ABSTRACT
The reuse of reclaimed water is a cost-effective way to alleviate water resource scarcity, but the residual pathogenic microorganisms inevitably influence the safety of its reuse. The transport behavior of pathogenic microorganisms in receiving porous media varies under different environmental factors and could be harmful to the natural ecology and even human health if not well treated. Biochar is expected to be an effective, environmentally-friendly functional material to inhibit the transport of pathogenic microorganisms, with unreplaceable advantages of low price, simple preparation method, and strong adsorption capacity. In the present paper, we start from identifying the transport behavior of typical pathogenic microorganisms in porous media, including protozoa, bacteria, and viruses, and then analyzing the primary factors affecting the transport of pathogenic microorganisms from the aspects of biology, physics, and chemistry. Furthermore, the effects of types of raw materials, pyrolysis temperature, particle size, and functional modification methods on the remediation performance of biochar for the transport of pathogenic microorganisms are clearly reviewed. Finally, we aim to clarify the transport rules of pathogenic microorganisms in porous media and provide biochar-based technical means for effectively inhibiting the transport of pathogenic microorganisms, thereby improving the ecological and health safety of reclaimed water reuse.
HIGHLIGHTS
Pathogenic microorganisms could spread widely through transport behavior in porous media.
The biological, physical, and chemical factors affecting the transport of pathogenic microorganisms were reviewed.
Parameters of biochar impacting the transport of pathogenic microorganisms were discussed.
Biochar is expected to have practical applications in inhibiting the transport of pathogenic microorganisms.
INTRODUCTION
The concentration limits of pathogenic microorganisms in reclaimed water and their transport behavior in receiving porous media (* refers to Escherichia coli (E. coli) and unlabeled refers to fecal coliform).
The concentration limits of pathogenic microorganisms in reclaimed water and their transport behavior in receiving porous media (* refers to Escherichia coli (E. coli) and unlabeled refers to fecal coliform).
The transport behavior of pathogenic microorganisms is easily affected by their properties and the physical and chemical properties of porous media (Abudalo et al. 2010; Kim et al. 2010; Jin et al. 2021). Due to the complex structures and spatial heterogeneity of porous media in nature, the transport behavior of pathogenic microorganisms in the environment is affected by multiple factors and becomes more complex (Dong et al. 2014; Zhang et al. 2021a). At present, there are many studies on the transport behavior of pathogenic microorganisms in porous media, and some studies have paid attention to the effects of biological factors (Haznedaroglu et al. 2010; Chandrasena et al. 2017; Kim & Kwon 2022), physical factors (Abit et al. 2012; Jin et al. 2021; Zhang et al. 2022), and chemical factors (Mohanram et al. 2010; Weaver et al. 2013; He et al. 2019) on the transport behavior of pathogenic microorganisms in porous media. However, no review has systematically summarized the transport rules of pathogenic microorganisms in porous media. Therefore, summarizing the transport rules of pathogenic microorganisms in porous media and clarifying their influencing factors has certain theoretical guiding significance for inhibiting the pollution of pathogenic microorganisms and improving the utilization rate of reclaimed water.
At present, environmental functional materials such as organic polymer materials, nanoparticles, natural minerals, activated carbon, and biochar have been used to inhibit the transport behavior of pathogenic microorganisms in porous media due to their unique physical and chemical properties (Ngwenya et al. 2015; Sasidharan et al. 2016; He et al. 2019). Among them, biochar is a carbon-rich substance produced by the pyrolysis of biomass at high temperatures under anaerobic or anoxic conditions. It has active functional groups, excellent pore structure, and large specific surface area (SSA), and has been widely used in environmental treatment and restoration (Wang & Wang 2019). The application of biochar to the environment is bound to impact the transport behavior of pathogenic microorganisms. Studies currently have shown that adding biochar can inhibit the transport of pathogenic microorganisms, especially bacteria in porous media (Mohanty & Boehm 2014; Fernando Perez-Mercado et al. 2019). However, some studies also stated that the transport of pathogenic microorganisms such as bacteria and viruses was promoted after adding the low-temperature pyrolyzed biochar into sand media (Abit et al. 2012; Bolster & Abit 2012; Sasidharan et al. 2016). The conflicts among previous studies greatly limit the application of biochar in inhibiting the transport of pathogenic microorganisms.
