a matter of fact, our previous study showed that aquaponics emitted more N2O than aquaculture did, with the N2O conversion ratio (the ratio of nitrogen emitted in the form of N2O to total nitrogen input) of 1.3% in aquaculture and 1.5−1.9% in aquaponics.8 To reduce N2O emission in aquaponics is of great practical significance since it helps to control the greenhouse effects and ozone depletion, contributing to the good application prospects of aquaponics as well. However, studies on the mitigation of N2O emission from aquaponics are scarce. In consideration of the susceptibility of nitrogen transformations in aquaponics, optimizing the operation conditions is the cutting-in point for mitigating N2O emission. Previous study has adopted the 15N labeling method to determine the N2O emission pathway in aquaponics, and results showed that 75.2−78.5% of N2O emission came from heterotrophic denitrification.14 Given that nitrification is the leading reaction rather than denitrification, the regulation of denitrification in aquaponics is rare. It is acknowledged that many factors affected the N2O emission in denitrification, and N2O emission in a lab-scale wastewater treatment system was reported to be lowest under the optimal growth conditions for denitrifying bacteria.15 In aquaponics, manually maintained high DO concentration for fish and plant growth would work against denitrification and the characteristic of carbon source deficiency in aquaculture water would also boost N2O emission.10,16,17 Thus, to reduce the N2O emission from denitrification, two opposite methods could be applied in aquaponics, one by inhibiting denitrification directly and another by reducing the N2O emission in denitrification via providing favorable denitrifying conditions. In this study, two types of optimization methods were designed, i.e., aeration in hydroponic bed to inhibit denitrification and addition of polylactic acid (PLA) to ameliorate the denitrification conditions, attempting to mitigate the N2O emission from the media-based aquaponics. The effects of two attempts on the production performances of aquaponics systems and nitrogen transformations were also monitored. And the acetylene (C2H2) inhibition technique was finally introduced to ascertain the N2O production pathway. Overall, the study aim was to find a practical method of mitigating N2O emission in aquaponics.

2. MATERIALS AND METHODS 2.1. Aquaponics Microcosms. Experimental aquaponics systems were located at the yard of Environment Research Institute of Shandong University. The study was carried out from June 26, 2016, to August 15, 2016, lasting for 50 days. Media-based aquaponics was adopted because of its high nutrient removal efficiency,18 and the experimental aquaponics consisted of mature systems which had been running for about two years before the redesign and the introduction of fresh tap water. Detailed description of the experimental aquaponics can be found in our previous study.10 In the present study, the fillers in the hydroponic bed contained gravel of 10 cm height (Φ 3−5 mm) at the bottom and perlite of 20 cm height (Φ 1−2 mm) on the top of the gravel. Common carp (Cyprinus carpio) and Chinese cabbage (Brassica chinensis) were employed. The cabbage was grown at 25 plants/m2, and carps were stocked at a density of 12 kg/m3. Automatic fish feeders were used to feed fish three times every day, and the total B

DOI: 10.1021/acs.jafc.7b03211 J. Agric. Food Chem. XXXX, XXX, XXX−XXX

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Journal of Agricultural and Food Chemistry incubated at 25 °C for 24 h, and gas samples were subsequently taken from each bottle to measure the N2O concentration. Gas inside the bottles was replaced by fresh air before the next C2H2 injection. The fraction of N2O emission from denitrification was assumed by dividing N2O concentration in bottles with acetylene by N2O concentration in acetylene-free bottles. 2.5. Statistics Analysis. All data shown in the manuscript were the average values of three replicates. SPSS 17.0 (IBM, USA) was used to perform statistical analysis of fish and plant production, using analysis of variance (ANOVA) followed by Duncan’s multiple range test at p < 0.05.

3. RESULTS 3.1. Physicochemical Parameters. The ranges of pH, temperature, and DO concentration in three treatments are presented in Table 1. There was no pH adjustment during the Table 1. Physical Parameters of Water in Each Treatment parameters

HA (n = 25)

PA (n = 25)

control (n = 25)

