Bulking and rising sludge are common problems in wastewater treatment plants (WWTPs) and are primarily caused by increased growth of filamentous bacteria such as Microthrix parvicella. It has a negative impact on sludge settling properties in activated sludge (AS) process, in addition to being responsible for foam formation. Different methods can be used to control sludge bulking. The aim of this study was to evaluate the dosage of on-site generated ozone in the recycled AS flow in a full-scale WWTP having problems caused by M. parvicella. The evaluation of the experiment was assessed by process data, microscopic analysis and microbial screening on the experimental and control line before, during and after the period of ozone dosage. The ozone treatment resulted in decreased abundance of M. parvicella and improved the settling properties, without impairing the overall process performance. Both chemical oxygen demand (COD)- and N-removal were unaffected and the dominant populations involved in nitrification, as analysed by fluorescent in situ hybridization, remained during the experimental period. When the ozone treatment was terminated, the problems with sludge bulking reappeared, indicating the importance of continuous evaluation of the process.

INTRODUCTION

In the activated sludge (AS) process in wastewater treatment plants (WWTPs), the solid-liquid separation between the treated water and the sludge in the secondary clarifier is a critical step (Clauss et al. 1998). The most common cause of poor settling is an excessive development of filamentous bacteria in the sludge, known as filamentous bulking (Kappeler & Gujer 1994; Eikelboom 2000). The filamentous bacterium Microthrix parvicella is frequently involved in bulking and foaming problems in municipal AS processes, especially those that include biological nitrogen and phosphorous removal due to the increased sludge retention time needed (Martins et al. 2004; Müller et al. 2007). For the WWTPs, these problems result in decreased capacity, low solid retention, increased costs and deteriorated effluent quality (van Leeuwen 1992).

Based on observations in full-scale WWTPs, M. parvicella seem to be highly versatile with several metabolic strategies for utilizing lipids available in the wastewater (Rossetti et al. 2005). It thrives and survives under a range of conditions and its presence does not indicate any specific operational conditions causing filamentous bulking. Therefore, non-specific methods that decrease the filaments, without removing the causes of M. parvicella proliferation permanently are often recommended to reduce filamentous bulking. These include different chemicals such as ballasting agents (often talc based), biocides (mostly chlorine based), coagulants (commonly synthetic polymers) or a combination of these products (Nielsen et al. 2005 and summarized in Kumari et al. 2009). As an alternative to these treatments, ozone can be used. Previous studies suggest that ozone causes inactivation of the filamentous bacteria through cell wall disintegration and cell lysis (White 1999; Caravelli et al. 2006). Advantages with ozone are that it shows a faster effect than chemical dosing and does not give chemical residues (Al, Fe, Cl) in the water (Ried et al. 2014). However, most studies concerning ozonation in AS have focused on minimizing the production of excess sludge rather than the filamentous bacteria and the recommended ozone dose is 30–50 g O3/kg total suspended solids (TSS) to reach a powerful and cost efficient sludge reduction (Chu et al. 2009b). The dose for bulking control is an order of magnitude lower, and only a few studies have considered the use and efficiency of low dosage in full-scale plants as an alternative to chemical bulking control (Saayman et al. 1996; Lyko et al. 2012; Nilsson et al. 2014; Ried et al. 2014).

In this study, the aim was to evaluate the possibility of combatting poor settling properties and filamentous bulking caused by M. parvicella by addition of on-site generated ozone to an AS process without compromising the overall process performance and nitrogen removal. For this purpose, settling properties and process data were combined with microscopy to estimate abundance of filaments and microbial screening of nitrifying bacteria. The ozone experiment was conducted in a full-scale WWTP over 110 days and the process was monitored in the experimental and control line before, during and after the period of ozone treatment.

MATERIALS AND METHODS

WWTP and full-scale experiment

The Himmerfjärden WWTP treats domestic (295,000 person equivalent, p.e.) and industrial wastewater (50,000–60,000 p.e.) using an AS process with nitrogen removal. The system has a plug flow configuration and includes an aeration tank for biochemical oxygen demand (BOD) removal and nitrification followed by secondary and final settler. This is followed by fluidized beds for denitrification. The treatment capacity is 3.9 m3/s and the effluent enters the recipient bay, Himmerfjärden, which is connected to the Baltic Sea.

