Next Article in Journal
COVID-19, the Climate, and Transformative Change: Comparing the Social Anatomies of Crises and Their Regulatory Responses
Next Article in Special Issue
Study on the Similarity of the Parameters of Biomass and Solid Waste Fuel Combustion for the Needs of Thermal Power Engineering
Previous Article in Journal
The Grass Is Always Greener on My Side: A Field Experiment Examining the Home Halo Effect
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Sustainability
Volume 12
Issue 16
10.3390/su12166336
sustainability-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Effects of Zeolite and Biochar Addition on Ammonia-Oxidizing Bacteria and Ammonia-Oxidizing Archaea Communities during Agricultural Waste Composting

by
Xin Wu
,
Liheng Ren
,
Jiachao Zhang
* and
Hui Peng
*
College of Resources and Environment, Hunan Agricultural University, Changsha 410128, China
*
Authors to whom correspondence should be addressed.
Sustainability 2020, 12(16), 6336; https://0-doi-org.brum.beds.ac.uk/10.3390/su12166336
Submission received: 21 July 2020 / Revised: 28 July 2020 / Accepted: 5 August 2020 / Published: 6 August 2020
(This article belongs to the Special Issue Environmental Science and Sustainable Waste Management)
Browse Figures
Versions Notes

Abstract

:
The effects of zeolite and biochar addition on ammonia-oxidizing bacteria (AOB) and archaea (AOA) communities during agricultural waste composting were determined in this study. Four treatments were conducted as follows: Treatment A as the control with no additive, Treatment B with 5% of zeolite, Treatment C with 5% of biochar, and Treatment D with 5% of zeolite and 5% biochar, respectively. The AOB and AOA amoA gene abundance as well as the ammonia monooxygenase (AMO) activity were estimated by quantitative PCR and enzyme-linked immunosorbent assay, respectively. The relationship between gene abundance and AMO enzyme activity was determined by regression analysis. Results indicated that the AOB was more abundant than that of AOA throughout the composting process. Addition of biochar and its integrated application with zeolite promoted the AOB community abundance and AMO enzyme activity. Significant positive relationships were obtained between AMO enzyme activity and AOB community abundance (r2 = 0.792; P < 0.01) and AOA community abundance (r2 = 0.772; P < 0.01), indicating that both bacteria and archaea played significant roles in microbial ammonia oxidation during composting. Using biochar and zeolite might promote the nitrification activity by altering the sample properties during agricultural waste composting.

1. Introduction

Composting has been widely recognized as an effective way to convert agricultural waste into valuable organic products [1,2]. Gaseous emissions inevitably reduced the nutrient content, which is a major challenge for the composting process [3,4]. During composting, a large quantity of nitrogen (9.6–50%) in the raw materials was released in the form of gas, mainly including ammonia (NH3) and nitrous oxide (N2O) [5,6]. CH4 and N2O, which are reported by the international panel on climate change (IPCC), are 30–210 times more likely to contribute to global warming than carbon dioxide (CO2) and are responsible for climate change or ozone depletion. Therefore, it is necessary to control the emission of gases to provide an efficient, economical and environmentally friendly process for the treatment of agricultural waste.
Nitrogen in composts could be fixed and the final product’s quality can be improved by a variety of physical, chemical and biological methods. Microbial inoculation and chemical/mineral material additives improved the composting efficiency, reduced nitrogen losses and mitigated greenhouse gas emissions [7,8,9]. Biochar, zeolite, bentonite and other additives can increase the porosity of compost materials, improve the air diffusion efficiency and reduce the emission risk of greenhouse gases. Such additives have the characteristics of porosity or a high specific surface area, which is beneficial to absorb nitrite nitrogen (NO2--N) and N2O in the compost matrix, promote complete nitrification or denitrification and reduce the release of N2O [10,11,12,13]. The addition of biochar + bamboo vinegar, struvite + nitrification inhibitor and earthworm manure + zeolite, among other measures, have also been shown to promote nitrogen retention in the composting system [10,11,14]. The effects of zeolite and biochar addition to nitrogen conservation during agricultural waste composting have attracted worldwide attention.
Recent research has demonstrated the effects of biochar and/or zeolite on organic matter degradation [15], nitrogen transformation [15,16] and gas emissions [16,17,18,19] during composting. The additional effects of biochar and zeolite on microbial communities have attracted worldwide attention. Microbial communities were found to play significant roles during agricultural waste composting. Many studies have been carried out to determine the response of bacterial and fungal communities to biochar and zeolite addition during agricultural waste composting. Biochar addition changed the microbial communities and their metabolic functions during rice straw composting with pig manure [20,21]. These studies helped to increase our understanding about the microbiological mechanism of nutrition cycling processes under different regulation strategies. As yet, little information is available about their effects on functional microbial communities, e.g., ammonia-oxidizing bacteria (AOB) and archaea (AOA).
AOB and AOA employ the same amoA gene that encodes the ammonia monooxygenase (AMO) enzyme subunit. The oxidation of ammonia is the rate-limiting step for nitrification, determining the nitrogen transformation balance between the reduced and oxidized states. Moreover, the addition of zeolite and biochar will affect the physicochemical properties of the composts, and further modify the microbial community and function of the compost. It is still necessary to investigate the factors related to nitrification and the possibility of promoting nitrification to reduce NH3 emissions [22]. Identifying and tracing the characteristics of the functional communities and relevant enzyme activities will deepen our understanding of the nitrogen balance mechanism during composting.
Hence, this research was carried out to determine the changes in the AOA and AOB communities and AMO enzyme activity during the composting process with adding of zeolite and biochar, and to provide theoretical guidance for the management of the composting process. The main aims of the study were 1) to determine the abundance dynamics of the functional AOA and AOB amoA genes; and 2) to obtain the relationship between AMO enzyme activity and amoA gene abundance during agricultural waste composting, with different amendments of zeolite and biochar. It is expected to deepen the insight into the pathway of the microbiological mechanism of nitrogen loss control with the addition of biochar and zeolite during agricultural waste composting.