Therefore, a literature review of studies reporting the transport behavior of pathogenic microorganisms in porous media and the remediation capability of biochar until February 2024 was performed. Publications were retrieved from databases including Web of Science, ScienceDirect, Springer, American Chemical Society, and Wiley. The following search strings were used: ‘transport’ AND ‘porous media’ AND (‘pathogenic microorganism’ OR ‘protozoa’ OR ‘bacteria’ OR ‘phages’ OR ‘cryptosporidium’ OR ‘giardia’ OR ‘amoeba’) and ‘transport’ AND ‘porous media’ AND ‘biochar’ AND (‘pathogenic microorganism’ OR ‘protozoa’ OR ‘bacteria’ OR ‘phages’ OR ‘cryptosporidium’ OR ‘giardia’ OR ‘amoeba’). Finally, we aim to provide information to reduce the risk of the transport of pathogenic microorganisms in the receiving porous media and improve the ecological and health safety of reclaimed water reuse.
INFLUENCING FACTORS OF THE TRANSPORT BEHAVIOR OF PATHOGENIC MICROORGANISMS IN POROUS MEDIA
Experimental design of a column experiment for studying the transport behavior of pathogenic microorganisms in porous media.
Experimental design of a column experiment for studying the transport behavior of pathogenic microorganisms in porous media.
Transport abilities of typical pathogenic microorganisms in porous media
| Pathogenic microorganism | Initial concentration | Type of porous media | Breakthrough percentage | Reference | |
|---|---|---|---|---|---|
| Protozoon | Cryptosporidium (oocysts/mL) | 1.4 × 103 ± 7.5 × 102 | Castricum soil, roosteren soil | 0.6–3% | Hijnen et al. (2005) |
| 2 × 106 | Quartz sand, ottawa sand | 1.0–96.3% | Kim et al. (2010) | ||
| 2 × 106 | Soil | 1–71% | Mohanram et al. (2010) | ||
| 100 | Sandy soil | 0–18.7% | Santamaria et al. (2011) | ||
| 2 × 106 | Quartz sand | 1–69% | Bradford et al. (2016) | ||
| Amoeba spores (spores/mL) | 2 × 102–2 × 103 | Quartz sand | 29.9–89.5% | Jin et al. (2021) | |
| 102–103 | Quartz sand | 21.4–83.2% | Jin et al. (2022) | ||
| Giardia (cysts/mL) | 1.6 × 103 ± 5.0 × 102 | Castricum soil, roosteren soil | 1.6–8.5% | Hijnen et al. (2005) | |
| 8.23 × 103 | Ottawa aquifer sand | 0.4–1.8% | Bradford et al. (2006) | ||
| Bacterium (CFU/mL) | E. coli | 1.0 × 108 ± 10% | Quartz sand | 4.0–85.0% | Yang et al. (2012b) |
| 1.5 × 107 ± 10% | Quartz sand | 47.8–92.7% | Wu et al. (2016) | ||
| 2.5 × 107 ± 10% | Quartz sand | 15.8–89.8% | Yang et al. (2016) | ||
| 1.5 × 107 ± 10% | Quartz sand | 23.2–84.0% | Wu et al. (2018) | ||
| 1.25 × 107 ± 10% | Quartz sand | 48.5–90.7% | He et al. (2018) | ||
| 1.5 × 107 ± 10% | Quartz sand | 4.4–92.5% | He et al. (2019) | ||
| 5 × 107 | Quartz sand | 63.3–70.0% | Liu et al. (2021) | ||
| 1.35 × 107 ± 10% or 1.35 × 108 ± 10% | Quartz sand | 33.9–94.2% | Zhang et al. (2021a) | ||
| 1.6 × 107 ± 10% | Quartz sand | 11.0–59.2% | He et al. (2022) | ||
