AbstractSynthetic detergent contains linear alkyl sulfonate (LAS) that presents a greater environmental risk compared to other contaminants. There has been an interest in replacing synthetic detergent with a more biodegradable detergent made from a mixture of sodium and potassium fatty acid. The present study conducted a field experiment by replacing the usage of detergent with soap (a combination of sodium and potassium fatty acid) in two household areas to evaluate the divergent effect of detergent and soap on the microbiome of the activated sludge process for sewage treatment. Results indicated that the use of soap increased the abundance of fatty acid-consuming bacteria and nitrogen-fixation bacteria. Additionally, soap enables more bacteria strains to be proactive in degrading organic matter, LAS, anionic, and nonionic surfactants. Consequently, replacing detergents with soap in WWTP service areas can positively influence microbial dynamics, improving the overall efficiency of the wastewater treatment process.
Graphical Abstract![]() 1. IntroductionThe viability and reproductive success of human and wildlife populations are influenced by anthropogenic endeavors [1], in particular the dissemination of potentially toxic chemicals. Marked by economic progress and industrial expansion, coupled with the advancement of sophisticated analytical techniques, various contaminants such as detergents, pesticides, antibiotics, illicit drug and microplastics have garnered scrutiny regarding their potential for exposure, toxicity, and risk evaluation [2–5]. Detergent is one of those contaminants that has been widely used worldwide. Detergents with linear alkylbenzene sulfonate (LAS) compounds tend to pose a higher environmental risk relative to the other contaminants [5,6].
LAS is an anionic surfactant, and its applications include detergents, emulsifiers, and penetrating agents. Due to its high cleansing capacity that decreases the surface tension of water, LAS has been extensively used as both household and industrial detergents [7]. LAS has various isotopes and isomers, typically ranging around C10 – C14 [8], and those with alkyl group carbons ranging from 10 (C10) to 14 (C14) were added to the water quality standards for the conservation of aquatic life since March 2013. Concerns over the effects on the aquatic environment are developing since LAS has been found in multiple wastewater treatment plants (WWTP) at quantities ranging from μg/L to mg/L [9,10]. In domestic wastewater, the concentrations of LAS commonly varied between 1000 and 10,000 μg/L, whereas in industrial wastewater around the globe, typically reached 83,000,000 μg/L [11,12].
According to the Japan Ministry of Environment, data obtained from public water monitoring, including 12,217 data points of rivers, lakes (2,414 data points) and the sea (3,674 data points) suggested that the LAS concentration ranged around 0.06 – 800 μg/L [13]. The maximum threshold for LAS concentration is set at 0.02 mg/L or less for freshwater areas and 0.006 mg/L or less for marine areas. In Yokohama City, the mean concentration of anion surfactants in influent sewage was determined to be 2.1 mg per liter, with a subsequent removal efficiency of 98% achieved during the wastewater treatment process [14]. However, despite remarkable removal via the activated sludge process in WWTP, high concentrations of LAS can disrupt the function of several microorganisms responsible for treatment in sewage treatment facilities and may slow down the treatment process [15].
A previous study reported that WWTP with 4.5 mg/L LAS has slightly lower microbial diversity than the other WWTPs with lower concentrations of LAS [16]. Furthermore, the study also reported that there are significant differences in microbial composition and abundance in WWTP with higher LAS demonstrated by the distinctly distant cluster of high LAS microbial group to the other group. Nevertheless, the study did not mention potential inhibition in microbial growth after exposure to LAS, since the study was primarily focused on determining the species that dominated the microbial communities and played a vital role in LAS degradation. Meanwhile, Dereszewska et al. [17] suggested that anionic surfactant loads exceeding 15 mg/g.dss have been observed to impede the respiration of activated sludge bacteria and diminish phosphorus removal capabilities. Moreover, such elevated loads have been found to alter the morphology of activated sludge flocs, leading to their fragmentation, as well as the lysis of protozoa cells. Other studies also demonstrated inhibition in the sewage degradation process due to the existence of LAS that results in lower degradation capacity and growth of biomass [18,19].
Due to the potential interferences in activated sludge microbiome caused by LAS concentration in WWTP, more biodegradable alternatives for detergent replacement are required. Several previous studies suggested the use of potassium fatty acids as this substance has low cytotoxicity, does not cause skin damage, and improves epidermal keratinocytes in human skin [20–22]. However, the effect of the usage of potassium fatty acids as detergent to WWTP’s activated sludge microbiome has not been extensively studied. Hence, the main aim of the current study was to determine how the usage of LAS and soap, made from a combination of sodium and potassium fatty acids, will affect the microbial communities responsible for sewage degradation in WWTP and which options will reduce the risk of damage to the dynamics of microorganisms.