2. Materials and Methods

2.1. Raw Materials and Composting Setup

Agricultural wastes (i.e., rice straw and vegetable leaf) were collected in the rural areas of Changsha, Hunan. Rice straw and vegetable leaf waste were air-dried and cut into 5–10 mm fragments. After being sieved through a 40-mesh screen to remove stones and plant debris, fresh soil was added to the composting piles to provide some microbial populations and the necessary nutrients. Bran was chosen to adjust the initial carbon/nitrogen (C/N) ratio.
The raw materials were homogenized at a ratio of 11:8:3:2 by weight (rice straw:fresh soil:vegetable leaf:bran). Four treatments were carried out as follows: Treatment A as the control with no additive, and to Treatments B, C and D were added zeolite (5%), biochar (5%) and a combined treatment (5% zeolite + 5% biochar), respectively. The zeolite used in this study was clinoptilolite zeolite, that can absorb and retain water longer and retain nutrients on its microcellular structures. Biochar was obtained from rice straw in a hypoxia environment (500 °C, 3 h) by using a tubular carbonization furnace (HeFeiJingKe, GDL−1500×, China). Composting piles (50 kg wet weight) were set up and packed loosely in open boxes with good thermal insulation performance. The initial C/N ratio and moisture content were about 30:1 and 60%, respectively. Composting piles were manually turned to avoid possible anaerobic conditions. The physicochemical properties of the raw materials and the different piles are shown in Table 1.

2.2. Samples Collection and Parameters Determination

The subsamples were collected on days 0, 7, 14, 21, 28, 35 and 42. Samples for DNA extraction for discerning the functional gene abundance and activity were stored at −20 °C before being used. Samples for determination of the physical-chemical properties were stored at 4 °C before being used. Pile temperature, pH, ammonium (NH4+-N) and nitrate (NO3--N) were determined according to our previous research [23,24]. After sampling, sterile deionized water was periodically added to maintain the moisture content of each pile in the range of 50% to 60%.

2.3. AMO Enzyme Activity Measurement

The activity of the AMO enzyme activity depends on, in part, on the content of the AMO protein. An AMO ELISA Kit was used to determine the AMO enzyme activity. The color of the stop solution changed from blue to yellow, and the color intensity was determined at 450 nm by a spectrophotometer (SpectraMax iD5). The AMO ELISA Kit has a series of calibration standards to determine the concentration of the AMO enzyme in the samples. Both the calibration and the sample standards were determined simultaneously. Meanwhile, the standard curve of the optical density versus AMO concentration was produced by the operator. Data of the AMO enzyme activity was calculated by comparing the value of the sample optical density with the standard curve [25].

2.4. Quantitative PCR

Total DNA was extracted from freeze-dried samples by using the PowerSoil kit (MoBio Laboratories, USA). The DNA extracts for each sample were combined to reduce possible variability and stored at −20 °C. Primers amoA−1f/amoA−2r [26] and CrenamoA−23f/CrenamoA−616r [26] were chosen for the AOB and AOA amoA gene abundance quantification, respectively. Quantitative PCR was conducted on an iCycler IQ5 Thermocycler (Bio-Rad, USA) with a 10 μL volume involving 0.5 μL of DNA extract, 0.2 μL of each primer, 5 μL of a real-time PCR mixture (2 × SYBR, Bioteke, Beijing) and 4.1 μL of sterile water. The quantitative PCR reaction was as follows: 95 °C for 3 min, 40 cycles of 40 s at 95 °C, 40 s at 55 °C and 40 s at 72 °C. Data were retrieved at 72 °C. The standard curves for the quantitative PCR were prepared with linearized plasmids containing cloned amoA after a 10-fold serial dilution. Melting curves were used to verify the amplification specificity of the amoA gene.

2.5. Data Analysis

Three replicates were used for the parameter, amoA gene abundance and AMO enzyme activity determination. The original data of the gene abundances were log10-transformed before further analysis. Least-significant difference (LSD) tests were performed to compare the mean values of the amoA gene abundance and the AMO enzyme activity in the different treatments on each sampling occasion by using SPSS (version 11.5). A regression analysis was performed between the AMO enzyme activity with log10-trasnformed AOB and AOA abundance to obtain the possible relationships of AOB and AOA with microbial ammonia-oxidizing activity.

3. Results

3.1. Physico-Chemical Parameters

The addition of zeolite and biochar changed the pile temperature during composting, with the maximum pile temperature for Treatments A, B, C and D being 51.0, 54.4, 62.4 and 56.5 °C, respectively (Figure 1a). The addition of biochar might accelerate the decomposition of the easy-degradable organics. Compared with the control treatment (Run A), the high temperature period was shortened by adding biochar.
The pH increased significantly during the first two weeks and then decreased gradually afterwards (Figure 1b). Significant changes in the nitrogen-relevant substances were obtained, indicating that the biochar and zeolite showed nitrogen conservation potential during composting. Because of the pH increase and mineralization of the nitrogen compounds, the NH4+-N rapidly accumulated during the thermophilic stage, but decreased afterwards due to NH3 volatilization (Figure 2a). The NO3−-N contents in Treatments C and D with biochar addition were significantly higher than that of Treatments A and B during the maturation stage (Figure 2b). The final contents for NO3--N were 857.8, 958.5, 1050.8 and 1082.6 mg/kg DW in the compost samples for Treatments A, B, C and D, respectively (Figure 2b).