pH temp (°C) DO (mg/L) fish tank hydroponic bed

7.5 ± 0.1 28.3 ± 1.7

7.5 ± 0.1 28.4 ± 1.5

7.5 ± 0.1 28.3 ± 1.6

3.90 ± 0.70 5.28 ± 0.57

4.45 ± 0.73 2.77 ± 0.60

4.72 ± 0.71 3.99 ± 0.56

whole study period, but pH was stable and the same in all three treatments. The water temperature in the three treatments was similar and favorable to the growth of the three main components. The main difference caused by HA and PA was in DO concentration variation. DO concentration in the fish tank of HA was relatively lower compared with those in PA and control, and this is because of the reduced aeration density for a compromise made to balance the energy input. But the DO concentration in the hydroponic bed of HA was the highest due to the additional aeration, followed by control and then PA. Specifically, Figure 1 shows the DO concentration dynamics during the whole study period in each treatment. TOC concentration at the end of study showed differences between the three treatments, which were 27.6 ± 3.3 mg/L in HA, 27.8 ± 2.7 mg/L in control, and 38.9 ± 3.9 mg/L in PA. This indicated that adding PLA in the hydroponic bed obtained the release of organic carbon. 3.2. Aquaponics Production Performance. There was no death and disease happening of either fish or plants in the present study. Aquaponics production performances including fish production and plant production both showed significant differences (p < 0.05) between HA and control, while no significant difference (p > 0.05) was calculated between PA and control (Table 2). The biomass increases of fish and plants in HA were obviously poorer than in the other two treatments. Food conversion ratio (FCR) and specific growth rate (SGR) values also demonstrated that fish had a poor growth condition in HA possibly because of the low DO concentration. 3.3. Nitrogen Compound Variation. Concentration variations of nitrogen compounds across the whole study period are shown in Figure 2. TAN concentration (a) and NO2−-N concentration (b) did not show differences between three treatments and always remained at low levels so that no harm was caused to fish growth. TAN concentration fluctuated around 1.0 mg/L, and NO2−-N concentration variation was smoother and below 0.2 mg/L most of the time. It was the dynamic changes of NO3−-N concentration in the three treatments that differed significantly (Figure 2c). During the

Figure 1. DO concentration dynamics in fish tank (a) and hydroponic bed (b).

Table 2. System Production Parameters in Each Treatment parameters biomass increase plant (kg/m2) fish (kg/m3) FCRb SGRc(%)

HA 3.04 2.54 2.82 0.35

± ± ± ±

0.39 0.32 0.36 0.05

PA aa a a a

4.87 3.22 2.22 0.44

± ± ± ±

0.56 0.27 0.23 0.03

control b b b b

4.33 3.14 2.29 0.43

± ± ± ±

0.58 0.36 0.34 0.06

b b b b

a

Different letters show significant differences at p < 0.05 bFCR (food conversion ratio) = total feed given (g) to fish/total wet weight gain (g) of fish. cSGR (specific growth rate) = (ln Wf − ln Wi) × 100/days; Wf is final weight of fish, and Wi is initial weight of fish

first rising period, the increasing rate of NO3−-N concentration in control was the fastest, followed by PA, and the slowest was in HA. Subsequently, NO3−-N concentration in PA and control started decreasing, and the decreasing rate in PA was faster than that in control. However, no decline of NO3−-N concentration in HA was detected. At the end of the study, organic nitrogen concentration ranged between 1.0 and 2.0 mg/L, contributing a little to nitrogen level in water. 3.4. Nitrogen Distribution. To evaluate the overall nitrogen distribution in aquaponics, nitrogen mass balance was calculated at the end of the study (Figure 3). First of all, the nitrogen accumulated in fish and plants, often referred to as nitrogen utilization efficiency (NUE), accounting for 35.2%, 50.0%, and 46.4% of the total nitrogen input in HA, PA, and control, respectively. Corresponding to the fish and plant production, NUE in HA was low and reduced by 24.1% compared with control. It was worth noting that nutrient contents of water in the three treatments were at different levels. With the same nitrogen input, in HA and PA only 23.3% and 15.6% of nitrogen remained in water, which was 36.5% in C

DOI: 10.1021/acs.jafc.7b03211 J. Agric. Food Chem. XXXX, XXX, XXX−XXX

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3.5. N2O Emission. The N2O emission fluxes in the three treatments are shown in Table 3. Compared with control, N2O Table 3. N2O Emission Fluxes (mg N·m−2·h−1) in Each Treatment time (d)

HA

PA

control

31 48

6.15 ± 3.3 9.15 ± 4.7

6.60 ± 3.0 5.46 ± 2.5

11.62 ± 5.3 21.82 ± 2.8

emission fluxes in HA and PA were reduced by 47.1−58.1% and 43.2−74.9%, respectively, indicating the excellent emission reduction was realized. Although the denitrification was the main emission pathway in all three treatments, the contribution of denitrification and nitrification to N2O emission in each treatment differed (Figure 4). There were respectively a

Figure 4. N2O production pathway in each treatment.

decrease and an increase in the denitrification contribution ratios in HA and PA compared with control, which was 62.4%, 86.4%, and 75.8% respectively. In HA, the nitrification and denitrification both affected the N2O emission, while in PA the denitrification almost dominated the N2O emission.

Figure 2. Nitrogen compound concentration variation in each treatment: (a) TAN, (b) NO2−-N, and (c) NO3−-N.