The experiment was carried out using two out of eight parallel biological treatment lines, each comprising a 2,710 m³ aeration tank, a 2,700 m³ secondary settler, and a 3,000 m³ final settler. One of the two lines was used to test the effect of ozone on sludge bulking and growth filamentous bacteria and the other was the untreated control. The OZAT® OZONGENERATOR TYP CF-6A (Air Liquide) was used for on-site generation of ozone. The ozone generator was fed with a gas composition of 98% O2 and 2% N2 resulting in ozone production when the oxygen flows through a field of high voltage, i.e. corona discharge. Ozone was injected to a partial return activated sludge (RAS) flow via a reactor with an injector consisting of a double venturi system. The injection of ozone in the return loop optimized the contact with the sludge, which involved dissolution of ozone in the RAS under a vacuum that is produced by the venturi part along with the high pressure RAS pump. The system was designed with a maximum treatment capacity of 30 m³/h RAS, corresponding to 10% of the total, normal RAS flow per line at Himmerfjärden WWTP. During the experimental period, dissolved oxygen (DO) control and DO set points were 2 mg/l and sludge age was approximately 15 days. The suspended solids (SS) in the aeration tank and return sludge were 2,600 mg/l and 5,000 mg/l, respectively.

Prior to ozone treatment, both lines were fed with the same RAS over several weeks to ensure similar conditions in the two lines, and at the start of the experiment the RAS flows were separated. Ozone was added continuously during 84 days. During the first 59 days the ozone dosage was 6.6 g O3/kg mixed liquor suspended solids (MLSS) after which it was lowered to 4.4 g O3/kg MLSS during days 60–82 and stopped at day 82 to investigate whether the problems with sludge bulking would reappear. The two doses are denoted high and low. The experiment was monitored one month before the start of ozone treatment, during the 82 days of operation with ozone and 28 days after terminating the ozone treatment.

Process parameters and sludge settling properties

MLSS Swedish Standard (SS) 02 81 12–3 were measured in the RAS and in the effluent after the final settler. Nitrate (NO3, Hach-Lange LCK 340) was measured in the treated and untreated RAS and ammonium (NH4+, Hach-Lange LCK 303) in the effluent from final settler for the evaluation of the effect of ozone on the nitrification process, being the first step in nitrogen removal at Himmerfjärden WWTP. To evaluate the overall process performance, influent and effluent chemical oxygen demand (COD) (Hach-Lange LCK 114) and dissolved organic carbon (DOC) (Hach-Lange LCK 385) were determined. In the RAS, total phosphorus (Tot-P, SS EN 11 89-6) was measured. The chemical process parameters were measured weekly except for SS, NO3 and NH4+ which were analysed every second day (n = 2).

To characterize sludge settling properties, the sludge volume index (SVI) was calculated according to Fitch & Kos (1976). SVI was measured once a week and the lower the SVI, the better the sludge settling properties.

Microscopic analysis of floc shape and filamentous bacteria

To monitor floc shape and filamentous bacteria during the course of the experiment, duplicate grab samples from each line were collected in the aeration tank for microscopic analysis before ozone treatment started, during the experimental period and after the treatment was terminated. Floc shape and size were determined weekly according to Jenkins et al. (2003). In the same samples, the abundance of filamentous bacteria, extended growth, and total filament growth was determined based on using crystal violet staining (Knoop & Kunst 1998) and the Jenkins scale (Jenkins et al. 2003). At four occasions (prior to ozone treatment and after 21, 48 and 81 days of ozone treatment) Gram & Neisser staining of sludge samples (Eikelboom 2000) was performed to verify detection of filamentous bacteria.

Estimation of viable cells and FISH analysis of M. parvicella and the nitrifying community

To estimate the fraction of viable microbial cells, image analysis was used to compare the amount of intact membranes with cells showing compromised membranes using the Live-dead kit (LIVE/DEAD®BacLight™ Bacterial Viability Kit, for microscopy and quantitative assays) in all samples. The assay can distinguish between cells with a compromised membrane as these are stained red and viable cells as these are stained green.

