Nitrate effects on chromate reduction in a methane-based biofilm
Graphical abstract
Introduction
Chromium (Cr) pollution of water bodies is caused by a variety of industries, including alloy production, petroleum refining, electroplating, dyes, and wood preservation (Kantar et al., 2008, He et al., 2015, Barnhart, 1997). Cr(VI) in water is a health concern because of its carcinogenicity, mutagenicity, and teratogenicity (Cieslak-Golonka, 1996), and the maximum contaminant level (MCL) of Cr for drinking water is 100 μg Cr/L (USEPA, 2015). A frequent co-contaminant with chromate in surface and ground waters is nitrate (NO3−), which is widely used in agricultural fertilizer and industrial production (Chen and Strous, 2013). NO3− and its reduction intermediate, nitrite (NO2−), impose serious negative effects, as they can cause methemoglobinemia in infants and accelerate water's eutrophication (Addiscott and Benjamin, 2004, Schindler, 1974). The typical MCLs for NO3− and NO2− in drinking water are 10 and 1 mg N/L, respectively (USEPA, 2015).
Biological reductions of Cr(VI) and NO3− have gained great interest in past decades due to their economic and environmental advantages over physicochemical remediation (Ganguli and Tripathi, 2002). Reduction of Cr(VI) to Cr(III) is a viable means for detoxifying wastewater containing Cr(VI). While Cr(VI) has a high solubility, Cr(III) can be precipitated as Cr(OH)3, and Cr(III) is approximately 100 times less toxic than Cr(VI). Reduction of NO3− to N2 gas renders it totally harmless.
Cr(VI) and NO3− can be reduced simultaneously in a variety of bioreactors. Sahinkaya and Kilic (2014) applied a column reactor with sulfur as the electron donor, Miao et al. (2015) used a granular sludge bed supplied with acetate, and Chung et al. (2006) utilized hydrogen (H2) gas in the membrane biofilm reactor (MBfR). Recently, methane (CH4)-based bio-reduction of Cr(VI) have gained attention (Hasin et al., 2010, Lai et al., 2016), since CH4 is relatively inexpensive and widely available (Modin et al., 2007, Lin et al., 2014, Hu et al., 2014).
A novel and promising means to supply CH4 to biomass is the CH4-based MBfR, in which CH4 diffuses through the walls of hollow-fiber membranes and is oxidized by biofilm attached on the fibers' outer wall, where microbial reductions of Cr(VI) and NO3− occur (Lai et al., 2014, Luo et al., 2015). Simultaneous Cr(VI) and NO3− bio-reduction in the CH4-based MBfR has never been explored. Thus, the first objective of this study is to test for interactions between Cr(VI) and NO3− reductions in a CH4-based MBfR. We study the reduction patterns of Cr(VI) and NO3− with different input of Cr(VI) and NO3− when the delivery capacity for the donor (CH4) is not rate limiting.
One possible interaction is that Cr(VI) inhibits NO3− reduction. He et al. (2015) saw that NO3− reduction by Pseudomonas aeruginosa strain PCN-2 was dramatically inhibited with increasing input Cr(VI). In contrast, the effects of NO3− on Cr(VI) reduction should depend on the microbial community. Chromate-reducing bacteria are phylogenetically diverse, e.g., Pseudomonas sp (McLean and Beveridge, 2001), Shewanella oneidensis (Myers et al., 2000), Bacillus sp (Campos et al., 1995), Enterobacter cloacae (Waki et al., 1989), Staphylococcus epidermidis (Vatsouria et al., 2005), and Desulfovibrio vulgaris (Lovley and Phillips, 1994). Positive and negative effects of NO3− on Cr(VI) reduction have been reported, depending on the strains. Han et al. reported that NO3− improved Cr(VI) reduction (10-fold more rapid) for strain RCH2 (Han et al., 2010), a bacterium similar to Pseudomonas stutzeri, Vatsouria et al. (2005) showed that Staphylococcus epidermidis L-02 reduced Cr(VI) with a relatively minor increased rate (11%) when NO3− was present, and Viamajala and Peyton (2002) found that Cr(VI) reduction by Shewanella oneidensis MR-1 was significantly inhibited when NO3− or NO2− was introduced into the medium. Furthermore, when NO3− was introduced, denitrifiers thrived and became strong competitors for electrons and spaces, a factor that might inhibit Cr(VI) reduction (Lai et al., 2014). Thus, our second objective is to characterize the community structure of the biofilms using high-throughput sequencing technology and use that information to understand the ecological basis for performance changes associated with the first objective.
Bio-reduction of Cr(VI) to Cr(III) can be mediated by a series of chromate reductases, including cytochromes and nitroreductases (Lovley and Phillips, 1994, He et al., 2010). Some reduction agents, e. g., glutathione (Liu et al., 2012), thioredoxin (Chen et al., 2014), and ferredoxin (Chardin et al., 2003), also have the capability to reduce Cr(VI). As competing electron accepters, NO3− and NO2− might interact with these metalloenzymes and thus influence Cr(VI) reduction (Aydin et al., 2006). Accordingly, Cr(VI) might alter enzyme conformation and affect essential functional genes involved in the denitrification process (Miao et al., 2015, Zou et al., 2014). Therefore, our third objective is to understand the evolution of functional genes using Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt).
Section snippets
Startup and continuous operation
Experiments were conducted with the same MBfR system and deoxygenated input medium as in Lai et al. (2016). The MBfR had composite hollow fibers (OD: 280 μm, ID: 180 μm) manufactured by Mitsubishi Rayon (model MHF-200TL, Mitsubishi, Ltd., Japan). The main bundle contained 32 fibers, while the coupon fibers were in 10 for biofilm sampling. The total membrane surface area was 58 cm2, while the total volume of the MBfR was 65 mL. The liquid inside the MBfR system was completely mixed by water
Interaction between chromate and nitrate reductions (objective one)
Fig. 1A shows the influent concentrations of Cr(VI) and NO3−, along with the effluent concentrations of Cr(VI), total soluble Cr, NO3−, and NO2−, while Fig. 1B shows the removal percentages of Cr(VI) and NO3−. The fluxes of Cr(VI), NO3−, and O2 (from eqs (2), (3))) are summarized in Table 1 for each stage at steady state. The actual CH4 flux was much smaller than the maximum CH4 flux that can be delivered through the composite fiber at the applied H2 pressure (10 psig), meaning that the CH4
Conclusions
In summary, we found NO3− had a significant inhibition effect on Cr(VI) reduction in the CH4-based MBfR, although the CH4 supply capacity was sufficient through all stages. When Cr(VI) was the only electron acceptor at a surface loading of 500 mg Cr/m2-d in Stage 1, Cr was fully removed. A NO3− loading rate at 280 mg N m−2-d in Stage 2 dramatically lowered Cr(VI) reduction to < 25%, while NO3− removal was only 50%. The Cr(VI) reduction recovered to only ∼70% in Stage 3 when NO3− was absent,
Acknowledgments
Authors greatly thank the “Open Project of State Key Laboratory of Urban Water Resource and Environment (Harbin Institute of Technology, Grant No QAK201605)”, the “National Natural Science Foundation of China (Grant No. 21377109, 21577123)”, and “Natural Science Funds for Distinguished Young Scholar of Zhejiang Province (LR17B070001)” for their financial support. We greatly thank the Shanghai Tongji Gao Tingyao Environmental Science & Technology Development Foundation for the partial support.
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