This work assessed the effect of adding different concentrations of nitrate (50–300 mg ·L−1) on the removal of dissolved and gaseous sulfide in an anaerobic reactor treating synthetic effluent containing sulfate (100 mg ·L−1) and organic matter (1 g COD·L−1). Autotrophic denitrification, stimulated by the addition of nitrate, was demonstrated to be a very effective approach for removal of dissolved sulfide even in the presence of a high concentration of organic matter (complete removal with 50 mg mg·L−1). However, it had a minor effect on H2S(g). Sulfide remained partially oxidized to elemental sulfur even with excess nitrate (100–300 mg mg·L−1). Therefore, the competition for this electron acceptor between the autotrophic and heterotrophic denitrification pathways may have prevented the conversion of the generated sulfide into sulfate again. No evidence of inhibition of methanogenesis and sulfidogenesis was found during nitrate supplementation.

  • Dissolved sulfide was completely removed with 50 mg ·L−1.

  • Autotrophic denitrification occurred even with high content of organic matter.

  • Sulfide was oxidized to S0 even with excess nitrate (100–300 mg ·L−1).

  • Heterotrophic denitrification may have prevented oxidation of sulfide to sulfate.

  • Methanogenesis and sulfidogenesis were not inhibited by nitrate supplementation.

During the anaerobic treatment of sulfate-containing wastewaters, such as domestic wastewater and some industrial effluents (e.g. textile, leather, paper and pulp, food, etc.), sulfate-reducing bacteria (SRB) use sulfate as an electron acceptor for the degradation of organic compounds, producing sulfide. This reduced sulfur compound can be present in both the liquid (H2S, HS, and S2−) and biogas (exclusively H2S), depending on the pH and temperature of the medium. For instance, at pH 7 (typical of anaerobic systems), 50% of sulfide is in the form of H2S (mostly dissolved in the liquid, and only a very small fraction in the biogas), and 50% in the form of HS (Lens et al. 1998).

The presence of H2S in the biogas is undesirable because this compound is corrosive, malodorous (even at a concentration as low as 0.2 ppm), toxic (chemical asphyxiant), and generates sulfur dioxide during the combustion of biogas (Krayzelova et al. 2015). Therefore, as it decreases the quality of the biogas, compromising its use as a fuel in cogeneration units, many technologies have been developed and improved to address this problem, such as chemical precipitation, caustic scrubbing, adsorption, bioscrubbing, biofiltration, microaeration, etc. (Muñoz et al. 2015; Wasajja et al. 2020).

However, as mentioned above, the dissolved fraction of sulfide (HS + H2S) is much greater than the gaseous one and can also cause a number of problems, such as inhibition of acetogens and methanogens, accumulation of inert material inside the reactor (e.g. metal sulfides), and malfunction of aerobic post-treatment systems (e.g. activated sludge bulking) (Pokorna-Krayzelova et al. 2018). Moreover, as H2S is volatile, it may be released from the anaerobic effluent into the air during the aeration in aerobic post-treatment systems or even after its discharge into the receiving water body, thus causing atmospheric contamination. Therefore, the dissolved sulfide is also an important problem associated with the anaerobic treatment of sulfate-containing wastewater that must be properly addressed.

Within this context, autotrophic denitrification via nitrate seems to be an appropriate solution for the removal of dissolved sulfide in anaerobic wastewater treatment systems, since sulfide can be used as an electron donor for the reduction of nitrate (Reyes-Avila et al. 2004; Beristain-Cardoso et al. 2008; Chen et al. 2008; Show et al. 2013; Di Capua et al. 2019). Depending on the nitrate availability, sulfide is partially oxidized to elemental sulfur or completely oxidized to sulfate (Equations (1) and (2), respectively). Therefore, the addition of nitrate to the system must be controlled to prioritize the reaction presented in Equation (1) and actually remove sulfur from wastewater, as elemental sulfur is insoluble.
formula
(1)
formula
(2)

It is worth mentioning that, for removing nitrogen from wastewater, anaerobic reactors are usually associated with aerobic post-treatment systems (Chernicharo et al. 2015). In such a sequential anaerobic-aerobic configuration, ammonium from the anaerobic reactor is oxidized to nitrate (nitrification) in the aerobic system. Then, part of the nitrified effluent is recirculated back to the anaerobic reactor to remove nitrate by denitrification (Kassab et al. 2010). Therefore, the nitrified effluent may also be used as a nitrate source for sulfide removal by autotrophic denitrification, supplying or at least decreasing the demand for an external nitrate source (nitrate salts) to be added to the anaerobic reactor.