Prior to ozone treatment, it was confirmed that M. parvicella was the dominating filamentous bacteria in the aeration tanks using the fluorescent in situ hybridization (FISH) probe Mpa_all 1410 as described by Levantesi et al. (2006). A permeabilization step was applied prior to the FISH procedure using mutanolysin to ensure permeability of the Gram positive cell wall (Erhart et al. 1997). Both the ammonia and nitrite oxidizing communities in the aeration tank were analysed by FISH probes before the experiment started and after 21 and 81 days of ozone treatment. Initially, several FISH probes for ammonia-oxidizing bacteria (AOB) were applied (Supplementary Table S1, available in the online version of this paper), but only a limited number of the probes resulted in a FISH signal suitable for quantification. Based on the initial screening, the following probes were used for quantification at the following sampling occasions: probe Cluster6a192 with competitor (Adamczyk et al. 2003) and probe Nmo218 (Gieseke et al. 2001) for detection of the Nitrosomonas oligotropha lineage. The nitrite oxidizing bacteria (NOB) were quantified using the genus probe for Nitrospira (Ntspa662 with competitor; Daims et al. 2001). FISH analysis of AOB and NOB were performed according to Nielsen et al. (2009).

RESULTS AND DISCUSSION

Effects on sludge bulking, settling properties and filamentous bacteria

In the present study, ozone treatment of the return sludge in low doses had an immediate effect on sludge bulking and a large impact on the sludge settling ability, which agrees with the few previous reports investigating ozone for bulking control (Saayman et al. 1996; Lyko et al. 2012; Nilsson et al. 2014). Before ozone treatment started, filamentous bulking occurred in both the experimental and control line of the AS process at Himmerfjärden WWTP. This coincided with high SVI values (around 200 ml/g in both lines) and the presence of filamentous bacteria identified as M. parvicella.

After only 1 week with the higher dosage (6.6 g O3/kg SS), there was a large difference in SVI between experimental and control line (Figure 1(a)) as well as sludge bulking (Supplementary Figure S1, available in the online version of this paper). During the period with this dose, there was a significant difference (P < 0.001, n = 7; t-test) between the mean value in the experimental (76 ± 21 ml/g) and the control line (238 ± 53 ml/g). Also during the period with a lower dosage (4.4 g O3/kg SS), which was set in order to see whether the positive effect remained, the difference between the lines was significant (P = 0.05, n = 3). The poor settling properties in the control line resulted in occasionally higher values of SS in the effluent from the final settler, whereas the values in the experimental line were below 14 mg/l during the entire period of ozone treatment (Supplementary Figure S2, available in the online version of this paper). Four weeks after terminating ozone addition, the settling properties were similar to pre-experimental levels in the control line (Supplementary Figure S2; P = 0.33, n = 3). However, 3 weeks of additional monitoring of the SVI showed that both lines displayed increasing SVI values (Figure 1(a)). This could be due to the decrease in temperature during September to January, since it is well known that M. parvicella is commonly more abundant when it is cold (e.g. Mamais et al. 1998; Martins et al. 2004; Rossetti et al. 2005).
Figure 1

(a) SVI and (b) floc density for the control (solid line) and experimental line (dashed line). The start of ozone treatment, the change in dosage and the end of ozone treatment are marked with vertical lines.

Figure 1

(a) SVI and (b) floc density for the control (solid line) and experimental line (dashed line). The start of ozone treatment, the change in dosage and the end of ozone treatment are marked with vertical lines.

The effect of ozone treatment was also reflected by a decrease in floc size and an increase in floc density. When the ozone dose was lowered, the density decreased and after the treatment was terminated, it was the same as for the control line (Figure 1(b)). For the size, an effect of the lower dose was not obvious, but after termination of ozone treatment, also floc size was similar between the two lines (data not shown).

Further microscopic examination of the sludge revealed that unbranched filamentous bacteria were entangled inside the sludge flocs and formed bridges between flocs (Supplementary Figure S3, available in the online version of this paper). However, both the total and the extended filament growth decreased rapidly after ozone treatment began (Figure 2(a) and 2(b)). The initial increase in total phosphorus content in the ozone treated RAS (Figure 3) could be an effect of released cell content due to the oxidizing effect of ozone causing cell lysis. This suggests that ozone penetrated the filamentous bacteria and caused irreversible damage leading to lysis, as described by Chu et al. (2009a). When the abundance of filamentous bacteria decreased, the RAS phosphorus content in the experimental and control lines started to converge (Figure 3).
Figure 2

(a) Total and (b) extended filament growth in the control (solid line) and experimental line (dashed line). The start of ozone treatment, the change in dosage and the end of ozone treatment are marked with vertical lines.

