Influence of light intensity on bacterial nitrifying activity in algal-bacterial photobioreactors and its implications for microalgae-based wastewater treatment

https://doi.org/10.1016/j.ibiod.2016.06.006Get rights and content

Highlights

  • Light irradiation over 500 μmol/m2 s reduces bacterial nitrifying activity.

  • Nitrite oxidizers are more light-sensitive than ammonia oxidizers.

  • Light attenuation by microalgae may prevent nitrification photoinhibition.

Abstract

The influence of irradiance on the nitrifying activity in photobioreactors of a bacterial consortium enriched from a wastewater treatment bioreactor was assessed using independent ammonium oxidation kinetic batch tests and respirometric assays. Culture irradiance below 250 μmol m−2 s−1 did not show a significant effect on nitrification activity, while irradiance at 500 and 1250 μmol m−2 s−1 caused a decrease of 20 and 60% in the specific total ammonium nitrogen removal rates and a reduction of 26 and 71% in the specific NO3 production rates, respectively. However, no significant influence of irradiance on the affinity constant of NH4+ oxidation was observed. The increasing nitrite accumulation at higher light intensities suggested a higher light sensitivity of nitrite oxidizers. Additionally, NH4+ oxidation respirometric assays showed a decrease in the oxygen uptake of 14 and 50% at 500 and 1250 μmol m−2 s−1, respectively. The experimental determination of the light extinction coefficient (λ) of the nitrifying bacterial consortium (λ = 0.0003 m2 g−1) and of Chlorella sorokiniana (λ = 0.1045 m2 g−1) allowed the estimation of light penetration in algal-bacterial high rate algal ponds, which showed that photoinhibition of nitrifying bacteria can be significantly mitigated in the presence of high density microalgal cultures.

Introduction

Microalgae mass cultivation has experienced a significant growth in the last years, boosted by the interest in third generation biofuel production. This interest on microalgal biofuels has been accompanied by economic and environmental sustainability studies, which recommended microalgae cultivation associated to either CO2 capture from flue gases (Kesaano and Sims, 2014) or wastewater treatment in order to reduce their high operational cost and environmental impact (Park et al., 2011, Lananan et al., 2014, Kim et al., 2013). This quest for a sustainable mass production of microalgae has generated an intensive research in the development of microalgae-based technologies for the treatment of urban, industrial and livestock wastewaters (Muñoz and Guieysse, 2006). Microalgae have been used as low cost in-situ oxygenators for the bacterial oxidation of organic carbon and ammonium (Su et al., 2011, Lananan et al., 2014) and as a fixation tool for the removal of soluble nitrogen and phosphorous via photosynthesis during wastewater treatment (Posadas et al., 2013). In these processes, nitrification can play a key role in nitrogen management (Hernández et al., 2011). On the one hand, nitrification can prevent nitrogen losses by NH3 volatilization (Abdel-Raouf et al., 2012), while reducing the toxic inhibitory effects of high NH3 concentrations on microalgae growth (Collos and Harrison, 2014). In addition, nitrification can support the implementation of N removal strategies via denitrification in wastewaters with a low C/N ratio (de Godos et al., 2014).

The coexistence of nitrifying bacteria and microalgae has been reported in High Rate Algal Ponds (HRAP) (Park et al., 2011) and biofilm photobioreactors devoted to the domestic wastewater treatment (Muñoz and Guieysse, 2006, Posadas et al., 2013). For example, Posadas et al. (2014) observed a decrease in NH3 stripping in an open biofilm photobioreactor treating domestic wastewater as a result of NH4+ nitrification and its associated pH decrease in the cultivation broth. Moreover, de Godos et al. (2014) reported removals of organic carbon and nitrogen exceeding 95% and 90%, respectively, during the treatment of wastewaters with low C/N ratios (∼3) in a novel two-stage anoxic-aerobic photobioreactor. Despite the relevance of nitrification in microalgae-based wastewater treatment systems, there are few studies assessing the influence of the particular environmental conditions present in algal-bacterial photobioreactors on the performance of nitrifying communities. The particular configuration of photobioreactors, compared to the deep tanks used in activated sludge processes, entails an efficient light penetration in the algal-bacterial cultivation broth as a result of their high illuminated area to volume ratio (Merchuk et al., 2007). In this context, while early studies suggested that light can inhibit both microbial ammonium and nitrite oxidation (Alleman et al., 1987, Diab and Shilo, 1988, Guerrero and Jones, 1996a, Guerrero and Jones, 1996b, Hooper and Terry, 1974, Kaplan et al., 2000, Merbt et al., 2012, Müller-Neuglück and Engel, 1961, Yoshioka and Saijo, 1984), others investigations observed a light-mediated nitrification enhancement (Harris and Smith, 2009). Therefore, there is a lack of fundamental studies assessing the impact of light intensity on the microbial kinetics of NH4+ and NO2 oxidation, and its potential implications in microalgae-based wastewater treatment in photobioreactors.

In this study, the influence of irradiance on the nitrifying bacterial activity was evaluated through kinetics and respirometric assays. In addition, the light extinction coefficients of nitrifying bacteria and Chlorella sorokiniana were experimentally determined and used to estimate the potential impact of light penetration on the global nitrification process in wastewater-treating HRAPs.

Section snippets

Microorganisms and cultivation media

The bacterial photoinhibition assays were inoculated with a nitrifying bacterial community obtained from a sequencing batch rotating disk bioreactor treating synthetic wastewater for 2 years using NH4+ as the sole energy and nitrogen source. The inoculum was prepared by acclimating the nitrifying community for 6 months in a modified Nakos and Wolcott mineral salt medium (MSM) (Elbanna et al., 2012), in the absence of light, at a constant pH of 7.5 ± 0.2 and dissolved oxygen concentrations over

Photoinhibition assays in batch ammonium oxidation kinetic tests

The kinetic tests illuminated at 0, 250, 500 and 1250 μmol m−2 s−1 showed a linear ammonium removal within the first 4, 4, 6 and 14 days of cultivation, respectively (Fig. 2). The initial specific ammonium removal rates at 0 and 250 μmol m−2 s−1 were not significantly different (0.101 ± 0.003 mg-TAN mg-VSS−1 d−1), while a reduction of 20% and 64% was observed at 500 and 1250 μmol m−2 s−1, respectively (Table 1). Likewise, while the specific nitrate production rates were comparable at 0 and

Discussion

This study confirmed that ammonium and nitrite oxidizers can be photoinhibited at the high irradiances typically encountered under outdoors conditions, which can achieve 2000–3000 μmol m−2 s−1 during peak hour (Wang et al., 2008). Culture irradiance below 250 μmol m−2 s−1 did not influence the activity of nitrifying bacterial cultures in terms of specific ammonium removal rate and nitrate production rates. However, light intensities of 1250 μmol m−2 s−1 reduced nitrifying activity by 64% and

Conclusions

This study showed a significant inhibitory effect of irradiance on the nitrifying activity of NH4+ and NO2 oxidizers above 500 μmol m−2 s−1. Nitrite oxidizers exhibited a lower phototolerance at the light intensities typically found under outdoors conditions. However, this inhibitory effect can be mitigated under photobioreactor operation due to the high extinction coefficient of the microalgae that symbiotically coexist with nitrifying bacteria.

Acknowledgements

Authors want to thank the financial support provided by projects Fondecyt 1120488 (CONICYT-Chile), USM 131342 and DIDUFRO DI14-0077. Author would also like to thank Dr. Carlos Vilchez for kindly supplying of C. sorokiniana. Dr. Jeison would like to acknowledge support provided by CRHIAM centre (CONICYT/FONDAP 15130015).

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