3.2. AOB and AOA amoA Gene Abundance

The bacterial (Figure 3) and archaeal amoA genes (Figure 4) widely existed during the whole composting process. The abundance of the AOB and AOA amoA gene ranged from 4.9 × 106 to 1.9 × 108 and 1.1 × 106 to 3.4 × 107 gene copies per g−1 DW compost sample. The addition of biochar or zeolite stimulated the AOB abundance. The AOB amoA gene was 1–2 orders of magnitude higher than its archaeal community counterparts, indicating that AOB rather than AOA might play more roles in microbial ammonia oxidization during composting with biochar and zeolite addition. The abundance of the AOB amoA genes was relatively higher during the second fermentation phase than that of the first fermentation. In the whole composting process, the addition of biochar rather than zeolite had a significant effect on the AOB and AOA communities.

3.3. AMO Enzyme Activity

The activities of the AMO enzyme in all treatments are presented in Figure 5. Treatment A without any addition had the lowest AMO enzyme activity. The AMO enzyme activity was significantly increased in Treatments C and D with biochar addition. The AMO activities in Treatments B and D were increased on Days 28 and 42. These results indicated that biochar rather than zeolite amendment promoted the microbial conversion of NH4+-N and increased the activity of the AMO genes.

3.4. Relationship Between AMO Enzyme Activity and amoA Gene Abundance

Significant positive relationships were obtained between the AMO enzyme activity and bacterial amoA gene abundance (Figure 6) as well as archaeal amoA gene abundance (Figure 7). The AMO enzyme activity increased as the bacterial and archaeal amoA community exponentially increased. The bacterial and archaeal amoA gene-coding communities can account for 79.2% (P < 0.01) and 77.2% (P < 0.01) of the variation in AMO enzyme activity. These results suggested that the AOB and AOA communities were both closely related to the AMO enzyme activity in the composting substrate.

4. Discussion

Pile temperatures exceeding 50 °C lasted for more than 5 days, which effectively killed the pathogenic microorganisms and ensured the compost is harmless for all treatments [27]. The pile temperature decreased gradually afterwards with the depletion in organic matter [19,28]. The bulking effect of the zeolite might enhance the heat radiation, thus lowering the pile temperature of the cooling stage and the maturation stage [29,30]. Adding biochar significantly increased the pH, which could be caused by the alkalinity characteristics of the biochar [31]. The combined addition of biochar and zeolite promoted nitrogen retention and nutrient transformation during composting [18]. Zeolite has selective adsorption and sieving properties, especially the high polarity molecules such as H2O, NH3, CO2, etc. [32]. Zeolite can reduce the NH3 volatilization loss up to 44% [33]. Biochar is widely used as an additive to improve composting conditions and improve the quality of compost products because of its stable porous structure and good adsorption properties [34]. Biochar addition during composting significantly increased the NO3--N content and pile temperature, and decreased the pH and NH4+-N [35]. Biochar and zeolite mixing decreased the water-filled pore space, causing better aeration, and might be a potential reason explaining the greenhouse gas emission reduction.
Soil pH is one of the main factors of AOB community structure, including the direct effects on AOB and indirect effects on soil activity [36]. pH directly determined the presence of ammonia in the soil form: when the pH is lowered, the ammonia (NH3) will be converted to ammonium (NH4+), which reduces the amount of substrate NH3, and affects the activity, abundance and even species of AOB [37]. In most acidic soils, the number of AOA is higher than that of AOB, suggesting that AOA has stronger adaptability to low-pH habitats. Indeed, [38] also found a similar conclusion in Chinese tea-garden soils. In acidic tea-garden soil, the AOA/AOB ratio increased with the decrease in soil pH value, and the number of AOA showed a good positive correlation with soil ammonia-oxidizing activity.
Amendment of biochar and zeolite resulted in increased input of carbon and would stimulate microbial community activity during composting. Biochar amendment induced high respiration rates and fast organic matter decomposition, indicating higher microbial activity [39]. Organic and inorganic compounds were filled into biochar pores after composting [40]. Biochar can serve as niches for microbial community cultivation, as the biochar will provide a nitrogen source and decrease the free NH3 toxicity towards the microbial species [41]. Moreover, improved microbial activities caused higher nutrient consumption and lignocellulose biodegradation, thereby reducing the availability of the carbon and nitrogen substances. AOB and AOA both contain AMO genes that catalyze the first step of ammonium oxidation, responsible for converting ammonia to hydroxylamine. Some studies showed that the AOA amoA gene abundance was significantly higher than that of the AOB [26,42]. However, another study also indicated that AOB rather than its archaeal counterparts were distributed widely during composting of manure from field-scale facilities [43].
Enzyme activities reflect the biochemical reaction extent in environmental samples (e.g., composts, soils and waters), and also serve as a potential biological indicator for nutrition condition [44]. The AMO enzyme is encoded by the amoA, amoB and amoC genes [45]. Its activity influenced the rate-limiting step of the reaction process of NH4+-N to NH2OH [46,47]. Stimulation or inhibition of AMO was the combination results of multiple factors and some NO3--N production did not require AMO participation [48]. Different responses of AOB, AOA and AMO activity can be used as important indicators of the potential changes in the physico-chemical/biological condition of the composting process.
Previous research indicated no inhibitory effect was observed on the activities of a microbial community after clinoptilolite application [49]. Biochar and zeolite amendment will also affect the availability of toxins that determine the growth and activity of the microbial community. Zeolite can absorb the NH4+ cations in water [16], soils [50] and composting piles [51]. At the thermophilic stage, addition of biochar consequently alleviated the initial low pH [35]. As an indirect substrate of AOB, the concentration of NH4+-N is directly related to the quantity and species of AOB: the increase in ammonium concentration can lead to the increase in AOB quantity. A series of microcosmic experiments and ecological studies also confirmed that AOA is more suitable for growth in low-substrate environments [52]. The growth of two AOB and AOA species were significantly different under different substrate concentrations [53]. AOB grows well under high concentration of ammonia nitrogen. AOA can grow under high, medium and low matrix concentrations, whose growth is actually inhibited under high matrix concentrations. In grassland soil with a high substrate concentration, the increase in ammonia-oxidizing activity was accompanied by the increase in the number of AOB, indicating that AOB were the main drivers of the soil ammonia-oxidizing reaction at high substrate concentrations [54]. It was also reported that a high NH4+-N content inhibited the CO2 assimilation of thermophilic AOA, indicating that high levels of NH4+-N could affect the AOA community abundance and structure [55].
Which community was relatively more important seemed to be site-specific, depending on the raw material condition and different control strategies during agricultural waste composting. The AOB in this study was more sensitive than the AOA to changes in samples with biochar and zeolite addition. The different responses of the AOA and AOB due to the various changes in the physical and chemical composting conditions can be used as an important indicator of potential environmental condition change after amendment with biochar and zeolite. A previous study showed that the AOA community was relatively more abundant than that of the AOB during tropical agricultural waste composting [56]. In agricultural soil, nitrogen-rich grassland ecosystems and mangrove sediments, AOB has an obvious influence [57]. Higher organic matter and O2 content during composting provided unfavorable conditions for the AOA communities.

