Effect of aquaculture salinity on nitrification and microbial community in moving bed bioreactors with immobilized microbial granules

doi:10.1016/j.biortech.2019.122427

Bioresource Technology

Volume 297, February 2020, 122427

https://doi.org/10.1016/j.biortech.2019.122427 Get rights and content

Highlights

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Immobilized microbial granules improved salinity tolerance.
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High ammonia removal (92%) was achieved at salinity up to 35.0 g/L.
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Nitrite oxidation bacteria was depressed at salinity above 15.0 g/L.
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Microbial community structure was shifted as salinity increased.
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Nitrosomonas sp. and Nitrospira sp. were the dominant genera.

Abstract

The novel immobilized microbial granules (IMG) shows a significant effect of nitrification for freshwater aquaculture. However, there is lack of evaluation study on the performance of nitrification at high salinity due to the concentration of recycled water or seawater utilization. A laboratory scale moving bed bioreactor (MBBR) with IMG was tested on recycled synthetic aquaculture wastewater for the nitrification at 2.5 mg/L NH₃-N daily. The results indicated that IMG showed a high salinity tolerance and effectively converted ammonia to nitrate up to 92% at high salinity of 35.0 g/L NaCl. As salinity increased from near zero to 35.0 g/L, the microbial activity of nitrite oxidation bacteria (NOB) in the IMG decreased by 86.32%. The microbial community analysis indicated that salinity significantly influenced the community structure. It was found that Nitrosomonas sp. and Nitrospira sp. were the dominant genera for ammonia oxidation bacteria (AOB) and NOB respectively at different salinity levels.

Graphical abstract

Introduction

Recirculating aquaculture systems (RAS) are viewed as a sustainable aquacultural practice to fulfill the rising global seafood demand (Navada et al., 2019). Compared to the flow-through production systems or the net-pens production systems, RAS use much less water, and the water can be recycled up to 90–99% by applying a series of water treatment methods (Badiola et al., 2012). In addition, RAS have a lower ecological impact than the marine fisheries by avoiding the direct discharge of nutrient and toxic waste into the sea (Zeller et al., 2018).

In order to mass produce the high nutrient-dense aquaculture products, the optimum water quality control and wastewater management is highly needed for an effective operation of RAS (Goddek et al., 2018). The high level of ammonia and nitrite for instance poses a high risks to the life of the aquatic animals (Goddek et al., 2018) and decrease the productivity of aquaculture (Wongkiew et al., 2017). Kumar et al. (2010) reported that marine larva could not tolerate the concentration of the total ammonia nitrogen (TAN) and nitrite-N above 1.0 mg/L. Ebeling et al. (2006) also suggested that the NH₃ concentration should be below 0.05 mg/L under long term exposure. On the other hand, the conversions of total ammonia and nitrate content are strongly related to the salinity level in wastewater. High salinity in wastewater treatment system can be considered as one of the common stress condition that might causes significantly negative impacts on the biological metabolic activity (Moussa et al., 2006), bacterial community structure (Kinyage et al., 2019), and settling properties of nitrifying bacteria, therefore causing the failure of nitrification processes (Yogalakshmi and Joseph, 2010). Extensive researches have been conducted and proved that microbial biomass and biodiversity of activated sludge may reduce significantly as increase of salinity level, while, the salt-tolerant microorganism which originally not the dominant species might increase gradually in the system (He et al., 2017). Hence, there is a need to maintain a low level of ammonia and nitrite content in the aquaculture water especially for the RAS (Jiang et al., 2019).

Use of IMG for nitrification has been widely known as an effective biotechnology technique for wastewater treatment (Dong et al., 2017). The novel IMG was composed of gel-based polymer granules with immobilized nitrifying bacteria that was enriched from a municipal wastewater treatment plant. It has the advantages of high biological density, high volumetric metabolic activities, limited sludge production, and short hydraulic retention time (HRT) (Tabassum et al., 2015) due to facilitating cell separation and protection from extreme conditions (Isaka et al., 2007). In the previous report by Tabassum et al. (2018), IMG could remove up to 95% of ammonia (3.5 mg/L) with a short HRT of 4 h. IMG was able to maintain optimum fresh water quality by removing nitrogen pollutant at an efficiency of 71.8% for NH₃-N and 51.5% for NO₂-N in a tested laboratory-scale system (Li et al., 2019). However, the overall performance of IMG in the brackish effluent and other water sources containing seawater with high salinity has not been studied.