4. DISCUSSION 4.1. Effect of Aeration Management and PLA Addition on Nitrogen Transformations. DO concentration differed greatly between three treatments and was one of the important factors that would have great influences on nitrogen transformations. In the fish tank, reduced aeration intensity in HA caused the decrease of DO concentration. Nonetheless, the DO concentration levels in the three treatments were sufficient to meet fish growth requirements according to their behavioral responses.23 Observed experimental phenomena showed that the feeding action of fish was not affected and fish can take in all fish feed input. But in the hydroponic bed where nitrogen transformations mainly took place,14 adding PLA in the hydroponic bed brought about a decrease in DO concentration, while supplying aeration in the hydroponic bed made an increase. Compared with other natural polymers, PLA has a different degradation process. PLA was first hydrolyzed into small size polymers or monomers by ester bond cleavage and then partially biodegraded by heterotrophic microbes which consumed oxygen to support the survivability and metabolism.24 It was worth noting that the DO concentration varied

Figure 3. Nitrogen mass balance in each treatment.

control. On the contrary, compared with control, the unaccounted nitrogen (“others”) which included N2 emission and NH3 volatilization and so forth in HA and PA increased by 48.8% and 20.2%, respectively. D

DOI: 10.1021/acs.jafc.7b03211 J. Agric. Food Chem. XXXX, XXX, XXX−XXX

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Journal of Agricultural and Food Chemistry

provided exogenous carbon sources for denitrification, and TOC data at the end of the experiment confirmed this. High TOC concentration was not detected because the PLA hydrolysis was slow and it can be utilized once produced. Degradation products of PLA like lactic acid and ethanol were proved to be good denitrification electron donors.30 Therefore, it was speculated that the reduced nitrogen in water of PA was mainly converted to N2, which made up a large part of unaccounted nitrogen. The nitrogen level in water mainly depended on the concentration of inorganic nitrogen compounds, since the organic nitrogen concentration was low. And most inorganic nitrogen was in the form of NO3−-N in the present study, which was similar to most aquaponics water.31,32 The present experimental devices had been running for about two years, and the nitrifying bacteria community has been built so TAN can be removed in time. NO2−-N is the intermediate product of nitrification and can be oxidized to NO3−-N with less enzyme and oxygen involved, so it is hardly accumulated. In aquaponics, NO3−-N was produced in the nitrification process and removed by plants and microbial denitrification. In the first 10 days, plant seedlings were just transplanted into aquaponics and a few nutrients were taken in. Plant absorption seemed to make no difference on NO3−-N concentration between the three treatments. The NO3−-N production rates in HA and PA were relatively lower than that in control, which was possibly due to NH3 stripping and denitrification, respectively. In the late stage of the study, plants grew well and affected the NO3−-N concentration by absorbing nitrogen. According to Table 1, plant biomass increase was higher in PA than in HA, so the NO3−-N concentration declined rapidly in PA. 4.2. Effect of Aeration Management and PLA Addition on N2O Emission. Fortunately, the two attempts both achieved N2O mitigation in media-based aquaponics. In HA, both nitrification and denitrification would have significant influences on N2O emission considering their respective contribution ratios to N2O emission. The reduced nitrogen level in water was responsible for the low N2O emission. Nitrogen was removed via NH3 stripping process, so less nitrogen moved to the subsequent nitrogen transformations and N2O emission decreased. In PA, denitrification was the major emission pathway of N2O emission, but the enhanced denitrification did not cause the elevated N2O emission. This was because the N2O emission in denitrification was affected by many factors. Low NO3−-N concentration and low DO concentration in PA would reduce the N2O/N2 ratio. N2O was one of the oxygen acceptors in the denitrification process; when NO3−-N was limited, the N2O/N2 emission ratio would decrease.33 In addition, the activity of N2O reductase which is in charge of N2O reduction was reported to be higher under low DO concentration condition,34 so N2O emission in PA was low. But from the perspective of economics, HA caused the decline of fish and plant growth, which had a negative effect on aquaponics development. Therefore, adding PLA into the hydroponic bed could be a potential alternative when constructing aquaponics systems. Contribution of nitrification and denitrification to N2O emission showed that denitrification was the main process for producing N2O in each treatment, which was similar to our previous study adopting the 15N labeling method.14 Since there was no difference in the substrate supply and incubation environment, the distinction shown in the contribution proportion of denitrification and nitrification was the