In the present study, the sampling periods were divided into two: treatment with LAS and treatment with soap. Microbial communities from sludge were investigated using high-throughput next-generation sequencing and metagenomics analysis. The utilization of high-throughput sequencing techniques for microbial community analysis, coupled with subsequent metagenomic investigations, facilitates the comprehensive taxonomic and functional profiling of entire microbial communities [23–25]. These findings are expected to provide valuable insight regarding the potential of sodium and potassium fatty acids to replace the usage of LAS and reduce the risk of slowing down WWTP performance.
2. Materials and Methods2.1. Materials and Field ExperimentIn this study, soap from Shabondama Soap Co., Ltd. was used as a substitute for synthetic detergent. Shabondama soap, referred to as "soap" hereafter, is composed of sodium and potassium fatty acids derived naturally from beef tallow, rice bran oil, and palm oil.
The present study aimed to assess the impact of replacing synthetic detergent (containing LAS) with soap on the microbial communities involved in wastewater treatment. Field experiments were conducted in two districts of Munakata City, Fukuoka Prefecture: Tomari (30 households, 61 people) and Toyooka (32 households, 77 people). Participants used only soap instead of synthetic detergents for 3 months. Both districts employed wastewater treatment plants (WWTP) using the contact aeration method in a batch reactor system, with a maximum daily capacity of 76 m3 in Tomari and 95 m3 in Toyooka. Sludge samples were collected from the treatment tank walls.
2.2. Data Collection and Analytical MethodsWater and sludge samples were collected before switching from synthetic detergent to soap on August 24th, 2021, during soap experiments on September 7th, September 14th, September 27th, October 13th, October 26th, November 9th, and November 25th, and after switching back to synthetic detergent on December 15th 2021, January 18th, and February 15th 2022. Water samples were collected from December onward to monitor the progress of the experiment after it was completed. All samples were subjected to environmental parameter analysis including temperature, pH, dissolved oxygen concentration (DO), biochemical oxygen demand (BOD), suspended solids (SS), non-ionic surfactants, linear alkyl benzene sulfonic acid (LAS), and anionic surfactants according to the Standard Methods for the Examination of Water and Wastewater [26]. Due to the hazardous chemical restriction policy from the Japanese government, chemical oxygen demand (COD) was measured using the permanganate method [27,28].
2.3. 16S Metagenomic Analysis Using Next-Generation Sequencing (NGS)As much as 1.5 ml of DNA samples were collected from synthetic detergent and soap experiments. The DNA was isolated utilizing the NucleoSpin® kit following the NucleoSpin®Soil Manual. Post-extraction, the DNA samples were sent to the Faculty of Medicine at Yamaguchi University, Japan, for 16S rRNA analysis using next-generation sequencing (NGS) of Illumina MiSeq. In this study, alpha diversity analysis was performed to examine the species diversity of microorganisms in low-temperature cultures. This involved calculating the Shannon Diversity Index, Simpson's Index, and Evenness Index. Furthermore, a microbial heatmap was created using MeV 4.9.0, and additional statistical analyses were conducted with STAMP [29] and PAST.
3. Results and Discussion3.1. Results of Field Experiments (Water Quality Analysis Results)The effect of replacing synthetic detergents with soap on BOD, COD, anionic surfactant, non-ionic surfactant, and LAS concentration in the influent and effluent of WWTP in the Toyooka and Tomari area can be seen in Fig. 1. There was a slight improvement in BOD and COD degradation during the experimental period when the switch to soap was made. On average, the BOD removal in both Tomari and Toyooka reached 96% removal on soap usage compared to 94% and 92%, respectively, on synthetic detergent. Similarly, COD removal efficiency improved to 83% and 87% vs. 82% and 81% in Tomari and Toyooka, respectively.