5. Conclusions

The effects of zeolite and biochar addition on the AOB and AOA amoA gene abundance and AMO enzyme activity were determined during agricultural waste composting. Results showed that the addition of zeolite and biochar changed the abundance of the AOB and AOA communities. A higher community abundance was found in samples with zeolite and biochar addition. Both the bacterial and archaeal amoA communities were found to be significantly and positively related to AMO enzyme activity during composting. The combined additives of zeolite and biochar stimulated the AOA and AOB communities and promoted nitrogen preservation during agricultural waste composting.

Author Contributions

Conceptualization, X.W. and L.R.; methodology, X.W. and L.R.; software, L.R. and H.P.; validation, X.W., and L.R.; formal analysis, X.W.; investigation, L.R.; resources, L.R. and J.Z.; data curation, L.R. and J.Z.; writing—original draft preparation, X.W. and L.R.; writing—review and editing, J.Z. and H.P.; visualization, J.Z.; supervision, J.Z. and H.P.; project administration, J.Z. and H.P.; funding acquisition, J.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (51408219), the Natural Science Foundation of Hunan Province (2020JJ5259), and the Outstanding Youth Fund project of Hunan Education Department (18B094).

Acknowledgments

The authors would like to thank the anonymous reviewers for their valuable comments and suggestions on previous versions of this paper.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Ren, L.; Cai, C.; Zhang, J.; Yang, Y.; Wu, G.; Luo, L.; Huang, H.; Zhou, Y.; Qin, P.; Yu, M. Key environmental factors to variation of ammonia-oxidizing archaea community and potential ammonia oxidation rate during agricultural waste composting. Bioresour. Technol. 2018, 270, 278–285. [Google Scholar] [CrossRef] [PubMed]
  2. Zeng, G.; Cheng, M.; Huang, D.; Lai, C.; Xu, P.; Wei, Z.; Li, N.; Zhang, C.; He, X.; He, Y. Study of the degradation of methylene blue by semi-solid-state fermentation of agricultural residues with Phanerochaete chrysosporium and reutilization of fermented residues. Waste Manag. 2015, 38, 424–430. [Google Scholar] [CrossRef] [PubMed]
  3. Bernal, M.; Alburquerque, J.; Moral, R. Composting of animal manures and chemical criteria for compost maturity assessment. A review. Bioresour. Technol. 2009, 100, 5444–5453. [Google Scholar] [CrossRef] [PubMed]
  4. Sánchez, A.; Artola, A.; Font, X.; Gea, T.; Barrena, R.; Gabriel, D.; Sánchez-Monedero, M.Á.; Roig, A.; Cayuela, M.L.; Mondini, C. Greenhouse gas emissions from organic waste composting. Environ. Chem. Lett. 2015, 13, 223–238. [Google Scholar] [CrossRef] [Green Version]
  5. Guillermo, P.; Raúl, M.; Eduardo, A.; Agustín, D.P. Gaseous emissions from management of solid waste: A systematic review. Glob. Chang. Biol. 2015, 21, 1313–1327. [Google Scholar]
  6. Chen, R.; Wang, Y.; Wang, W.; Wei, S.; Jing, Z.; Lin, X. N2O emissions and nitrogen transformation during windrow composting of dairy manure. J. Environ. Manag. 2015, 160, 121–127. [Google Scholar] [CrossRef]
  7. Du, J.; Zhang, Y.; Qu, M.; Yin, Y.; Fan, K.; Hu, B.; Zhang, H.; Wei, M.; Ma, C. Effects of biochar on the microbial activity and community structure during sewage sludge composting. Bioresour. Technol. 2019, 272, 171–179. [Google Scholar] [CrossRef]
  8. Zhang, J.; Luo, L.; Gao, J.; Peng, Q.; Huang, H.; Chen, A.; Lu, L.; Yan, B.; Wong, J.W. Ammonia-oxidizing bacterial communities and shaping factors with different Phanerochaete chrysosporium inoculation regimes during agricultural waste composting. RSC Adv. 2016, 6, 61473–61481. [Google Scholar] [CrossRef]
  9. Zhang, Y.; Zhao, Y.; Chen, Y.; Lu, Q.; Li, M.; Wang, X.; Wei, Y.; Xie, X.; Wei, Z. A regulating method for reducing nitrogen loss based on enriched ammonia-oxidizing bacteria during composting. Bioresour. Technol. 2016, 221, 276–283. [Google Scholar] [CrossRef]
  10. Awasthi, M.K.; Wang, M.; Pandey, A.; Chen, H.; Awasthi, S.K.; Wang, Q.; Ren, X.; Lahori, A.H.; Li, D.-S.; Li, R. Heterogeneity of zeolite combined with biochar properties as a function of sewage sludge composting and production of nutrient-rich compost. Waste Manag. 2017, 68, 760–773. [Google Scholar] [CrossRef]
  11. Jiang, T.; Ma, X.; Tang, Q.; Yang, J.; Li, G.; Schuchardt, F. Combined use of nitrification inhibitor and struvite crystallization to reduce the NH3 and N2O emissions during composting. Bioresour. Technol. 2016, 217, 210–218. [Google Scholar] [CrossRef] [PubMed]