However, the presence of organic matter can hinder the process due to the competition for nitrate between the autotrophic and heterotrophic denitrification (Show et al. 2013). Consequently, setting the correct dosage of nitrate (from chemicals or nitrified effluents) in systems treating wastewater containing organic matter may not be simple. Therefore, it is important to investigate further this approach in anaerobic reactors treating wastewater containing sulfate and organic matter (e.g. domestic wastewater), as various metabolic pathways (methanogenesis, sulfidogenesis, heterotrophic and autotrophic denitrification) occur simultaneously and can affect each other. Additionally, it is important to mention that most studies have investigated the autotrophic denitrification process for effluents that already contain sulfide (non-biogenic sulfide) and low content of organic matter (Show et al. 2013; Huang et al. 2016; Liu et al. 2017).

Hence, this work assessed the effect of adding different concentrations of nitrate on the removal of dissolved and gaseous sulfide in an anaerobic reactor treating synthetic effluent containing sulfate and organic matter.

Experimental set-up

The experimental investigation was carried out in an upflow anaerobic sludge blanket (UASB) reactor (working volume of 3.0 L) inoculated with anaerobic sludge (∼56 g TVS·L−1) from a UASB reactor of a domestic wastewater treatment plant (Fortaleza, Ceará, Brazil) and operated at a hydraulic retention time (HRT) of 8 h and room temperature of approximately 28 °C. The reactor was fed with synthetic wastewater composed of ethanol as a carbon source (∼1.0 g COD·L−1), sodium sulfate (Na2SO4) as a sulfate source (∼0.1 g ·L−1), basal medium (Firmino et al. 2010), and sodium bicarbonate (NaHCO3) as a buffer (1.0 g·L−1) to keep the pH close to 7.0. When necessary, sodium nitrate (NaNO3) was used as a nitrate source and added to the wastewater. The feeding tank was stored at approximately 5 °C to prevent premature degradation of the wastewater. The biogas produced was measured by a MilliGascounter MGC-1 V3.3 PMMA gas meter (Dr-Ing. RITTER Apparatebau GmbH & Co. KG, Germany).

Experimental procedure

The experimental investigation was carried out throughout six periods (Table 1). In period I, the anaerobic reactor was fed with nitrate-free wastewater. Then, from period II to V, different nitrate concentrations were added to the wastewater (100, 200, 300, and 50 mg ·L−1, respectively) to evaluate its effect on the removal of dissolved and gaseous sulfide. It is worth mentioning that nitrate was dosed in excess to minimize the competition between the heterotrophic and autotrophic denitrification pathways. Finally, in period VI, the reactor was operated under the same conditions as in period I.