| Bacillus subtilis | 1.5 × 107 ± 10% | Quartz sand | 63.3–93.8% | Wu et al. (2016) | |
| 1.1 × 109 | Aquifer soil | 10.9–16.5% | Oudega et al. (2021) | ||
| Salmonella typhimurium | 6.4 × 108––1.93 × 109 | Fontainebleau sand | 33.1–52.0% | Zheng et al. (2022) | |
| Pseudomonas putida | 5 × 107 | Quartz sand | 65.2–70.0% | Liu et al. (2021) | |
| Desulfovibrio sp. | 5 × 107 | Quartz sand | 58.7–70.0% | Liu et al. (2021) | |
| Shewanella oneidensis MR1 | 5 × 107 | Quartz sand | 37.5–70.0% | Liu et al. (2021) | |
| Shewanella putrefaciens CN32 | 5 × 107 | Quartz sand | 43.2–70.0% | Liu et al. (2021) | |
| Virus (PFU/mL) | ΦX174 phage | (3.7+0.9) × 103 | Glass beads | 31.9–43.6% | Syngouna & Chrysikopoulos (2016) |
| 106 | Sand | 1–93% | Xu et al. (2017) | ||
| 2.1 × 109 | Aquifer soil | 0.3–0.4% | Oudega et al. (2021) | ||
| MS2 phage | 109 | Sand, sand loaded with iron oxide | 0.1–50.1% | Bradley et al. (2011) | |
| 108–1010 | Quartz sand | 82% | Ghanem et al. (2016) | ||
| (11.6 ± 4.4) × 103 | Glass beads | 29.9–51.6% | Syngouna & Chrysikopoulos (2016) | ||
| vB_PSPS-H40/1 phage | 108–1010 | Quartz sand | 12% | Ghanem et al. (2016) | |
| 108–1010 | Quartz sand | 25% | Ghanem et al. (2018) | ||
| PSA-HM1 phage | 108–1010 | Quartz sand | 36% | Ghanem et al. (2016) | |
| 108–1010 | Quartz sand | 80% | Ghanem et al. (2018) | ||
| T4 phage | 108–1010 | Quartz sand | 4% | Ghanem et al. (2016) | |
| 108–1010 | Quartz sand | 63% | Ghanem et al. (2018) | ||
| vB_EcoM-ep3 phage | 106 | Natural sand | 33.2–59.0% | Qin et al. (2020) | |
| 106 | Natural sand | 6.6–38.8% | Zhang et al. (2021b) | ||
| PSA-HP1 phage | 108–1010 | Quartz sand | 75% | Ghanem et al. (2016) | |
| PSA-HS2 phage | 108–1010 | Quartz sand | 63% | Ghanem et al. (2016) | |
| vB_PSPS-H6/1 phage | 108–1010 | Quartz sand | 24% | Ghanem et al. (2016) | |
| H3/49 phage | 108–1010 | Quartz sand | <1% | Ghanem et al. (2016) | |
| Pathogenic microorganism | Initial concentration | Type of porous media | Breakthrough percentage | Reference | |
|---|---|---|---|---|---|
| Protozoon | Cryptosporidium (oocysts/mL) | 1.4 × 103 ± 7.5 × 102 | Castricum soil, roosteren soil | 0.6–3% | Hijnen et al. (2005) |
| 2 × 106 | Quartz sand, ottawa sand | 1.0–96.3% | Kim et al. (2010) | ||
| 2 × 106 | Soil | 1–71% | Mohanram et al. (2010) | ||
| 100 | Sandy soil | 0–18.7% | Santamaria et al. (2011) | ||
| 2 × 106 | Quartz sand | 1–69% | Bradford et al. (2016) | ||
| Amoeba spores (spores/mL) | 2 × 102–2 × 103 | Quartz sand | 29.9–89.5% | Jin et al. (2021) | |
| 102–103 | Quartz sand | 21.4–83.2% | Jin et al. (2022) | ||
| Giardia (cysts/mL) | 1.6 × 103 ± 5.0 × 102 | Castricum soil, roosteren soil | 1.6–8.5% | Hijnen et al. (2005) | |
| 8.23 × 103 | Ottawa aquifer sand | 0.4–1.8% | Bradford et al. (2006) | ||