  12. Santos, A.; Bustamante, M.; Tortosa, G.; Moral, R.; Bernal, M. Gaseous emissions and process development during composting of pig slurry: The influence of the proportion of cotton gin waste. J. Clean. Prod. 2016, 112, 81–90. [Google Scholar] [CrossRef]
  13. Wang, X.; Zhao, Y.; Wang, H.; Zhao, X.; Cui, H.; Wei, Z. Reducing nitrogen loss and phytotoxicity during beer vinasse composting with biochar addition. Waste Manag. 2017, 61, 150–156. [Google Scholar] [CrossRef] [PubMed]
  14. Wang, Q.; Awasthi, M.K.; Ren, X.; Zhao, J.; Li, R.; Wang, Z.; Wang, M.; Chen, H.; Zhang, Z. Combining biochar, zeolite and wood vinegar for composting of pig manure: The effect on greenhouse gas emission and nitrogen conservation. Waste Manag. 2018, 74, 221–230. [Google Scholar] [CrossRef]
  15. Sanchez-Garcia, M.; Alburquerque, J.A.; Sanchez-Monedero, M.A.; Roig, A.; Cayuela, M.L. Biochar accelerates organic matter degradation and enhances N mineralisation during composting of poultry manure without a relevant impact on gas emissions. Bioresour. Technol. 2015, 192, 272–279. [Google Scholar] [CrossRef]
  16. Chan, M.T.; Selvam, A.; Wong, J.W. Reducing nitrogen loss and salinity during ‘struvite’ food waste composting by zeolite amendment. Bioresour. Technol. 2016, 200, 838–844. [Google Scholar] [CrossRef]
  17. Awasthi, M.K.; Wang, Q.; Huang, H.; Ren, X.; Lahori, A.H.; Mahar, A.; Ali, A.; Shen, F.; Li, R.; Zhang, Z. Influence of zeolite and lime as additives on greenhouse gas emissions and maturity evolution during sewage sludge composting. Bioresour. Technol. 2016, 216, 172–181. [Google Scholar] [CrossRef]
  18. Awasthi, M.K.; Wang, Q.; Ren, X.; Zhao, J.; Huang, H.; Awasthi, S.K.; Lahori, A.H.; Li, R.; Zhou, L.; Zhang, Z. Role of biochar amendment in mitigation of nitrogen loss and greenhouse gas emission during sewage sludge composting. Bioresour. Technol. 2016, 219, 270–280. [Google Scholar] [CrossRef]
  19. Czekała, W.; Malińska, K.; Cáceres, R.; Janczak, D.; Dach, J.; Lewicki, A. Co-composting of poultry manure mixtures amended with biochar–The effect of biochar on temperature and C-CO2 emission. Bioresour. Technol. 2016, 200, 921–927. [Google Scholar] [CrossRef]
  20. Jindo, K.; Suto, K.; Matsumoto, K.; García, C.; Sonoki, T.; Sanchez-Monedero, M. Chemical and biochemical characterisation of biochar-blended composts prepared from poultry manure. Bioresour. Technol. 2012, 110, 396–404. [Google Scholar] [CrossRef]
  21. Zhou, G.; Xu, X.; Qiu, X.; Zhang, J. Biochar influences the succession of microbial communities and the metabolic functions during rice straw composting with pig manure. Bioresour. Technol. 2019, 272, 10–18. [Google Scholar] [CrossRef] [PubMed]
  22. Cáceres, R.; Malińska, K.; Marfà, O. Nitrification within composting: A review. Waste Manag. 2018, 72, 119–137. [Google Scholar] [CrossRef] [PubMed]
  23. Zhang, J.; Zeng, G.; Chen, Y.; Liang, J.; Zhang, C.; Huang, B.; Sun, W.; Chen, M.; Yu, M.; Huang, H. Phanerochaete chrysosporium inoculation shapes the indigenous fungal communities during agricultural waste composting. Biodegradation 2014, 25, 669–680. [Google Scholar] [CrossRef]
  24. Zhang, J.; Zeng, G.; Chen, Y.; Yu, M.; Huang, H.; Fan, C.; Zhu, Y.; Li, H.; Liu, Z.; Chen, M. Impact of Phanerochaete chrysosporium inoculation on indigenous bacterial communities during agricultural waste composting. Appl. Microbiol. Biotechnol. 2013, 97, 3159–3169. [Google Scholar] [CrossRef] [PubMed]
  25. Taylor, A.E.; Giguere, A.T.; Zoebelein, C.M.; Myrold, D.D.; Bottomley, P.J. Modeling of soil nitrification responses to temperature reveals thermodynamic differences between ammonia-oxidizing activity of archaea and bacteria. ISME J. 2017, 11, 896–908. [Google Scholar] [CrossRef]
  26. Zeng, G.; Zhang, J.; Chen, Y.; Yu, Z.; Yu, M.; Li, H.; Liu, Z.; Chen, M.; Lu, L.; Hu, C. Relative contributions of archaea and bacteria to microbial ammonia oxidation differ under different conditions during agricultural waste composting. Bioresour. Technol. 2011, 102, 9026–9032. [Google Scholar] [CrossRef]
  27. Wang, Q.; Wang, Z.; Awasthi, M.K.; Jiang, Y.; Li, R.; Ren, X.; Zhao, J.; Shen, F.; Wang, M.; Zhang, Z. Evaluation of medical stone amendment for the reduction of nitrogen loss and bioavailability of heavy metals during pig manure composting. Bioresour. Technol. 2016, 220, 297–304. [Google Scholar] [CrossRef]
  28. Wang, C.; Lu, H.; Dong, D.; Deng, H.; Strong, P.; Wang, H.; Wu, W. Insight into the effects of biochar on manure composting: Evidence supporting the relationship between N2O emission and denitrifying community. Environ. Sci. Technol. 2013, 47, 7341–7349. [Google Scholar] [CrossRef]