Figure 2

(a) Total and (b) extended filament growth in the control (solid line) and experimental line (dashed line). The start of ozone treatment, the change in dosage and the end of ozone treatment are marked with vertical lines.

Figure 3

Total phosphorus in the treated (dashed line) and untreated (solid line) RAS.

Figure 3

Total phosphorus in the treated (dashed line) and untreated (solid line) RAS.

The Gram positive staining and Neisser positive phosphor granules indicated that M. parvicella were present in large numbers in the sample from the untreated line during the entire period of operation (data not shown). By contrast, only a few M. parvicella remained inside the sludge flocs after 21 days of ozone treatment and Gram staining showed that the filaments were either Gram positive with many empty cells or even completely Gram negative. After 48 days, mostly Gram negative cells and almost empty phosphorus granules were detected in the sludge from the ozone-treated line. When lowering the ozone dose, more filamentous bacteria stained Gram positive and contained Neisser positive phosphor granules (data not shown). Thus, the lowered ozone dosage had lower impact on M. parvicella. Nevertheless, since the settling properties were good (Figure 1) and the amount of both extended and total filaments were low, we conclude that both ozonation conditions were adequate to control filamentous bulking. In previous studies, ozone dosage of 2.8–5.0 O3/kg SS was sufficient to control filamentous bulking with improvements on sludge settling properties in full-scale WWTPs (Nilsson et al. 2014) and even lower ozone dosages (1.4–1.7 O3/kg SS) have been shown to have positive effects on the settling ability (Saayman et al. 1996; Lyko et al. 2012; Ried et al. 2014). There is no report on how long these effects last, but in the present study we show that after 8 days without ozone treatment the problems with the filamentous bacteria started to reappear and after 22 days the levels were the same as in the control (Figure 2(a) and 2(b)).

Worth noting is that Himmerfjärden WWTP is still using ozone treatment all year round, when needed. However, if ozonation is used for a longer period, the efficiency of the treatment decreases, but after a temporary stop the effect reappears. Exposure to sub-lethal ozone doses could potentially lead to adaptation and resistance to ozone of some bacteria. This is poorly studied, but Dziurla et al. (2005) showed that no development of resistance to ozonation occurred after sludge treatment with low ozone doses in their study. Two plausible explanations to a decrease in efficiency are: (i) the gradual increase of soluble compounds can protect the cells from lysis (Foladori et al. 2010); and (ii) the proteins released can affect the sludge dewatering negatively due to their charge on the surface (Chu et al. 2009b). Therefore, altering operation (on/off) is a conceivable solution as described by Ried et al. (2014).

Effects on process performance and nitrifying bacteria

COD reduction was efficient in both lines, as there were no differences in influent and effluent COD (Figure 4(a)) or DOC (data not shown) between the treated and control line. Similarly, no differences in nitrate concentration in the untreated (12.0 ± 5.3 mg NO3-N L−1) and treated RAS (11.9 ± 6.8 mg NO3-N L−1) during the period of ozone treatment was observed. Also the average ammonium levels in the effluent of the final settler were similar in the two lines with 1.29 ± 0.70 mg NH4-N L−1 and 1.35 ± 0.66 mg NH4-N L−1 in the treated and untreated line, respectively (Figure 4(b)). Moreover, no big difference was observed on the live:dead ratio between control and experimental line (Table 1). Thus, in agreement with Nilsson et al. (2014) the overall process performance in terms of COD and nitrogen removal were equally good in the two lines, showing that ozone had no negative impact on the treatment process.
Table 1

The ratio between living and dead cells and relative abundance of AOB and NOB in the control (untreated) and experimental (treated) line