| Bacterium (CFU/mL) | E. coli | 1.0 × 108 ± 10% | Quartz sand | 4.0–85.0% | Yang et al. (2012b) |
| 1.5 × 107 ± 10% | Quartz sand | 47.8–92.7% | Wu et al. (2016) | ||
| 2.5 × 107 ± 10% | Quartz sand | 15.8–89.8% | Yang et al. (2016) | ||
| 1.5 × 107 ± 10% | Quartz sand | 23.2–84.0% | Wu et al. (2018) | ||
| 1.25 × 107 ± 10% | Quartz sand | 48.5–90.7% | He et al. (2018) | ||
| 1.5 × 107 ± 10% | Quartz sand | 4.4–92.5% | He et al. (2019) | ||
| 5 × 107 | Quartz sand | 63.3–70.0% | Liu et al. (2021) | ||
| 1.35 × 107 ± 10% or 1.35 × 108 ± 10% | Quartz sand | 33.9–94.2% | Zhang et al. (2021a) | ||
| 1.6 × 107 ± 10% | Quartz sand | 11.0–59.2% | He et al. (2022) | ||
| Bacillus subtilis | 1.5 × 107 ± 10% | Quartz sand | 63.3–93.8% | Wu et al. (2016) | |
| 1.1 × 109 | Aquifer soil | 10.9–16.5% | Oudega et al. (2021) | ||
| Salmonella typhimurium | 6.4 × 108––1.93 × 109 | Fontainebleau sand | 33.1–52.0% | Zheng et al. (2022) | |
| Pseudomonas putida | 5 × 107 | Quartz sand | 65.2–70.0% | Liu et al. (2021) | |
| Desulfovibrio sp. | 5 × 107 | Quartz sand | 58.7–70.0% | Liu et al. (2021) | |
| Shewanella oneidensis MR1 | 5 × 107 | Quartz sand | 37.5–70.0% | Liu et al. (2021) | |
| Shewanella putrefaciens CN32 | 5 × 107 | Quartz sand | 43.2–70.0% | Liu et al. (2021) | |
| Virus (PFU/mL) | ΦX174 phage | (3.7+0.9) × 103 | Glass beads | 31.9–43.6% | Syngouna & Chrysikopoulos (2016) |
| 106 | Sand | 1–93% | Xu et al. (2017) | ||
| 2.1 × 109 | Aquifer soil | 0.3–0.4% | Oudega et al. (2021) | ||
| MS2 phage | 109 | Sand, sand loaded with iron oxide | 0.1–50.1% | Bradley et al. (2011) | |
| 108–1010 | Quartz sand | 82% | Ghanem et al. (2016) | ||
| (11.6 ± 4.4) × 103 | Glass beads | 29.9–51.6% | Syngouna & Chrysikopoulos (2016) | ||
| vB_PSPS-H40/1 phage | 108–1010 | Quartz sand | 12% | Ghanem et al. (2016) | |
| 108–1010 | Quartz sand | 25% | Ghanem et al. (2018) | ||
| PSA-HM1 phage | 108–1010 | Quartz sand | 36% | Ghanem et al. (2016) | |
| 108–1010 | Quartz sand | 80% | Ghanem et al. (2018) | ||
| T4 phage | 108–1010 | Quartz sand | 4% | Ghanem et al. (2016) | |
| 108–1010 | Quartz sand | 63% | Ghanem et al. (2018) | ||
| vB_EcoM-ep3 phage | 106 | Natural sand | 33.2–59.0% | Qin et al. (2020) | |
| 106 | Natural sand | 6.6–38.8% | Zhang et al. (2021b) | ||
| PSA-HP1 phage | 108–1010 | Quartz sand | 75% | Ghanem et al. (2016) | |
| PSA-HS2 phage | 108–1010 | Quartz sand | 63% | Ghanem et al. (2016) | |
| vB_PSPS-H6/1 phage | 108–1010 | Quartz sand | 24% | Ghanem et al. (2016) | |
| H3/49 phage | 108–1010 | Quartz sand | <1% | Ghanem et al. (2016) | |
The breakthrough percentage referred to the percentage of pathogenic microorganisms passing through columns, it was obtained by the following equation: Breakthrough percentage (%) = the total number of pathogenic microorganisms passing through columns/the total number of pathogenic microorganisms input × 100%.