  29. Villasenor, J.; Rodriguez, L.; Fernandez, F. Composting domestic sewage sludge with natural zeolites in a rotary drum reactor. Bioresour. Technol. 2011, 102, 1447–1454. [Google Scholar] [CrossRef]
  30. Zhang, J.; Sui, Q.; Li, K.; Chen, M.; Tong, J.; Qi, L.; Wei, Y. Influence of natural zeolite and nitrification inhibitor on organics degradation and nitrogen transformation during sludge composting. Environ. Sci. Pollut. Res. 2015, 23, 1324–1334. [Google Scholar] [CrossRef]
  31. Li, R.; Wang, Q.; Zhang, Z.; Zhang, G.; Li, Z.; Wang, L.; Zheng, J. Nutrient transformation during aerobic composting of pig manure with biochar prepared at different temperatures. Environ. Technol. 2015, 36, 815–826. [Google Scholar] [CrossRef] [PubMed]
  32. Venglovsky, J.; Sasakova, N.; Vargova, M.; Pacajova, Z.; Placha, I.; Petrovsky, M.; Harichova, D. Evolution of temperature and chemical parameters during composting of the pig slurry solid fraction amended with natural zeolite. Bioresour. Technol. 2005, 96, 181–189. [Google Scholar] [CrossRef]
  33. Kithome, M.; Paul, J.; Bomke, A. Reducing nitrogen losses during simulated composting of poultry manure using adsorbents or chemical amendments. J. Environ. Qual. 1999, 28, 194–201. [Google Scholar] [CrossRef]
  34. Steiner, C.; Das, K.C.; Melear, N.; Lakly, D. Reducing nitrogen loss during poultry litter composting using biochar. J. Environ. Qual. 2010, 39, 1236–1242. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  35. Malińska, K.; Zabochnicka-Świątek, M.; Dach, J. Effects of biochar amendment on ammonia emission during composting of sewage sludge. Ecol. Eng. 2014, 71, 474–478. [Google Scholar] [CrossRef]
  36. Enwall, K.; Nyberg, K.; Bertilsson, S.; Cederlund, H.; Stenström, J.; Hallin, S. Long-term impact of fertilization on activity and composition of bacterial communities and metabolic guilds in agricultural soil. Soil Biol. Biochem. 2007, 39, 106–115. [Google Scholar] [CrossRef]
  37. Mendum, T.; Hirsch, P. Changes in the population structure of β-group autotrophic ammonia oxidising bacteria in arable soils in response to agricultural practice. Soil Biol. Biochem. 2002, 34, 1479–1485. [Google Scholar] [CrossRef]
  38. Yao, H.; Gao, Y.; Nicol, G.W.; Campbell, C.D.; Prosser, J.I.; Zhang, L.; Han, W.; Singh, B.K. Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Appl. Environ. Microbiol. 2011, 77, 4618–4625. [Google Scholar] [CrossRef] [Green Version]
  39. Clough, T.; Condron, L.; Kammann, C.; Müller, C. A review of biochar and soil nitrogen dynamics. Agronomy 2013, 3, 275–293. [Google Scholar] [CrossRef] [Green Version]
  40. Agyarko-Mintah, E.; Cowie, A.; Singh, B.P.; Joseph, S.; Van Zwieten, L.; Cowie, A.; Harden, S.; Smillie, R. Biochar increases nitrogen retention and lowers greenhouse gas emissions when added to composting poultry litter. Waste Manag. 2017, 61, 138–149. [Google Scholar] [CrossRef]
  41. Sun, D.; Lan, Y.; Xu, E.G.; Meng, J.; Chen, W. Biochar as a novel niche for culturing microbial communities in composting. Waste Manag. 2016, 54, 93–100. [Google Scholar] [CrossRef] [PubMed]
  42. Yamamoto, N.; Otawa, K.; Nakai, Y. Diversity and abundance of ammonia-oxidizing bacteria and ammonia-oxidizing archaea during cattle manure composting. Microb. Ecol. 2010, 60, 807–815. [Google Scholar] [CrossRef] [PubMed]
  43. Nozomi, Y.; Ryu, O.; Yoshihisa, S.; Chika, T.; Yutaka, N. Ammonia-oxidizing bacteria rather than ammonia-oxidizing archaea were widely distributed in animal manure composts from field-scale facilities. Microbes Environ. 2012, 27, 519–524. [Google Scholar]
  44. Tang, J.; Zhang, J.; Ren, L.; Zhou, Y.; Gao, J.; Luo, L.; Yang, Y.; Peng, Q.; Huang, H.; Chen, A. Diagnosis of soil contamination using microbiological indices: A review on heavy metal pollution. J. Environ. Manag. 2019, 242, 121–130. [Google Scholar] [CrossRef] [PubMed]
  45. Feike, J.; Jurgens, K.; Hollibaugh, J.T.; Kruger, S.; Jost, G.; Labrenz, M. Measuring unbiased metatranscriptomics in suboxic waters of the central Baltic Sea using a new in situ fixation system. ISME J. 2012, 6, 461–470. [Google Scholar] [CrossRef]
  46. Kuypers, M.M.M.; Marchant, H.K.; Kartal, B. The microbial nitrogen-cycling network. Nat. Rev. Microbiol. 2018, 16, 263–276. [Google Scholar] [CrossRef]
  47. Urakawa, H.; Rajan, S.; Feeney, M.E.; Sobecky, P.A.; Mortazavi, B. Ecological response of nitrification to oil spills and its impact on the nitrogen cycle. Environ. Microbiol. 2019, 21, 18–33. [Google Scholar] [CrossRef] [Green Version]