In the present study, LAS, anionic surfactants, and non-ionic surfactants were used as parameters to evaluate the biodegradability of synthetic detergent and soap. Anionic surfactants, including LAS, are widely used in detergents, shampoos, and body soaps, and non-ionic surfactants are widely used in wetting agents and food industries [30]. From the surfactants and LAS measurements shown in Fig. 1(c) and (d), there were different responses observed in Tomari and Toyooka upon replacement to soap. In Tomori, the influent concentration of LAS, anionic, and non-ionic surfactants showed a decrease on the first day of soap replacement. Then, the concentration gradually increased along with the experimental periods and eventually soared after switching back to the usage of detergent. Despite the increase in LAS and surfactant concentration, the Tomori WWTP managed to maintain removal efficiency of LAS and surfactant in the range of 95 –98% during the usage of soap while returning to the range of 90 – 95% after switching back to synthetic detergent usage. Meanwhile in Toyooka, during the experimental periods, the LAS, anionic, and non-ionic surfactant concentrations showed an overall decreasing trend with removal efficiency ranging around 86 – 96% compared to 84 – 93% on synthetic detergent.
In Tomari WWTP, the decrease in BOD and COD removal efficiency, followed by a significant increase in LAS, anionic surfactants, and nonionic surfactants after switching back to synthetic detergent uses, causes massive formation of persistent foam (Fig. 2(a)). These findings can be a result of the immense usage of synthetic detergent by the residents after the experiment ended. Besides anthropogenic factors, temperature can also be a regulating factor that influences the foam formation in WWTP [30]. A previous study showed that a temperature of 20 – 30°C has an ideal surface tension for foaming ability and stability [31]. However, as seen in Fig. 2(b), foaming started to form after the experiment with soap ended while at the same time, the temperature started to decline to below 25°C from October, possibly due to the transition from autumn to winter. This signified that the usage of synthetic detergent generated more persistent foam in WWTP despite lower temperature and surface tension.
3.2. Alpha Diversity and Principal Component Analysis (PCA)In the present study, alpha diversity analysis including the Simpson index, Shannon index, Evenness index, and PCA in Tomari (Fig. 3(a)) and Toyooka (Fig. 3(b)), was utilized to provide insights into microbial community responses towards the usage of synthetic detergent and soap. Diversity indices are common analyses to assess the impact of environmental factors on microbial communities [24, 32–34].
Interestingly, the microbial diversity of Tomari WWTP and Toyooka WWTP showed opposite trends toward the introduction of soap. In Tomari, both the richness index (Shannon and Simpson) and the evenness index showed a declining trend during the soap experiment indicating that the use of soap caused domination of a certain species. When observed using PCA, only a few of the samples flocked into similar clusters, indicating similarity, while the other formed a noticeable distance from each other, indicating dissimilarity. This finding suggests that microbial communities in Tomari WWTP showed continuous changes in diversity during the treatment with soap and synthetic detergent.
Conversely, in Toyooka, all diversity indices demonstrated parallel patterns in microbial richness and evenness. This finding indicates stability in microbial diversity along the treatment process where the abundance of microorganisms was diversely distributed without domination from a single species of microorganisms. As seen in Fig. 3(b), before the soap experiment, the microbial diversity was at the lowest value in both species richness and evenness. After the detergent was replaced with soap, there was a significant surge in microbial richness and evenness, marking the potential increase in several microorganisms’ abundance. Increasing species abundance can be beneficial for the wastewater treatment process as it requires a vast array of microorganisms to degrade various organic matter from the sewage. After the soap experiment ended, the microorganisms in the WWTP managed to maintain their diversity for 1 month, however, immediately returned to the early level the next month. This finding further substantiated the potential more beneficial impact on microbial communities by the usage of soap compared to the usage of synthetic detergent.
3.3. Response of Microbial Communities towards Synthetic Detergent and Soap ExperimentFrom the 16S metagenomic analysis using NGS, the top 40 microbial communities with more than 0.2% relative abundance in Tomori and Toyooka WWTP are shown in Fig. 4(a) and (b), respectively. Both Tomari and Toyooka WWTP exhibited different compositions of microorganisms. This difference may be the primary cause of the contrasting response between microbial communities in Tomari WWTP and Toyooka WWTP toward the soap replacement (as previously discussed in Section 3.2).
In Tomari WWTP, before soap replacement, Thermomonas was found as the predominant bacteria among microbial communities with 3.09% relative abundance followed by Pedosphaera (3.07%), Azomonas (2.48%), and Vogesella (2.47%). Thermomonas is known as a denitrifying bacterium that is capable of the degradation of nonionic surfactants [35]. However, on the first day after replacing the synthetic detergent with soap, the abundance of Thermomonas started to decline following the decrease of nonionic surfactant concentration while the microbial domination started to shift to Runella (3.47%), Vogesella (3.02%), and Caldilinea (2.90%). Runella is a strain commonly found in activated sludge with a temperature of 25°C that actively metabolizes fatty acid [36]. Similar to Runella, Vogesella is also responsible for fatty acid metabolism and biosynthesis [37,38]. The growth of microorganisms with fatty acid metabolism properties is expected since the soap was made from a mixture of sodium and potassium fatty acid which triggered several microorganisms grown on fatty acids consumption.