Influencing factors of the transport behavior of pathogenic microorganisms in porous media. (a) biological factors; (b) physical factors; and (c) chemical factors.
Influencing factors of the transport behavior of pathogenic microorganisms in porous media. (a) biological factors; (b) physical factors; and (c) chemical factors.
Biological factors
The size of pathogenic microorganisms
The size of typical pathogenic microorganisms is protozoa (1–100 μm) > bacteria (0.1–10 μm) > viruses (18–1,500 nm) (Figure 1), and their transport abilities in porous media gradually increase with decreasing size (Hijnen et al. 2005). For example, the effluent concentrations of Giardia intestinalis, Cryptosporidium parvum, Clostridiumper fringens, and E. coli in the soil column were decreased by 3.9–6.2 log10, while that of the MS2 phage was decreased by only 3.3 log10 (Hijnen et al. 2005). Chandrasena et al. (2017) also found that the effluent concentrations of Cryptosporidium Oocysts, Clostridium perfringens, and E. coli in the stormwater biofilters were reduced by about 1.7–2 log10, while the concentration of adenoviruses was only reduced by about 1 log10. However, it has also been shown that a smaller phage phiX174 might be trapped by the narrow pores of the porous media, resulting in a lower transport ability than Bacillus subtilis endospores (Oudega et al. 2021). Therefore, the size of pathogenic microorganisms and the characteristics of porous media should be considered comprehensively to judge the transport abilities of pathogenic microorganisms.
The flagella of bacteria
The flagella are the key motor organ of bacteria, giving them the ability to smooth swim, swim backward, and execute a tumble. Flagella can promote bacterial deposition on the surface of the porous media by increasing the number of contacts between bacteria and the porous media (Zhang et al. 2021a). Bacteria with sticky flagella have a lower energy barrier with porous media and can be more closely adsorbed on the surface of porous media (Haznedaroglu et al. 2010; Zhang et al. 2021a). For example, under the ionic condition of 10 mM KCl, the breakthrough percentage of Salmonella enterica SGSC 2478 without flagella in quartz sand columns was 81%, while that of Salmonella enterica ST 5383 and SGSC 1512 with flagella was only 36 and 37%, respectively (Haznedaroglu et al. 2010). Under the ionic condition of 25 mM NaCl, the breakthrough percentage of E. coli MG1655 ΔfliC without flagella, E. coli MG1655 with normal flagella, and E. coli RP437 with sticky flagella in quartz sand columns were 85.0, 65.9, and 42.1%, respectively (Zhang et al. 2021a). In addition, a few studies have focused on the interactions between flagellated bacteria and non-flagellated bacteria in porous media. When both coexist, non-flagellated bacteria can gain transport ability by hitchhiking on flagellated bacteria (Samad et al. 2017; Balseiro-Romero et al. 2022).
The chemotaxis of bacteria
Chemotaxis refers to the biased movement of bacteria when sensing coexisting chemicals. Bacteria can move toward favorable chemicals while escaping from noxious chemicals in porous media, thus affecting their transport behavior in porous media. For example, when favorable chemicals were added to the outlet of columns, the breakthrough percentage of bacteria was significantly increased (Balseiro-Romero et al. 2022), whereas when favorable chemicals were added into porous media, two-thirds of bacteria were retained in the column (Gao et al. 2022). Wang et al. (2023) found that the breakthrough percentage of gentamicin-sensitive E. coli S17-1 in quartz sand columns increased by 13.48% when 5 μg/L gentamicin was added into the background solution due to its chemotaxis to gentamicin.