  48. Huang, X.; Xu, Y.; He, T.; Jia, H.; Feng, M.; Xiang, S.; Wang, S.; Ni, J.; Xie, D.; Li, Z. Ammonium transformed into nitrous oxide via nitric oxide by Pseudomonas putida Y-9 under aerobic conditions without hydroxylamine as intermediate. Bioresour. Technol. 2019, 277, 87–93. [Google Scholar] [CrossRef]
  49. Madrini, B.; Shibusawa, S.; Kojima, Y.; Hosaka, S. Effect of natural zeolite (clinoptilolite) on ammonia emissions of leftover food-rice hulls composting at the initial stage of the thermophilic process. J. Agric. Meteorol. 2016, 72, 12–19. [Google Scholar] [CrossRef] [Green Version]
  50. Lim, S.-S.; Lee, D.-S.; Kwak, J.-H.; Park, H.-J.; Kim, H.-Y.; Choi, W.-J. Fly ash and zeolite amendments increase soil nutrient retention but decrease paddy rice growth in a low fertility soil. J. Soils Sediment 2016, 16, 756–766. [Google Scholar] [CrossRef]
  51. Koenig, R.T.; Palmer, M.D.; Miner, F.D., Jr.; Miller, B.E.; Harrison, J.D. Chemical amendments and process controls to reduce ammonia volatilization during in-house composting. Compost Sci. Util. 2005, 13, 141–149. [Google Scholar] [CrossRef]
  52. Martens-Habbena, W.; Stahl, D.A. Nitrogen metabolism and kinetics of ammonia-oxidizing archaea. Methods Enzymol. 2011, 496, 465–487. [Google Scholar] [PubMed]
  53. Verhamme, D.T.; Prosser, J.I.; Nicol, G.W. Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J. 2011, 5, 1067–1071. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  54. Di, H.J.; Cameron, K.C.; Shen, J.P.; Winefield, C.S.; O’Callaghan, M.; Bowatte, S.; He, J.Z. Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiol. Ecol. 2010, 72, 386–394. [Google Scholar] [CrossRef] [Green Version]
  55. Hatzenpichler, R.; Lebedeva, E.V.; Spieck, E.; Stoecker, K.; Richter, A.; Daims, H.; Wagner, M. A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc. Natl. Acad. Sci. USA 2008, 105, 2134–2139. [Google Scholar] [CrossRef] [Green Version]
  56. De Gannes, V.; Eudoxie, G.; Dyer, D.H.; Hickey, W.J. Diversity and abundance of ammonia oxidizing archaea in tropical compost systems. Front. Microbiol. 2012, 3, 224. [Google Scholar] [CrossRef] [Green Version]
  57. Ding, L.J.; An, X.L.; Li, S.; Zhang, G.L.; Zhu, Y.G. Nitrogen loss through anaerobic ammonium oxidation coupled to iron reduction from paddy soils in a chronosequence. Environ. Sci. Technol. 2014, 48, 10641–10647. [Google Scholar] [CrossRef] [PubMed]
Sustainability 12 06336 g001 550
Figure 1. Pile temperature (a) and pH (b) for different treatments. Run A: control; Run B: compost + zeolite (5%); Run C: compost + biochar (5%); Run D: compost + zeolite (5%) + biochar (5%).
Figure 1. Pile temperature (a) and pH (b) for different treatments. Run A: control; Run B: compost + zeolite (5%); Run C: compost + biochar (5%); Run D: compost + zeolite (5%) + biochar (5%).
Sustainability 12 06336 g001
Sustainability 12 06336 g002 550
Figure 2. Ammonium (a) and nitrate (b) for different treatments. Run A: control; Run B: compost + zeolite (5%); Run C: compost + biochar (5%); Run D: compost + zeolite (5%) + biochar (5%).
Figure 2. Ammonium (a) and nitrate (b) for different treatments. Run A: control; Run B: compost + zeolite (5%); Run C: compost + biochar (5%); Run D: compost + zeolite (5%) + biochar (5%).
Sustainability 12 06336 g002
Sustainability 12 06336 g003 550
Figure 3. The bacterial amoA gene abundance for the different treatments. Different letters above the error bars indicate significant differences (P < 0.05) at each sampling occasion. Run A: control; Run B: compost + zeolite (5%); Run C: compost + biochar (5%); Run D: compost + zeolite (5%) + biochar (5%). The error bar is the mean value ± standard error.
Figure 3. The bacterial amoA gene abundance for the different treatments. Different letters above the error bars indicate significant differences (P < 0.05) at each sampling occasion. Run A: control; Run B: compost + zeolite (5%); Run C: compost + biochar (5%); Run D: compost + zeolite (5%) + biochar (5%). The error bar is the mean value ± standard error.
Sustainability 12 06336 g003
Sustainability 12 06336 g004 550
Figure 4. Archaeal amoA gene abundance for the different treatments. Different letters above the error bars indicate significant differences (P < 0.05) at each sampling occasion. Run A: control; Run B: compost + zeolite (5%); Run C: compost + biochar (5%); Run D: compost + zeolite (5%) + biochar (5%). The error bar is the mean value ± standard error.
Figure 4. Archaeal amoA gene abundance for the different treatments. Different letters above the error bars indicate significant differences (P < 0.05) at each sampling occasion. Run A: control; Run B: compost + zeolite (5%); Run C: compost + biochar (5%); Run D: compost + zeolite (5%) + biochar (5%). The error bar is the mean value ± standard error.