Target FISH probe Before treatment (%) Day 21 treated (%) Day 21 untreated (%) Day 81 treated (%) Day 81 untreated (%) 
Live:dead  87 74 72 79 79 
AOB Cluster6a 3.6a ± 4.5 2.9 ± 2.4 2.8 ± 2.6 4.3 ± 2.1 4.8 ± 2.1 
 Nmo218 3.4a ± 2.3 2.9 ± 2.4 2.6 ± 2.5 3.7 ± 2.8 4.5 ± 4.2 
NOB Ntspa662 2.4 ± 1.6 1.8 ± 1.8 2.3 ± 1.5 1.1 ± 1.2 0.6 ± 0.7 
Target FISH probe Before treatment (%) Day 21 treated (%) Day 21 untreated (%) Day 81 treated (%) Day 81 untreated (%) 
Live:dead  87 74 72 79 79 
AOB Cluster6a 3.6a ± 4.5 2.9 ± 2.4 2.8 ± 2.6 4.3 ± 2.1 4.8 ± 2.1 
 Nmo218 3.4a ± 2.3 2.9 ± 2.4 2.6 ± 2.5 3.7 ± 2.8 4.5 ± 4.2 
NOB Ntspa662 2.4 ± 1.6 1.8 ± 1.8 2.3 ± 1.5 1.1 ± 1.2 0.6 ± 0.7 

aThe dilution of the sample could result in an overestimation of the population.

Figure 4

(a) Influent and effluent COD values for the control (solid line) and experimental line (dashed line). (b) Ammonium in effluent of final settler in the control (solid line) and experimental line (dashed line). The start of ozone treatment, the change in dosage and the end of ozone treatment are marked with vertical lines.

Figure 4

(a) Influent and effluent COD values for the control (solid line) and experimental line (dashed line). (b) Ammonium in effluent of final settler in the control (solid line) and experimental line (dashed line). The start of ozone treatment, the change in dosage and the end of ozone treatment are marked with vertical lines.

The results on nitrogen transformations and removal indicate that no inhibition of ammonia and nitrite oxidation occurred due to treatment with ozone and the microbial analysis of the nitrifying community using FISH confirms that (Table 1). Positive signal for AOB was observed using the two probes Cluster 6a192 and Nmo218, and for NOB the probe Ntspa662 indicating that Nitrosomonas spp. in cluster 6a and Nitrospira spp. were involved in oxidation of ammonia and nitrite, respectively. Cluster 6a192 includes both the N. oligotropha and Nitrosomonas ureae lineages. However, since the two probes resulted in equal abundance of the targets and only Nmo218 detects N. ureae, this suggests that the AOB were dominated by N. oligotropha. These AOB are common in other Swedish WWTPs (e.g. Hallin et al. 2005; Rodriguez-Caballero et al. 2012) and several studies have shown the presence of N. oligotropha in WWTPs with low influent ammonium concentrations (Bollmann & Laanbroek 2001; Koops & Pommerening-Röser 2001; Limpiyakorn et al. 2007) like Himmerfjärden WWTP.

For both the Nitrosomonas spp. and the Nitrospira spp., minor variations in the size of the communities in relation to the total bacterial community (according to live:dead staining) were observed over time, but there was no effect of ozone treatment on population abundance (Table 1). There was a decrease in the number of NOBs 80 days after ozone treatment started, but since the NOBs decreased in both the treated and untreated line, this could be due to the lower temperature during the winter period within experimental time that resulted in decreased growth rates. However, no effect could be seen on the effluent ammonium concentration indicating that there still were enough bacteria present for an efficient removal process. Alternatively, other NOB not detected by our probes could be performing nitrite oxidation. That nitrifiers, but not M. parvicella were unaffected by ozone could be because nitrifying bacteria are often located in the inner zone of the flocs and thereby more protected (Böhler & Siegrist 2004), whereas M. parvicella are present in the bulk water. They also have a high surface area to volume ratio making them more predisposed to ozone attack (Ried et al. 2014) than other microorganisms.

CONCLUSIONS

We have demonstrated that low ozone doses can be used to demolish the filamentous sludge structures and control the re-growth of filamentous bacteria, such as M. parvicella, without disturbing the overall process performance and nitrogen removal capacity of the WWTP and the microbial populations important for the process. Therefore, ozone treatment can be recommended when bulking problems are highlighted by high values of SVI and filament indices. However, the reappearance of sludge bulking was evident once the ozone treatment stopped. Therefore, the effects of ozone treatment on sludge bulking caused by filamentous bacteria must be evaluated continuously.

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Supplementary data