Table 1

Operational performance of the anaerobic reactor throughout the experiment

PeriodIIIIIIIVVVI
Duration (days) 116 147 42 51 63 42 
Added nitratea (mg·L−1– 100 200 300 50 – 
N/S molar ratiob – 1.4 3.9 4.4 0.7 – 
CODc Influent (mg·L−11,051 (112) 918 (101) 1,135 (190) 1,139 (91) 1,119 (157) 1,228 (141) 
 Effluent (mg·L−1113 (40) 63 (26) 74 (27) 65 (27) 67 (34) 56 (20) 
 REd (%) 89.3 (3.4) 93.5 (3.0) 93.4 (3.0) 94.4 (2.2) 94.0 (3.0) 95.4 (1.8) 
 Influent (mg·L−1115 (11) 126 (12) 122 (16) 147 (6) 155 (12) 151 (8) 
 Effluent (mg·L−152 (12) 57 (16) 53 (11) 55 (14) 62 (17) 55 (4) 
 RE (%) 54.9 (8.7) 54.1 (12.5) 56.4 (9.6) 63.0 (8.8) 60.1 (9.9) 63.8 (3.7) 
S2− Effluent (mg·L−114.9 (3.0) 3.6 (2.0) 2.9 (1.4) 0.5 (0.7) 23.5 (3.9) 
 Influent (mg·L−163 (3) 64 (9) 72 (14) 59 (7) 60 (3) 81 (9) 
 Effluent (mg·L−159 (4) 61 (11) 64 (13) 53 (7) 55 (3) 76 (7) 
 RE (%) 6.4 (3.7) 7.1 (4.9) 11.6 (5.3) 9.3 (8.1) 8.5 (4.7) 7.0 (4.9) 
 Influent (mg·L−1– 18 (7) 10 (10) 36 (22) 9 (8) – 
 Effluent (mg·L−1– – 
 RE (%) – 100 (0) 100 (0) 100 (0) 100 (0) – 
 Influent (mg·L−1– 84 (11) 174 (12) 244 (44) 42 (12) – 
 Effluent (mg·L−1– 13 (9) 1 (4) 1 (3) – 
 RE (%) – 97.4 (7.1) 99.2 (2.5) 99.4 (1.2) 100 (0) – 
H2Biogas (%) 0.2 (0.0) 0.2 (0.2) 0.3 (0.1) 0.1 (0.1) 0.1 (0.0) 0.3 (0.1) 
CH4 Biogas (%) 83.3 (3.8) 80.1 (6.4) 70.9 (4.0) 65.7 (5.1) 79.5 (5.6) 90.3 (1.1) 
 Biogas (L·g )e 0.32 (0.06) 0.29 (0.08) 0.26 (0.05) 0.26 (0.05) 0.30 (0.05) 0.26 (0.03) 
Air Biogas (%) 5.6 (4.3) 11.3 (7.0) 25.3 (4.4) 31.2 (5.1) 15.2 (4.9) 2.8 (0.6) 
PeriodIIIIIIIVVVI
Duration (days) 116 147 42 51 63 42 
Added nitratea (mg·L−1– 100 200 300 50 – 
N/S molar ratiob – 1.4 3.9 4.4 0.7 – 
CODc Influent (mg·L−11,051 (112) 918 (101) 1,135 (190) 1,139 (91) 1,119 (157) 1,228 (141) 
 Effluent (mg·L−1113 (40) 63 (26) 74 (27) 65 (27) 67 (34) 56 (20) 
 REd (%) 89.3 (3.4) 93.5 (3.0) 93.4 (3.0) 94.4 (2.2) 94.0 (3.0) 95.4 (1.8) 
 Influent (mg·L−1115 (11) 126 (12) 122 (16) 147 (6) 155 (12) 151 (8) 
 Effluent (mg·L−152 (12) 57 (16) 53 (11) 55 (14) 62 (17) 55 (4) 
 RE (%) 54.9 (8.7) 54.1 (12.5) 56.4 (9.6) 63.0 (8.8) 60.1 (9.9) 63.8 (3.7) 
S2− Effluent (mg·L−114.9 (3.0) 3.6 (2.0) 2.9 (1.4) 0.5 (0.7) 23.5 (3.9) 
 Influent (mg·L−163 (3) 64 (9) 72 (14) 59 (7) 60 (3) 81 (9) 
 Effluent (mg·L−159 (4) 61 (11) 64 (13) 53 (7) 55 (3) 76 (7) 
 RE (%) 6.4 (3.7) 7.1 (4.9) 11.6 (5.3) 9.3 (8.1) 8.5 (4.7) 7.0 (4.9) 
 Influent (mg·L−1– 18 (7) 10 (10) 36 (22) 9 (8) – 
 Effluent (mg·L−1– – 
 RE (%) – 100 (0) 100 (0) 100 (0) 100 (0) – 
 Influent (mg·L−1– 84 (11) 174 (12) 244 (44) 42 (12) – 
 Effluent (mg·L−1– 13 (9) 1 (4) 1 (3) – 
 RE (%) – 97.4 (7.1) 99.2 (2.5) 99.4 (1.2) 100 (0) – 
H2Biogas (%) 0.2 (0.0) 0.2 (0.2) 0.3 (0.1) 0.1 (0.1) 0.1 (0.0) 0.3 (0.1) 
CH4 Biogas (%) 83.3 (3.8) 80.1 (6.4) 70.9 (4.0) 65.7 (5.1) 79.5 (5.6) 90.3 (1.1) 
 Biogas (L·g )e 0.32 (0.06) 0.29 (0.08) 0.26 (0.05) 0.26 (0.05) 0.30 (0.05) 0.26 (0.03) 
Air Biogas (%) 5.6 (4.3) 11.3 (7.0) 25.3 (4.4) 31.2 (5.1) 15.2 (4.9) 2.8 (0.6) 