The EPS of pathogenic microorganisms
The surface of pathogenic microorganisms is easily attached to the EPS secreted by themselves. The presence of EPS can enhance the surface hydrophobicity and roughness of protozoa and bacteria to form large aggregates, thus promoting their deposition on the surface of porous media (Liu et al. 2007; Jin et al. 2021). In addition, biological clogging caused by excessive EPS accumulation can further inhibit the transport ability of pathogenic microorganisms (Kim & Kwon 2022; Zheng et al. 2024). For example, the breakthrough percentage of Dictyostelium discoideum spores decreased by 13.59% in quartz sand columns due to the existence of EPS. The increase in the content of β-sheets, which represents hydrophobic proteins in EPS components, leads to the binding between spores through hydrophobic interaction, which is the main reason for the decrease in the breakthrough percentage (Jin et al. 2021). Liu et al. (2007) found the C/C0 of the breakthrough plateau of Pseudomonas aeruginosa PDO300 (mucoid alginate-overproducing strain) was 30% lower than Pseudomonas aeruginosa PAO1 psl pel (mutant strain with a deficiency in exopolysaccharide production).
Physical factors
The porosity of porous media
With the decrease of the particle size of the porous media, the porosity of the porous media decreased, while the SSA and roughness of the media increased, providing more deposition sites for pathogenic microorganisms. Therefore, the smaller the porosity of porous media, the lower the transport ability of pathogenic microorganisms tends to be (He et al. 2020; Jin et al. 2021; Eisfeld et al. 2022). For example, the breakthrough percentage of Dictyostelium discoideum spores in quartz sand columns with porosity of 0.47 and 0.42 was 45.17 and 39.49%, respectively (Jin et al. 2021). Zhang et al. (2022) showed that when the porosity of quartz sand columns decreased from 0.424 ± 0.005 to 0.414 ± 0.003, the breakthrough percentage of Gram-negative E. coli and Gram-positive Bacillus subtilis was reduced by 13.0 and 12.7%, respectively. Zhang et al. (2021a) showed that as the porosity of quartz sand columns decreased from 0.44 to 0.39, the breakthrough percentage of E. coli MG1655, E. coli MG1655 Δflic, E. coli RP437, and E. coli RP437 fliCst decreased by 25.1–32.9%.
The surface mineral composition of porous media
Porous media in the environment are rich in types and complex in composition, and there are metal oxides, clay, and other minerals on the surface of the porous media (Guo et al. 2021a). The existence of these substances may decrease the electro-negativity of the zeta potential of the porous media, thus inhibiting the transport of pathogenic microorganisms by reducing the electrostatic repulsion between pathogenic microorganisms and porous media (Dong et al. 2014). Dong et al. (2014) found that in 20 mM NaCl solution, the breakthrough percentage of E. coli BL21 in bare quartz sand columns was 71.1%, while the breakthrough percentage in iron mineral-loaded quartz sand columns was significantly reduced to 0.27%. Zhuang & Jin (2003) showed that the addition of aluminum oxide to the quartz sand columns resulted in an obvious hysteresis of the breakthrough plateau during the transport process of ΦX174 and MS2 phages, and the C/C0 of the breakthrough plateau in the aluminum oxide-loaded quartz sand columns was lower than that in the bare quartz sand columns.