significantly during the study period, and this was because the present aquaponics systems were operated under natural climatic conditions. Many factors have influences on the DO concentration, and in the present study, it was believed that the DO concentration in the fish tank was mainly influenced by the water temperature and fish activities, and the DO concentration in the hydroponic bed was mainly influenced by water temperature. Being a significant influence, the water temperature (Figure S1) recorded during the study period showed huge fluctuation. In addition, the activities of fish were not the same every day and they were difficult to predict. When the activities of fish became strenuous, more oxygen would be consumed, and vice versa. Thus, the fluctuation of DO concentration was stronger in the fish tank than in the hydroponic bed. From the nitrogen mass balance (Figure 3), the notable phenomena were the differences between NUE of the three treatments. Given the fact that nitrogen input to the three treatments was almost the same, the NUE values were related to the fish and plant production. The growth of fish in HA was poor, possibly because the digestion and absorption abilities were impaired by the relatively low DO concentration, although this DO concentration level would not cause fish death.25 When it came to plant production, good ventilation character in the hydroponic bed of HA was believed to promote plant growth, but in the present study different results were observed. With high DO concentration, plant biomass increase was low in HA, and this was related to the low nitrogen level in water. The nitrogen compound concentration in HA was approximately half that in control in the late stage of the study (Figure 2c), resulting in the poor growth of plants. But plant growth in PA was not affected by low nitrogen level. Studies have demonstrated that low-molecule organic carbon matter in the rhizosphere can be absorbed directly by plants possibly to balance the nutrient intake,26−28 and the fermentation products of lactic acid are formic acid and acetic acid, which possibly promoted the growth of plants. However, nitrogen concentration in nutrient solution was proved to have an influence on the functional components in leaves of plants, so the quality of plants in PA still needed to be evaluated.29 Compared with control, whether in HA or PA, the nitrogen content in water decreased, but the unaccounted nitrogen mainly including N2 and NH3 increased. However, the reasons for this result in HA and PA were not same. In aquaponics, NH3 was produced as the main form of fish excreta and was the original source of nitrogen compounds in water. NH3 can be competitively stripped by aeration and used as the substrate of nitrification. With the same aeration density, the aeration equipment in HA was installed in both the fish tank and the hydroponic bed. Besides, it was worth noting that the gas− liquid contacting area in the hydroponic bed was expanded significantly because of the presence of fillers, and then the diffusion of ammonia from aqueous phase to gaseous phase under the aeration condition would be enhanced. So, it was estimated that NH3 emission in HA possibly accounted for a large proportion of unaccounted nitrogen. In PA, lower DO concentration was a favorable condition for denitrification. Denitrification would happen at anoxic microenvironments which existed in the hydroponic bed. The oxygen diffusion process transported oxygen into the spaces inside the microbial floc and fillers. As the DO concentration was lowered in PA, the scale of anoxic microenvironments increased, and denitrification activity would be enhanced. Besides, the PLA addition E

DOI: 10.1021/acs.jafc.7b03211 J. Agric. Food Chem. XXXX, XXX, XXX−XXX

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consequence of different microbial characteristics in perlite. However, the study period was too short to form the differences in microbial community structures. A few years is always needed when changes in the soil environment lead to changes in microbial community structures.35 Abundances of genes (i.e., amoA, nirK, nirS, 16S rRNA) which could reflect the numbers of corresponding microbes involved in nitrogen transformations were measured at the end of the study, and the results demonstrated the stability of microbial community structures (Figure S2). It appears from these results that the changed activities of the microbial community influenced by the field environment of aquaponics might be the reasons for the difference in N2O emission pathway. In HA, high DO concentration in the hydroponic bed was the beneficial condition for nitrification. In aerobic nitrification, N2O can be produced from the oxidation of hydroxylamine and nitrifier denitrification by AOB. Given that AOB denitrification was induced by high nitrite concentration, which did not show up in the present study, the oxidation of hydroxylamine was deemed as the main pathway for producing N2O.36 Chemical decomposition and biological oxidation of the hydroxylamine were both favored under relatively high DO concentration conditions,37 while in PA, the circumstance was on the opposite side. Low DO concentration and exogenous organic carbon addition in PA resulted in strong denitrification, and weakened the N2O emission in nitrification at the same time, so the percentage of nitrification to N2O emission dropped.

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ASSOCIATED CONTENT

* Supporting Information S

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jafc.7b03211. Water temperature variation, materials and methods about the microbial analysis of the abundance of the genes in aquaponics, and results of microbial analysis (PDF)

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AUTHOR INFORMATION

Corresponding Author

*Phone: +86 15688889793. E-mail: [email protected]. ORCID

Zhen Hu: 0000-0002-4728-945X Funding

This work was supported by China Major Science and Technology Program for Water Pollution Control and Treatment (No. 2017ZX07101003), Shandong Provincial Key Research and Development Plan (No. 2017GSF216011), National Natural Science Foundation of China (No. 41401562), Fundamental Research Funds of Shandong University (No. 2017JC025), and National Science Foundation for Post-Doctoral Scientists of China (No. 2014M561197). Notes

The authors declare no competing financial interest.

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REFERENCES

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DOI: 10.1021/acs.jafc.7b03211 J. Agric. Food Chem. XXXX, XXX, XXX−XXX