The standard deviation is shown in parentheses.

aNitrate concentration added to the wastewater. A small fraction of nitrate was reduced to nitrite in the feeding tank.

bRatio between the measured nitrate (as N) and the expected sulfide (as S) produced from the sulfate reduction.

cChemical oxygen demand.

dRemoval efficiency.

eLiter per gram of removed chemical oxygen demand.

Analytical methods

COD, dissolved sulfide, and ammonium were determined according to APHA (2012). Sulfate, nitrite, and nitrate were determined by a Dionex™ ICS-1100 ion chromatograph equipped with a Dionex™ IonPac™ AG23 pre-column (2 × 50 mm), a Dionex™ IonPac™ AS23 column (2 × 250 mm), and a Dionex™ AERS™ 500 suppressor (2 mm) (Thermo Scientific, USA). 5 μL of the filtered sample (0.45 μm) were injected and then eluted by an aqueous solution containing 4.5 mM sodium carbonate and 0.8 mM sodium bicarbonate at a constant flow of 0.25 mL·min−1. The oven temperature was 30 °C, the applied current was 7 mA, and the running time was 30 min. The levels of CH4, CO2, and air (O2 + N2) in the biogas were determined by gas chromatography with thermal conductivity detection (GC-TCD 17A, Shimadzu Corporation, Japan) as described elsewhere (Firmino et al. 2015). The levels of H2S and NH3 in the biogas were determined by a Dräger X-am® 5600 gas meter (Drägerwerk AG & Co. KGaA, Germany).

Statistical methods

The Mann-Whitney Rank Sum non-parametric test was used to compare, at a 5% significance level, the experimental data obtained throughout the different periods.

In period I, when the reactor was fed with nitrate-free wastewater, a high COD removal efficiency (RE) was achieved (89%), resulting in a methane production of 0.32 liter per gram of removed COD (Table 1). The sulfate RE was 55%, producing 134 mg S·d−1 of dissolved sulfide and 7 mg S·d−1 of H2S in the biogas, accounting for 38.8% and 2.1% of the inlet sulfur load, respectively (Figure 1).

Figure 1

Sulfur mass balance. Sulfate (▪), dissolved sulfide (▪), and H2S(g) (▪).

Figure 1

Sulfur mass balance. Sulfate (▪), dissolved sulfide (▪), and H2S(g) (▪).

Close modal

In period II, with the addition of 100 mg ·L−1, there was a significant increase in the COD RE (p < 0.001) compared to period I (Table 1). In fact, nitrate can improve the removal of organic matter due to the activity of heterotrophic denitrifying microorganisms (Show et al. 2013). The sulfate RE (p = 0.778) and effluent concentration (p = 0.238) remained similar to those of the previous period (Table 1). Therefore, apparently, the addition of nitrate did not hinder sulfate reduction. On the other hand, the concentration of dissolved sulfide was 73% lower than that of period I (p < 0.001) and 83% lower than the expected concentration (theoretical concentration from reduced sulfate, 23 mg S2−·L−1). Most likely, the biogenic sulfide (generated from sulfate reduction) was partially oxidized to elemental sulfur by autotrophic denitrifying bacteria, which use sulfide as an electron donor to reduce nitrate to nitrogen gas (Equation (1)) (Di Capua et al. 2019).

Regarding H2S(g), there was no significant difference between periods I and II (p = 0.060) (Table 1). However, due to the equilibrium between the dissolved and gaseous fractions of sulfide (Henry's law), a decrease in the H2S(g) load was expected in period II, as the dissolved sulfide was considerably removed. Therefore, probably, the measurement method used in the present study was not sufficiently accurate to detect such small variations in the levels of H2S in the biogas. Regarding the sulfur mass balance, the dissolved sulfide accounted for only 8.6% of the inlet sulfur load, and the gaseous fraction, 1.6%. Since the effluent sulfate remained, representing 45.2% of the inlet sulfur load, a large gap in the mass balance was found (Figure 1), most likely due to elemental sulfur formation, as reported in previous studies (Cardoso et al. 2006; Chen et al. 2008; Moraes et al. 2012).