Sustainability 12 06336 g004
Sustainability 12 06336 g005 550
Figure 5. Changes in ammonia monooxygenase (AMO) enzyme activity for the different treatments. Different letters above the error bars indicate significant differences (P < 0.05) at each sampling occasion. Run A: control; Run B: compost + zeolite (5%); Run C: compost + biochar (5%); Run D: compost + zeolite (5%) + biochar (5%). AMO: ammonium monooxygenase activity. The error bar is the mean value ± standard error.
Figure 5. Changes in ammonia monooxygenase (AMO) enzyme activity for the different treatments. Different letters above the error bars indicate significant differences (P < 0.05) at each sampling occasion. Run A: control; Run B: compost + zeolite (5%); Run C: compost + biochar (5%); Run D: compost + zeolite (5%) + biochar (5%). AMO: ammonium monooxygenase activity. The error bar is the mean value ± standard error.
Sustainability 12 06336 g005
Sustainability 12 06336 g006 550
Figure 6. Relationships between ammonia monooxygenase (AMO) enzyme activity and bacterial amoA gene abundance during agricultural waste composting process. Line indicates the fitted curve, where y is the AMO enzyme activity (mmol g−1 d−1 DW sample) and x is the Log10 transformed AOB amoA gene abundance (gene copies g−1 DW sample) (n = 28). Run A: control; Run B: compost + zeolite (5%); Run C: compost + biochar (5%); Run D: compost + zeolite (5%) + biochar (5%).
Figure 6. Relationships between ammonia monooxygenase (AMO) enzyme activity and bacterial amoA gene abundance during agricultural waste composting process. Line indicates the fitted curve, where y is the AMO enzyme activity (mmol g−1 d−1 DW sample) and x is the Log10 transformed AOB amoA gene abundance (gene copies g−1 DW sample) (n = 28). Run A: control; Run B: compost + zeolite (5%); Run C: compost + biochar (5%); Run D: compost + zeolite (5%) + biochar (5%).
Sustainability 12 06336 g006
Sustainability 12 06336 g007 550
Figure 7. Relationships between ammonia monooxygenase (AMO) enzyme activity and archaeal amoA gene abundance during agricultural waste composting process. Line indicates the fitted curve, where y is the AMO enzyme activity (mmol g−1 d−1 DW sample) and x is the Log10 transformed AOA amoA gene abundance (gene copies g−1 DW sample) (n = 28). Run A: control; Run B: compost + zeolite (5%); Run C: compost + biochar (5%); Run D: compost + zeolite (5%) + biochar (5%).
Figure 7. Relationships between ammonia monooxygenase (AMO) enzyme activity and archaeal amoA gene abundance during agricultural waste composting process. Line indicates the fitted curve, where y is the AMO enzyme activity (mmol g−1 d−1 DW sample) and x is the Log10 transformed AOA amoA gene abundance (gene copies g−1 DW sample) (n = 28). Run A: control; Run B: compost + zeolite (5%); Run C: compost + biochar (5%); Run D: compost + zeolite (5%) + biochar (5%).
Sustainability 12 06336 g007
Table
Table 1. The physicochemical properties of the raw materials and different piles for composting.
Table 1. The physicochemical properties of the raw materials and different piles for composting.
Raw materials or Different PilesTOC (%)TN (%)C/N ratioMoisture (%)pHAmmonium (mg/kg)Nitrate (mg/kg)
Rice straw436.88.750.27.9---
Vegetable112.54.823.479.67.2--
Soil62.42.322.815.85.8--
Bran474.844.510.712.5---
Zeolite---1.2---
Biochar50.0--7.09.0838.27.0
Run A272.58.331.762.35.42692.8957.2
Run B251.68.529.659.85.65673.5890.5
Run C275.58.432.858.65.25668.21016.8
Run D259.68.730.958.25.24659.81027.2
- Data was not determined. TOC: Total organic carbon; TN: Total nitrogen.

Share and Cite

MDPI and ACS Style

Wu, X.; Ren, L.; Zhang, J.; Peng, H. Effects of Zeolite and Biochar Addition on Ammonia-Oxidizing Bacteria and Ammonia-Oxidizing Archaea Communities during Agricultural Waste Composting. Sustainability 2020, 12, 6336. https://0-doi-org.brum.beds.ac.uk/10.3390/su12166336

AMA Style

Wu X, Ren L, Zhang J, Peng H. Effects of Zeolite and Biochar Addition on Ammonia-Oxidizing Bacteria and Ammonia-Oxidizing Archaea Communities during Agricultural Waste Composting. Sustainability. 2020; 12(16):6336. https://0-doi-org.brum.beds.ac.uk/10.3390/su12166336

Chicago/Turabian Style

Wu, Xin, Liheng Ren, Jiachao Zhang, and Hui Peng. 2020. "Effects of Zeolite and Biochar Addition on Ammonia-Oxidizing Bacteria and Ammonia-Oxidizing Archaea Communities during Agricultural Waste Composting" Sustainability 12, no. 16: 6336. https://0-doi-org.brum.beds.ac.uk/10.3390/su12166336

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop