Two anaerobic fixed-structured bed reactors were fed with synthetic wastewater simulating the soluble fraction of sugarcane vinasse to evaluate the interference of sulfidogenesis on methanogenesis. The reactors running in parallel were subjected to the same operating conditions. The influent organic matter concentration (in term of chemical oxygen demand (COD)) remained close to 4,000 mgCOD L−1 and the hydraulic retention time was 24 hours. One reactor, the methanogenic (control reactor), received sulfate only to provide the sulfur required as a nutrient to the methanogenic biomass. The other one, the sulfidogenic/methanogenic reactor (SMR), received sulfate concentration corresponding to COD/sulfate ratios of 4, 5 and 3. In the last phase, the COD removal efficiencies were higher than 96% in both reactors and the SMR achieved 97% of sulfate removal efficiency (COD/sulfate ratio of 3 and influent sulfate concentration close to 1,300 mgSO42− L−1). Both reactors also had similar methane yields in this phase, close to 350 mLCH4 gCODremoved−1 at standard temperature and pressure. These results indicated no significant inhibition of methanogenic activity under the sulfidogenic conditions assessed.

INTRODUCTION

The energy recovery potential from sugarcane vinasse in the form of methane, before fertirrigation, has been strongly promoted in Brazil (Salomon & Lora 2009). One of the difficulties in implementing the anaerobic digestion process in this class of wastes is the sulfidogenesis interference as an alternative route to organic matter degradation. In this route, the electron flow is diverted from methane production to sulfide production by the sulfate-reducing bacteria (SRB) (Lens et al. 1998).

In fact, until recently, the application of anaerobic technology for sulfate-rich wastewater treatment was considered undesirable due to the hydrogen sulfide (H2S) production. H2S is responsible for several problems, for instance toxicity, corrosion, malodor, decrease in effluent and biogas quality, and lower methane production (Hulshoff Pol et al. 1998). Currently, on account of the increasing knowledge about the biochemistry and microbiology of anaerobic processes via the sulfidogenic pathway, this technology is now a viable option for treating organic wastewater containing sulfate. However, adequate strategies must be applied to integrate the sulfate reduction and methanogenic processes (Lens et al. 2002).

The chemical oxygen demand (COD) to sulfate ratio is often reported as directly affecting the main route of organic matter degradation in the presence of sulfate (McCartney & Oleszkiewicz 1993). It is known that COD/sulfate ratio of 0.67 is the theoretical limit to achieve the complete removal of all organic matter by the sulfate-reduction process. For lower COD/sulfate ratios, more organic substrate is needed to achieve complete sulfate removal. In systems with COD/sulfate ratios higher than 0.67, the removal of all organic matter will only be achieved by associating the sulfidogenic with the methanogenic process (Lens et al. 1998).

Sulfate reduction coupled to organic matter oxidation is independent of the hydrogen partial pressure (Lens et al. 1998). Thus, the sulfidogenic systems should be less sensitive to organic overloads than the methanogenic systems, which require a balance between the acetogenic and methanogenic processes (Hulshoff Pol et al. 1998). However, the disadvantage of sulfidogenic reactors is their inefficient acetate removal (Omil et al. 1996), due to the inefficient capacity of the SRB to complete oxidation of this substrate (Cao et al. 2012).

Even under limiting sulfate conditions (COD/sulfate > 0.67) the SRB can partially oxidize volatile acids produced during acidogenesis, producing acetate, which may be used as a substrate for the acetoclastic methanogenic archaea (MA) (Damianovic & Foresti 2009). Thus, the bacterial consortium in this environment can lead to enhanced organic matter removal and methane production.

This work evaluated the interference of sulfidogenesis on methanogenesis and COD removal in a structured fixed-bed reactor treating synthetic wastewater with a composition similar to the soluble fraction of a sugarcane vinasse.

MATERIAL AND METHODS

Experimental configuration

Two anaerobic fixed-structured bed and upflow reactors (Camiloti et al. 2013) were operated at 24 hours of hydraulic retention time with a working volume of 1.65 L. Both reactors were kept at controlled temperature of 25 °C during the entire experimental period (213 days). The material support was laid out in seven vertical strips of prismatic polyurethane foam, 500 mm in length. Figure 1 shows a schematic illustration of the fixed-structured bed reactor.

Figure 1

(a) Anaerobic fixed-structured bed reactor (dimensions in mm). 1 influent inlet, 2 peristaltic pump, 3 mixture zone, 4 purge, 5 biogas outlet, 6 effluent outlet, 7 immobilization matrix. (b) Cross-sectional view of the bed.

Figure 1

(a) Anaerobic fixed-structured bed reactor (dimensions in mm). 1 influent inlet, 2 peristaltic pump, 3 mixture zone, 4 purge, 5 biogas outlet, 6 effluent outlet, 7 immobilization matrix. (b) Cross-sectional view of the bed.

The support material was inoculated with biomass from an upflow anaerobic sludge blanket reactor treating poultry slaughterhouse wastewater following the protocol described by Zaiat et al. (1994). After inoculation, the reactors were kept under effluent recirculation for 5 consecutive days.

Synthetic wastewater

The synthetic wastewater used was based on the soluble fraction of the sugarcane vinasse composition presented by Rocha (2012). The synthetic wastewater was diluted to obtain 4,000 mgCOD L−1. Table 1 shows the characteristics of the synthetic feed.

Table 1

Synthetic wastewater characterization (substance-based concentration)

Component Concentrations (mg L−1
CODSoluble 4,000 
Sucrose (C12H22O112,700 
Ethanol (CH3CH2OH) 380 
Phenol (C6H5OH) 100 
NH4Cl 256.35 
KCl 742.30 
KH2PO4 84.36 
CaCl2.2H291.70 
NaCl 129.50 
MgCl2.6H2219.60 
FeCl3.6H26.12 
MnCl2.4H21.31 
CuCl2.2H20.12 
ZnCl2 0.10 
NiCl2.6H20.10 
PbCl2 0.04 
CdCl2.H20.01 
LiCl 0.001 
Nitrilotriacetic acid (C6H9NO61.07 
Component Concentrations (mg L−1
CODSoluble 4,000 
Sucrose (C12H22O112,700 
Ethanol (CH3CH2OH) 380 
Phenol (C6H5OH) 100 
NH4Cl 256.35 
KCl 742.30 
KH2PO4 84.36 
CaCl2.2H291.70 
NaCl 129.50 
MgCl2.6H2219.60 
FeCl3.6H26.12 
MnCl2.4H21.31 
CuCl2.2H20.12 
ZnCl2 0.10 
NiCl2.6H20.10 
PbCl2 0.04 
CdCl2.H20.01 
LiCl 0.001 
Nitrilotriacetic acid (C6H9NO61.07 

The control reactor (CR) received sulfate (25 mg SO42− L−1) only to provide the anaerobic biomass nutritional requirements, and the sulfidogenic/methanogenic reactor (SMR) was operated with COD/sulfate ratios of 4, 5 and 3. Since the sulfate concentration of vinasse varies during the harvest season (Barrera et al. 2014), these values were chosen to simulate previously reported concentrations. The influent received 1.4 mgNaHCO3 mgCOD−1 during phases I to III to maintain the pH at a desirable range. In phase IV the sodium bicarbonate dosage was decreased to 0.7 mgNaHCO3 mgCOD−1.

Analytical

The determinations of COD, alkalinity, total sulfide and pH were carried out in accordance with Standard Methods (APHA 2005). In order to remove the aqueous sulfide prior to the COD analysis, excess zinc sulfate (ZnSO4) was added to the samples. Next, the solution was centrifuged (5 minutes, 5,000 rpm) and the supernatant was tested for soluble COD. Sulfate was determined by ion chromatography (Dionex ICS 5000) equipped with an anion-exchange column (IonPac® AS25-HC) and a conductivity detector. The organic acids were analyzed by gas chromatography (GC-2010, Shimadzu) with an HP-INNOWax capillary column and a flame ionization detector. The biogas was bubbled through a sodium hydroxide solution (15%) to retain H2S and CO2, and the methane produced was measured by the liquid displacement method (Aquino et al. 2007).

Methane yield

To evaluate the interference of sulfidogenesis on methane production the methane yields (Equation (1)) obtained in both systems were calculated. This included only the amounts of organic matter removed exclusively by the methanogenic pathway, disregarding the COD used in the sulfate reduction process (Giménez et al. 2012). The methane yields were determined at STP (standard temperature and pressure – 0 °C and 1 atm) with the maximum theoretical yield of 350 mLCH4 gCODremoved−1. 
formula
1
where ηCH4 is the methane yield (mLCH4 gCODremoved−1); fCH4 is the methane flow-rate (mL day−1); and CODCH4 is the amount of COD removed exclusively by the methanogenic route (g day−1). These values were calculated considering that to reduce 1 g of SO42− SRB oxidize 0.67 g of COD (Lens et al. 1998), according to Equation (2). 
formula
2
 
formula
3
where CODremoved is the total amount of COD removed in the SMR reactor (g day−1); CODSO4 is the amount of COD converted by sulfate reduction (g day−1); and SO4 removed is the amount of sulfate removed (g day−1).
To calculate the methane yields, the dissolved methane concentration in the effluent was taken into account. The dissolved methane was estimated according to Henry's law (Aquino et al. 2007): 
formula
4
where XCH4 is the dissolved methane concentration (g L−1); MCH4 is the molar mass of methane (16 g mol−1); PCH4 is the methane partial pressure in the biogas (atm); and KH is Henry's law constants (at 25 °C, KH = 1.34 × 10−3 mol L−1 atm−1).

Statistical methods

The experimental data relating to the methane yields obtained in both reactors were subjected to the Lilliefors statistical test to verify the data normality. Since the test indicated a nonparametric data distribution, they were compared using the Kruskal–Wallis test. At statistical significance level (p) greater than 0.05, no significant differences were observed between the methane yields from both reactors. The statistical analyses were carried out using BioEstat® software.

RESULTS AND DISCUSSION

COD removal

The reactors were initially operated for 80 days with increasing concentrations of organic matter (ranging from 800 to 2,000 mgCOD L−1). During this starting phase, the SMR reactor was operated with COD/sulfate ratio of 3 for the sulfidogenic processes. The COD concentration was then kept constant (close to 4,000 mg L−1) due to a limitation in the biogas measurement apparatus, after which the present study was initiated.

Four different operational phases were tested. Pseudo-steady state conditions indicated the end of the phases and were characterized by a constant organic matter removal efficiency (variations were lower than 10%). The applied operating conditions and the results are summarized in Table 2.

Table 2

Operational conditions, efficiencies of COD and sulfate removal, total dissolved sulfide (TDS) and free sulfide (H2S) concentrations, methane production and the COD converted by methanogenic (CODCH4) or sulfidogenic routes (CODSO4) in each phase (N ≥ 10)

    Phases
 
 Parameters II III IV 
CR COD influent (mg L−13,870 ± 280 4,160 ± 120 4,220 ± 230 4,020 ± 190 
COD removal (%) 94.6 ± 1.3 95.8 ± 1.5 96.1 ± 1.5 97.1 ± 1.0 
CODCH4 (g day−15.8 ± 0.4 6.3 ± 0.4 6.5 ± 0.5 6.4 ± 1.0 
CH4 flow-rate (mL day−11,340 ± 240 2,013 ± 180 2,100 ± 160 2,000 ± 220 
SMR COD influent (mg L−13,910 ± 205 4,200 ± 190 4,180 ± 260 3,980 ± 200 
SO42− influent (mgSO42− L−11,050 ± 70 875 ± 90 1,350 ± 60 1,380 ± 90 
COD/SO42− ratio 3.9 ± 0.2 4.9 ± 0.4 3.1 ± 0.2 2.9 ± 0.3 
COD removal (%) 83.2 ± 4.6 89.1 ± 2.1 93.8 ± 1.0 96.1 ± 1.0 
SO42− removal (%) 85.2 ± 4.6 92.6 ± 4.6 96.5 ± 2.5 97.3 ± 1.4 
TDS (mg L−1195 ± 15 190 ± 7 320 ± 25 290 ± 20 
Free sulfide (mgH2S L−134 ± 8 30 ± 8 50 ± 16 48 ± 17 
CODCH4 (g day−14.3 ± 0.4 5.0 ± 0.3 4.8 ± 0.6 4.6 ± 0.8 
CODSO4 (g day−11.0 ± 0.1 0.9 ± 0.1 1.4 ± 0.1 1.4 ± 0.2 
CH4 flow-rate (mL day−1930 ± 100 1,620 ± 100 1,510 ± 100 1,560 ± 210 
    Phases
 
 Parameters II III IV 
CR COD influent (mg L−13,870 ± 280 4,160 ± 120 4,220 ± 230 4,020 ± 190 
COD removal (%) 94.6 ± 1.3 95.8 ± 1.5 96.1 ± 1.5 97.1 ± 1.0 
CODCH4 (g day−15.8 ± 0.4 6.3 ± 0.4 6.5 ± 0.5 6.4 ± 1.0 
CH4 flow-rate (mL day−11,340 ± 240 2,013 ± 180 2,100 ± 160 2,000 ± 220 
SMR COD influent (mg L−13,910 ± 205 4,200 ± 190 4,180 ± 260 3,980 ± 200 
SO42− influent (mgSO42− L−11,050 ± 70 875 ± 90 1,350 ± 60 1,380 ± 90 
COD/SO42− ratio 3.9 ± 0.2 4.9 ± 0.4 3.1 ± 0.2 2.9 ± 0.3 
COD removal (%) 83.2 ± 4.6 89.1 ± 2.1 93.8 ± 1.0 96.1 ± 1.0 
SO42− removal (%) 85.2 ± 4.6 92.6 ± 4.6 96.5 ± 2.5 97.3 ± 1.4 
TDS (mg L−1195 ± 15 190 ± 7 320 ± 25 290 ± 20 
Free sulfide (mgH2S L−134 ± 8 30 ± 8 50 ± 16 48 ± 17 
CODCH4 (g day−14.3 ± 0.4 5.0 ± 0.3 4.8 ± 0.6 4.6 ± 0.8 
CODSO4 (g day−11.0 ± 0.1 0.9 ± 0.1 1.4 ± 0.1 1.4 ± 0.2 
CH4 flow-rate (mL day−1930 ± 100 1,620 ± 100 1,510 ± 100 1,560 ± 210 

The pH feed values during the entire operational time were 8.0 ± 0.2. The effluent pH of CR and SMR reactors were 7.6 ± 0.2 and 7.7 ± 0.2, respectively. The volatile suspended solids (VSS) were 140 ± 23 mgVSS L−1 in CR reactor effluent and 110 ± 46 mgVSS L−1 in SMR reactor effluent.

During the preliminary phase, the COD removal efficiencies in the CR and SMR reactors were close to 94% and 89%, respectively. No significant organic acid accumulation was detected in both reactors (data not shown). After the organic loading increase (phase I), the SMR reactor presented lower COD removal efficiencies (Figure 2(a)) and higher concentrations of acetate and propionate in its effluent. These occurrences were not observed in the CR reactor (Figure 2(b)).

Figure 2

(a) Boxplot analysis of COD removal efficiency in both reactors. (b) Averages of volatile organic acids in both reactor effluents with standard deviations.

Figure 2

(a) Boxplot analysis of COD removal efficiency in both reactors. (b) Averages of volatile organic acids in both reactor effluents with standard deviations.

The acetate accumulation in sulfidogenic reactors has been attributed to the higher acetate production via the incomplete oxidation of organic matter by the SRB (Nagpal et al. 2000; Gallegos-Garcia et al. 2009; Bertolino et al. 2012). Furthermore, the negligible performance of SRB acetate oxidizers in anaerobic reactors has been described (Lens et al. 2002; Cao et al. 2012).

The low acetate removal in the SMR reactor can be explained by the inhibitory effects of the hydrogen sulfide on the methanogenic activity. The critical values found in the literature for anaerobic fixed-film reactors were in the level of 400 mgTDS L−1 and 125 mgH2S L−1 (Maillacheruvu et al. 1993). However, in the SMR reactor the total dissolved sulfide (TDS) and free sulfide (H2S) concentrations remained below these values (Table 2). In fact, the acetate consumption is commonly identified as a limiting step in the anaerobic process due to the low growth rates of acetoclastic MA (Aquino & Chernicharo 2005), mainly under sulfidogenic conditions (Visser et al. 1996). This may be due to the higher sensitivity of acetoclastic MA to sulfide toxicity (O’Flaherty & Colleran 1998; Yamaguchi et al. 1999). Then, the acetoclastic MA subjected to the SMR reactor conditions may have required more adaptation and growth time when compared with the CR reactor performance.

In sulfidogenic systems SRB on for consume the propionate more efficiently than do other microorganisms (O’Flaherty & Colleran 1998; Barrera et al. 2014). However, the SMR reactor effluent presented higher propionate concentrations in phase I (Figure 2(b)). It is possible that the SRB populations were not yet sufficient (or fully active) in the SMR reactor to maintain the fermentation products under control (Bertolino et al. 2012) after increasing the organic loading. It should also be noted that during this phase the COD/sulfate ratio in the SMR reactor was kept at 4 (higher than in the preliminary phase). Thereafter, the propionate-degrading SRB are not very effective competitors for the available sulfate (Visser et al. 1993). Thus, increasing the COD/sulfate ratio could limit the performance of SRB in the propionate removal process.

The application of the COD/sulfate ratio of 5 in phase II, maintaining the COD influent concentration close to 4,000 mgL−1, was advantageous to the methanogenic contribution in terms of organic matter removal (Figure 3). This resulted in increased COD removal efficiencies (Figure 2(a)) and increased methane production (Table 2) in the SMR reactor.

Figure 3

Electron flow distributed between methanogenesis and sulfidogenesis in the SMR reactor.

Figure 3

Electron flow distributed between methanogenesis and sulfidogenesis in the SMR reactor.

In phases III and IV the COD/sulfate ratio of the SMR reactor was adjusted to 3 by increasing the influent sulfate concentration (875 to 1,350 mgSO42− L−1). The performance of the SMR reactor, according to COD removal, was similar to the CR reactor. The acetate concentration decreased (Figure 2(b)), the methane flow-rate increased (Table 2) and, immediately after the influent sulfate increase, the propionate was readily consumed. The sulfate removal efficiencies also increased from 93% (phase II) to 97% (phases III and IV). These results suggest the participation of SRB in the propionate metabolism in the SMR reactor, indicating the successful acclimation of acetoclastic MA under the sulfidogenic conditions applied (Isa et al. 1986).

Conversely, COD/sulfate ratio of 3 is higher than the theoretical ratios to obtain the complete and incomplete oxidation of organic matter via the sulfidogenic route (Damianovic & Foresti 2007). In fact, at COD/sulfate ratios higher than 2.8, the methane-producing organisms begin to predominate over sulfate reducers (Choi & Rim 1991). This condition makes possible a positive association between methanogenic and sulfidogenic processes, resulting in increased COD and sulfate removal efficiencies (Vilela et al. 2014).

In the last step (phase IV), the sodium bicarbonate dosage in the influent was cut in half (4,000 to 2,000 mgHCO3− L−1). The alkalinity availability did not influence the COD removal efficiencies and methane production (Table 2). In phases I to III the influent pH applied to both reactors was close to 8.0. In the same period the effluent pH from the two reactors was close to 7.7. In phase IV, while the SMR reactor kept the same pH value, the effluent pH in the CR reactor decreased to 7.4. This result showed the robustness of the two reactors, particularly the SMR reactor, since some organic matter oxidation reactions by SRB metabolism generate alkalinity (Kaksonen & Puhakka 2007).

Biogas production

As expected, the SMR reactor presented lower methane flow-rates than the CR reactor in all phases (Figure 4(a)). This pattern does not mean that the methanogenic activity was inhibited by sulfidogenic conditions, but that an amount of COD was removed by the sulfate-reduction route, generating sulfide instead of methane (Table 2). In fact, the COD degraded by the methanogenic pathway was approximately 80% of total COD degraded in the SMR reactor (Figure 3). Thus, this reactor tends to present a methane production 20% lower than the CR reactor.

Figure 4

Boxplot analysis of (a) methane flow-rate and (b) methane yield per COD removed, considering only the electron flow by methanogenic route.

Figure 4

Boxplot analysis of (a) methane flow-rate and (b) methane yield per COD removed, considering only the electron flow by methanogenic route.

The two reactors showed close methane yield values (methane yield was defined as the volume of methane produced per amount of COD removed exclusively by methanogenic route – Equation (1)). On some days of phases II, III and IV the SMR reactor exceed the methane yield obtained in the CR reactor (Figure 4(b)). These results demonstrate the adaptation potential of the acetoclastic MA, evidencing that under the sulfidogenic conditions applied to the SMR reactor there is no inhibition of these organisms.

Michaud et al. (2002) reported that, during the start-up period and after organic overloads or perturbations in anaerobic fixed-film reactors, the methane yields achieved in these systems could be lower than the theoretical values expected. This is because methane-producing microorganisms use carbon for their anabolism (fixation, cell growth and biofilm maturation). Outside these periods, carbon is mainly converted into biogas and the methane yield should be close to the theoretical value. In fact, during phase I, both reactors showed lower methane yields than the theoretical value (Figure 4(b)). This behavior suggests that under the new conditions imposed (wastewater, COD composition and concentration, and support material) the biofilm was still in the adaptation period. In turn, in phases II to IV, both reactors achieved methane yields close to the theoretical value (350 mL gCODremoved−1 at STP). This result would not be expected if the MA were under stress or inhibited in the SMR reactor.

The Kruskal–Wallis statistical analysis also indicated there were no significant (p > 0.05) differences between both reactors regarding the methane yields (methane produced per COD removed via the methanogenic route) in all phases. This result confirmed there was no significant inhibition of the methanogenic populations in the SMR reactor.

The dissolved methane concentrations estimated for the effluent of the two reactors remained close to 15 mgCH4 L−1, which corresponds to about 15% of the total methane produced. The literature has generally reported that the rates of dissolved methane lost in the effluent are close to 40% (Giménez et al. 2012). However, this value was found in pilot- and full-scale plants. In the present study, the reactors used are smaller (bench-scale) which would allow more effective methane release, mainly due to the lower water column (700 mm). The structured arrangement of the bed, keeping a free cross-sectional area (Figure 1), may also have favored the methane emission. In fact, this configuration was developed to avoid the accumulation of biomass in the bed and the clogging and channeling effects (Mockaitis et al. 2014), which could block the biogas release.

CONCLUSIONS

It appears that the experimental time was crucial to fully establish the methanogenic and sulfidogenic balanced process in the SMR reactor.

The simultaneous (sulfidogenic/methanogenic) process proved to be efficient and robust for the organic matter and sulfate removal. However, it required a longer adaptation period of the participating populations under the SMR reactor conditions, mainly for the acetoclastic MA.

The methane yield, considering the COD portion removed exclusively via methanogenesis, in the SMR reactor was similar to that obtained in the CR reactor. Thus, the sulfate reduction route did not cause significant damage to or inhibition of the methanogens under the studied conditions. Rather, the positive association between both processes enabled the anaerobic treatment of organic and sulfate-rich wastewaters (such as vinasse), with energy recovery by using the methane produced.

ACKNOWLEDGEMENTS

The authors gratefully acknowledge the National Council for Scientific and Technological Development (CNPq) (n° 131014/2012-9) and the São Paulo Research Foundation (FAPESP) (n° 2009/15984-0) for their financial support.

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