The nitrate RE was quite high (97%) in period II. Consequently, an increase in the nitrogen fraction in the biogas (air) was observed in relation to period I (Table 1) because of the denitrification process. In addition, as there was no nitrite accumulation in the effluent (Table 1), it is likely that the removed nitrate was completely reduced to nitrogen gas (complete denitrification). It is worth mentioning that the oxidation of sulfide to elemental sulfur consumed only 14.5 mg ·L−1. Consequently, the remaining nitrate and nitrite were reduced to nitrogen gas by heterotrophic denitrification. However, this pathway accounted for only 5.4% of the removed COD.

It is important to mention that the available nitrate (N/S = 1.4) was close to the stoichiometric demand for the complete oxidation of sulfide to sulfate (N/S = 1.6) (Equation (2)). Nonetheless, there was no clear evidence of such a reaction, since the effluent sulfate concentration remained similar to that of period I (p = 0.238) (Table 1). This may have occurred due to strong competition between the autotrophic and heterotrophic denitrification pathways, caused by the high availability of organic matter. Chen et al. (2008), using an expanded granular bed reactor (HRT of ∼12 h) to treat synthetic wastewater containing 200 mg S2−·L−1, 465 mg ·L−1, and 200–480 mg COD·L−1 (acetate), found that, with higher concentrations of carbon source (480 mg COD·L−1), the heterotrophic denitrifying bacteria predominated over the autotrophic ones, compromising the conversion of sulfide into elemental sulfur. In contrast, in the present experiment, no inhibitory effect was identified on autotrophic denitrification, caused by the high availability of ethanol (∼900 mg COD·L−1).

In periods III and IV, when much higher nitrate concentrations were added (200 and 300 mg ·L−1, respectively), the removal of sulfide from gaseous and liquid phases showed a similar behavior to that of period II, although a slightly better RE of dissolved sulfide was found in period IV (1.1% of the inlet sulfur load) (Figure 1). Nitrate was almost totally consumed, and, unexpectedly, no evidence of either inhibition of sulfidogenesis or reoxidation of sulfide to sulfate was found again, since the effluent sulfate concentrations remained similar (p = 0.533) (Table 1). Beristain-Cardoso et al. (2008), operating an inverse fluidized bed reactor (HRT of 25 h) fed with synthetic wastewater containing approximately 73 mg S2−·L−1 and 1,050 mg ·L−1, observed that, when the acetate concentration was decreased from 872 to 737 mg COD·L−1, sulfide ceased to be partially oxidized to elemental sulfur (72.5% of the effluent sulfur load) and was completely oxidized to sulfate. According to the authors, the smaller amount of the organic electron donor favored the complete oxidation of sulfide (Equation (2)), as it increased the availability of nitrate for the autotrophic pathway. Therefore, in the present study, the high ethanol concentration may have prevented the conversion of sulfide into sulfate even in the presence of excess nitrate. Accordingly, only 14.8 and 21.1 mg ·L−1 were reduced autotrophically in periods III (N/S = 3.9) and IV (N/S = 4.4), respectively. In addition, it is worth mentioning that, although heterotrophic denitrification consumed from 10% to 15% of the removed COD in these periods, it did not compromise the methane production (p = 0.264) (Table 1).

In period V, with a lower nitrate concentration (50 mg ·L−1), the COD RE (p = 0.925), sulfate RE (p = 0.379), and methane production (p = 0.051) remained similar to those of period IV (Table 1). Despite the reduced availability of nitrate (N/S = 0.7), this electron acceptor was still in excess (almost 2 times the stoichiometric demand for the oxidation of sulfide to elemental sulfur), which ensured the complete removal of dissolved sulfide (Table 1). Concerning the H2S(g) load (∼3 mg·d−1), it was the lowest value obtained during the entire experiment (only 0.7% of the inlet sulfur load) (Figure 1). Interestingly, even with a lower nitrate concentration, sulfide removal by autotrophic denitrification was more efficient than with higher nitrate concentrations (periods II to IV). Due to the aforementioned competition for nitrate between the autotrophic and heterotrophic pathways, sulfide removal was expected to be impaired. Therefore, the continuous exposure of the microbiota to increasing nitrate concentrations for 240 days (periods II–IV) may have favored the growth of autotrophic denitrifying species; that is, an enrichment of the microbial community, which made the process more efficient. However, it is important to mention that molecular biology techniques are needed to confirm this hypothesis. In this period, heterotrophic denitrification accounted for only 1.6% of COD removal.

According to Show et al. (2013), while sulfide is partially oxidized to elemental sulfur, nitrate is partially reduced to nitrite by autotrophic denitrifiers, which is subsequently reduced to nitrogen gas by heterotrophic denitrifiers. Di Capua et al. (2016) also observed the same behavior in a mixed culture of autotrophic and heterotrophic denitrifiers using elemental sulfur as an electron donor. Thus, such a hypothesis may justify the occurrence of sulfide oxidation even in the presence of high concentrations of organic matter. However, further studies should be carried out to confirm whether autotrophic denitrification via nitrate is incomplete and autotrophic denitrification via nitrite is inhibited by organic matter. It is worth mentioning that, in periods II to V, a small fraction of nitrate was reduced to nitrite in the feeding tank, even under refrigeration (5 °C). However, this did not hinder the process, as nitrate was always in excess during the entire experiment. In addition, nitrite can be used in both autotrophic and heterotrophic denitrifying pathways, although the literature reports that it is preferably used by heterotrophic denitrifiers (Show et al. 2013).

In period VI, to reinforce the role of nitrate on sulfide removal, its supplementation was ceased. No significant changes were observed in the COD RE (p = 0.300) and methane production (p = 0.080) compared to the previous period (Table 1). Thus, methanogenesis was not inhibited by denitrification throughout the experiment. Although the sulfate RE also remained similar to that of period V (p = 0.462), the dissolved sulfide increased noticeably (Table 1). Actually, it was 1.6 time greater than that observed in period I (also without nitrate) (p < 0.001), possibly due to the higher sulfate concentration in the influent (p < 0.001) (Table 1). Additionally, as part of the generated elemental sulfur tends to accumulate inside the system (sludge blanket and walls of the reactor), when the addition of nitrate is interrupted, elemental sulfur is also used as an electron acceptor by the SRB, increasing the sulfide production (Auguet et al. 2015). Therefore, the addition of nitrate played a key role in the removal of dissolved sulfide, although its effect on H2S(g) was negligible. Nonetheless, this gaseous fraction represented approximately only 5% of the generated sulfide in the anaerobic periods (I and VI). Thus, most of this pollutant can be properly removed from anaerobic systems, preventing likely environmental impacts by the discharge of sulfide-containing wastewater.

Finally, from an engineering perspective, it is important to remember that anaerobic reactors are not able to remove nutrients, particularly nitrogen. Thus, to overcome this limitation as well as to remove some residual organic matter, they are usually associated with aerobic post-treatment systems (Chernicharo et al. 2015). In such a sequential anaerobic-aerobic configuration, ammonium from the anaerobic reactor is oxidized to nitrate in the aerobic system. Then, part of the nitrified effluent is recirculated back to the anaerobic reactor to remove nitrate by denitrification (Kassab et al. 2010). Therefore, the nitrified effluent may also be used as a nitrate source for sulfide removal by autotrophic denitrification, supplying or at least decreasing the demand for an external nitrate source (nitrate salts) to be added to the anaerobic reactor.

Autotrophic denitrification, stimulated by the addition of nitrate, was demonstrated to be a very effective approach for removal of dissolved sulfide even in the presence of a high concentration of organic matter. However, it had a minor effect on H2S(g).

Sulfide remained partially oxidized to elemental sulfur even with excess nitrate. Therefore, the competition for this electron acceptor between the autotrophic and heterotrophic denitrification pathways may have prevented the conversion of the generated sulfide into sulfate again.

No evidence of inhibition of methanogenesis and sulfidogenesis was found during nitrate supplementation.

The authors thank the following Brazilian institutions: Conselho Nacional de Desenvolvimento Científico e Tecnológico; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior; Fundação de Amparo à Pesquisa do Estado de Minas Gerais; and Instituto Nacional de Ciência e Tecnologia em Estações Sustentáveis de Tratamento de Esgoto.

All relevant data are included in the paper or its Supplementary Information.

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