Nitrifying bacteria from the brackish and marine water have been characterized using universal 16S rRNA gene and bacterial amoA gene sequencing (Kumar et al., 2010). They reported that the most dominant AOB included Nitrosomonas sp. and Nitrosospira sp and the most dominant NOB were Nitrobacter sp. and Nitrospira sp. Gonzalez-Silva et al. (2016) studied the microbial communities at different salinity using 454-pyrosequencing of 16S rRNA gene amplicons. The results indicated that Nitrosomonas sp was the sole AOB species in the three reactors. Nitrobacter sp. and Nitrospira sp. were the key NOB species in the freshwater and N. marine for the salt water reactors. However, a limited number of studies are available in the literature addressing the nitrification efficiency and microbial community of nitrifying bacteria using immobilized microbes under a range of salinity level.

In this study, a laboratory-scale MBBR filled with IMG was developed to treat nitrogen pollutant in the simulated RAS with the ammonia concentration of 2.5 mg/L using brackish and seawater. The microbial activities and communities for AOB and NOB were monitored under different salinity levels in order to evaluate the nitrification process using IMG. The results from this study are expected to provide useful benchmarks for developing MBBR with IMG, advancing the knowledge of designing effective inoculum in IMG in the future work by knowing the dominant microbial community at different salinity levels and its corresponding performance.

Section snippets

Bioreactor system

The immobilized microbial granules (IMG) are the form of gel-polymer cubic granules that were immobilized with nitrifying bacteria (the side length is 2–5 mm, with a specific gravity of 1.02–1.08) (Fig. 1). The inoculated microbial cells were collected from a local wastewater treatment plant and enriched with ammonia-containing wastewater prior to the immobilization. The granules were comprised of enriched microbial culture, powdered activated carbon from bamboo pieces and waterborne

The effect of salinity on nitrification

The changes in the concentrations of ammonia, nitrite and nitrate in the MBBR at different salinities are shown in Fig. 2. Over 14 d of operation at a salinity of near zero, the NH₃-N was converted to NO₃⁻-N completely with the final concentration of 0.2 mg/L. The removal efficiency increased gradually and then stabilized at 84.9–92.0% (Fig. 2a) without nitrite accumulation (Fig. 2b). The average rate of nitrate accumulation was found at 2.2 g/(L·d) (Fig. 2c). The salinity increased to 5.0 mg/L

Conclusions

The novel Immobilized microbial granules (IMG) were characterized in response to the increased salinity up to 35.0 g/L NaCl in the MBBR in terms of nitrifying metabolic activities and microbial communities. It was found that ammonia was effectively removed and converted to nitrate and nitrite with conversion efficiency up to 92% with salinity of 35.0 g/L NaCl. Inhibition occurred for the conversion of nitrite to nitrate at the salinity above 15.0 to 25.0 g/L NaCl, resulting in the accumulation

CRediT authorship contribution statement

Yueshu Gao: Conceptualization, Methodology, Writing - original draft. Xupeng Wang: Investigation, Visualization. Jialun Li: Investigation, Software. Chew Tin Lee: Visualization, Writing - review & editing. Pei Ying Ong: Software, Validation. Zhenjia Zhang: Supervision, Resources. Chunjie Li: Writing - review & editing, Project administration.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

This research is financially supported by Natural Science Foundation Council of China (No. 21808141), National Science and Technology Commission of Shanghai Municipality (No. 18230743000) and Startup Fund for Youngman Research at SJTU (17X100040069). We appreciate help and suggestions from Dr. Weimin Wu, Department of Civil & Environmental Engineering, Stanford University, USA and Dr. Haslenda Hashim, Faculty of Chemical & Energy Engineering, Universiti Teknologi Malaysia, Malaysia.