On the final day of the soap experiment, Arenimonas and Caldilinea showed remarkable growth to dominate 8.2% and 4.2% of the total microbial communities, respectively. The presence of Arenimonas is important in the wastewater treatment process as a denitrifying bacteria that is responsible for nitrogen removal [39,40]. LAS, even in low concentration, can inhibit the growth of denitrifying bacteria which can cause an imbalance in the nitrogen cycle in the wastewater treatment process [41]. The flourishing growth of Arenimonas during the soap experiment suggested that the usage of soap potentially preserved the denitrification process in the wastewater treatment system. Meanwhile, the abundance of known LAS-degrading bacteria such as Pseudomonas sp. and Acinetobacter sp. [42–44], fluctuated around 0.56% – 1.9% and 0.3% – 1.78%, respectively during the soap experiment while increasing significantly on synthetic detergent usage. This indicates that these bacteria are more suitable for wastewater with higher LAS conditions.
Meanwhile, in Toyooka WWTP, before the application of soap, Arenimonas showed dominance in microbial communities with 5.9% relative abundance followed by Runella and Vogesella (4.8% and 4.4%, respectively). After the introduction of soap, several known fatty acid consumers, such as Runella and Vogesella, prevailed in the majority of microbial communities. Caldilinea was also found to thrive in the soap experiment (0.66% – 3% relative abundance) compared to synthetic detergent (0.33 – 0.39%). Caldilinea is a key player in the wastewater treatment process as these strains possess nitrite reductase gene (nrfAH) that contributes to the anaerobic ammonium oxidation process, playing a vital role in the nitrogen cycle by converting ammonia into nitrogen gas, thereby removing nitrogenous compounds from wastewater efficiently [45,46].
The other strains involved in the nitrogen fixation process in wastewater treatment, such as Thermomonas, Novophingobium, and Nitrospira also exhibited considerable dominance in microbial communities during soap experiments. These strains still maintain their dominance after switching back to the usage of synthetic detergent. This finding suggests that the soap experiment may have triggered the growth of nitrifying and denitrifying bacteria and adaptation to the exposure of LAS.
3.4. Correlation Between Microbial Communities and Environmental Parameters during Different Treatment ConditionsUtilizing Pearson correlation, the present study evaluated the inter-correlations of microbial communities to the changes in dissolved oxygen (DO), temperature, removal of organic matter, surfactants, and LAS removal in the wastewater between synthetic detergent and soap. As seen in Fig. 5(a), in Tomari WWTP, despite both soap and synthetic detergent showing insignificant differences in DO levels (less than 0.5 mg O2/L in the influent, and ranging around 5.6 – 7.1 mg O2/L in the effluent), the shift from synthetic detergent to soap increases the abundance of several microbial communities, such as Clostridium and Pseudomonas strains, which are known for their aerobic properties and influence changes in DO levels.
Temperature factors may also influence the biodegradation of organic matter during the activated sludge process. Several previous studies have suggested that the optimum temperature for the activated sludge process ranges between 14 and 30°C, which aligns with the optimal growth conditions for mesophilic microorganisms [47,48]. Despite the temperature ranging from 20 to 27°C during the soap experiment, compared to 13 to 26°C with synthetic detergent, the number of temperature-correlated strains did not exhibit any significant differences. This suggests that the abundance of the majority of microbial communities in both soap and synthetic detergent experiments showed similar alignment with the temperature gradients.
The current study found an increase in the number of microbial strains positively correlated to the BOD and COD removal during the soap experiment, in comparison to the synthetic detergent, was observed. This finding suggests that the usage of soap enables several strains, that were inactive during the usage of synthetic detergent, to contribute more to the degradation of the organic matter. Nevertheless, the usage of soap did not elevate the number of bacteria involved in LAS and surfactant removal but caused the increasing activity of bacteria that previously had a low correlation to LAS and surfactant removal (e.g. Pseudomonas, Thermomonas, and Novosphingobium) while also caused inactivation to several bacteria strains that previously have a higher correlation to LAS and surfactant removal (e.g. Verrucomicrobium, Flavobacterium, and Nitrospira).
The observed shift in microbial activity during the soap experiment was attributed to the substrate preferences of distinct microbial communities. The various surfactants present in synthetic detergents enhance the solubility of organic matter in sewage sludge, thereby promoting microbial communities that depend extensively on the production of volatile fatty acids (VFAs) [49]. These VFAs are generated through the degradation of complex carbohydrates via hydrolysis and acidogenesis processes [25]. The shift to using soap eliminates the supply of surfactants, thereby reducing the reliance of certain microbial communities on surfactants to break down complex carbohydrates into VFAs. Instead, these communities are inundated with an abundance of fatty acids and lipid-based substrates, which significantly alters the microbial landscape followed by the potential metabolic pathway change from carbohydrate metabolism to lipids and fatty acids metabolism. Pseudomonas Thermomonas, two nitrifying-denitrifying bacteria with proteolytic and lipolytic capabilities, exhibited extensive activity during the soap experiment periods. Their enzymatic abilities allow them to efficiently process fatty acids and lipids from the soap, explaining their dominance in the microbial community under these conditions [50,51].
Contrary to the Tomari WWTP, the microbial communities at Toyooka WWTP (Fig. 5(b)) exhibit mixed responses to changes in DO levels and temperature following the switch to soap. The temperature levels in Toyooka WWTP have an identical gradient to Tomari WWTP, however, the DO levels in the effluent fluctuate in a wider threshold (4.1 – 7 mgO2/L in soap experiment, 6.8 – 8.1 mgO2/L during synthetic detergent usage). The metagenomics analysis of the Toyooka WWTP provides a clearer picture that using soap allows the majority of microbial communities to participate in the degradation of COD, LAS, anionic, and nonionic surfactants. This indicates that the microbial communities in Toyooka WWTP prefer lower surfactant concentrations to enhance microbial activity and demonstrate tolerance to variations in substrate availability. This finding further demonstrates that the usage of soap may be beneficial for microbial communities in the WWTP system.
4. ConclusionsThis extensive investigation delved into the response of microbial communities toward the change of detergent usage, from synthetic detergent to soap made by the combination of sodium and potassium fatty acids, and its effect on the performance of the wastewater treatment process. Conducted in two areas, Tomari and Toyooka, the results suggest that the switch to soap promoted the abundance of microorganisms involved in fatty acid metabolism and the nitrification-denitrification process. The usage of soap further enhanced the number of microorganisms involved in the wastewater treatment process to degrade organic matter, LAS, anionic, and nonionic surfactants. Therefore, replacement with soap in the WWTP service area can be beneficial for the wastewater treatment process as it provides a positive effect on the microorganisms’ dynamics responsible for wastewater treatment.
NotesAuthor Contributions P.C. (Associate Professor in Environmental Engineering) performed conceptualization methodology, formal analysis, investigation, data curation, and writing—original draft. T.I. (Professor in Environmental Engineering): conceptualization, methodology, resources, writing— review and editing, supervision, project administration, and funding acquisition. G.A.W.S. (PhD Scholar): conceptualization, methodology, resources, formal analysis, visualization, writing—review and editing. A.F. (Researcher): conceptualization, methodology, resources, reviewing, and data analysis. Y.M. (Researcher): conceptualization, methodology, resources, reviewing, and data analysis. M.K. (Researcher): conceptualization, data curation, resources, reviewing, and data analysis. M.Y. (Company Representative): resources, investigation, and reviewing. T.K. (Company Representative): resources, investigation, and reviewing. T.K. (Company Representative): resources, reviewing, and investigation. References1. Hoekstra AY, Wiedmann TO. Humanity’s unsustainable environmental footprint. Science. 2014;344:1114–1117.
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![]() ![]() Fig. 1The influent and effluent concentration of BOD and COD in Tomari (a), Toyooka (b), and the concentration of anionic, nonionic surfactants, and LAS in Tomari (c) and Toyooka (d). ![]() Fig. 2Photos were taken from Tomari WWTP showing the lower intensity of foaming during the experiment using soap (left) than synthetic detergent (right) (a) and water temperature observed during the present study (b). ![]() Fig. 3The dynamics of alpha diversity analysis of microbial communities during the usage of synthetic detergent and soap in Tomari (a) and Toyooka (b). ![]() |
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