The flow rate of the water
Generally speaking, the increasing flow rate would increase hydrodynamic shear stress between the water flow and the media, which will lead to the desorption of pathogenic microorganisms attached to the porous media. Simultaneously, the high flow rate can reduce the hydraulic residence time of pathogenic microorganisms in porous media, thereby decreasing the number of collisions with the porous media. The aforementioned phenomenons together enhance the transport ability of pathogenic microorganisms (Zhang et al. 2022). For example, the breakthrough percentage of Dictyostelium discoideum spores (representative amoeba spores) in quartz sand columns increased significantly from 39.5–45.2 to 77.1–89.5% when the water flow rate increased from 0.5 to 2.5 cm/min (Jin et al. 2021). In 0.1 mM NaCl solution, when the water flow rate increased from 0.2 to 0.5 cm/min, the breakthrough percentage of Cryptosporidium parvum oocysts in quartz sand columns increased from 50.6 to 68.7% (Kim et al. 2010). Wang et al. (2023) found that when the flow rate increased from 0.07 to 0.28 cm/min, the breakthrough percentage of antibiotic-resistant E. coli and antibiotic-sensitive E. coli in quartz sand columns increased from 42.66–43.71 to 70.49–71.06%. Walshe et al. (2010) also showed that the breakthrough percentage of MS2 phage in gravel columns containing kaoline increased with the increase of flow rate, which increased from 1–2 to 7–16% when the flow rate increased from 1.6 to 3.1 cm/min.
The saturation of the water
Compared with saturated porous media, unsaturated porous media are more likely to cause bacteria and viruses to deposit on the surface of the porous media due to the existence of air–water interfaces or solid–water interfaces, thus reducing their transport abilities (Abit et al. 2012). Madumathi et al. (2017) showed that the C/C0 of the breakthrough plateau of E. coli BL21 in quartz sand columns decreased from 68% under saturated conditions to 46% under unsaturated conditions. Other studies showed that E. coli phages have a lower transport ability in unsaturated quartz sand mainly because of the presence of solid–water interfaces in porous media (Qin et al. 2020; Zhang et al. 2021b). The decrease of water saturation in porous media led to the decrease of water film thickness on the surface of the media, which increased the possibility of collisions between E. coli phages and porous media and made it easier to deposit on the surface of the media (Zhang et al. 2021b). However, Bai et al. (2016) and Bai & Lamy (2021) obtained opposite results. The transport abilities of E. coli, Klebsiella sp., and Rhodococcus rhodochrous in saturated and unsaturated media were similar, and unsaturated porous media was even beneficial for the transport of bacteria. That was probably caused by the loss of adsorption sites in part of the unsaturated zones, thus offsetting or even exceeding the inhibition of the air–water interface on the transport of bacteria.
The temperature of the water
Temperature may affect the transport ability of pathogenic microorganisms by influencing their growth states, activity, and surface properties (Kim & Walker 2009; Birgander et al. 2018). Kim & Walker (2009) found that E. coli D21g and XL1-Blue had the weakest transport ability at 10°C compared with 5 and 25°C. Sarkar et al. (1994) showed that compared with 25 °C, Bacillus Liceniformis JF-2 had lower Brownian motion at 4 °C and was more likely to form larger cell clusters, resulting in lower transport ability. Sasidharan et al. (2017) showed that in 10 mM NaCl solution, with the temperature rising from 4 to 20°C, the C/C0 of the breakthrough plateau of PRD1 and ΦX174 viruses decreased by 1 log10. At present, the effect of temperature on the transport behavior of pathogenic microorganisms is still inconclusive, and the differences in the above studies may be caused by the differences in different types of pathogenic microorganisms.
Chemical factors
The pH value of the water
The pH value can affect the transport ability of pathogenic microorganisms by influencing the zeta potential of the surface of pathogenic microorganisms and porous media. Under natural conditions, the surface of pathogenic microorganisms and porous media are negatively charged. With the increase of pH value, the negative charge on the surface of pathogenic microorganisms and porous media increases, and the electrostatic repulsion between them gradually increases, resulting in the gradual enhancement of the transport ability of pathogenic microorganisms (Mohanram et al. 2010; He et al. 2019). For example, as the pH value increased from 3 to 9, the breakthrough percentage of Cryptosporidium parvum oocysts in the Drummer soil columns increased by 63% (Mohanram et al. 2010). Suliman et al. (2017) reported that as the pH value increased from 2.0 to 8.0, the negative zeta potential of E. coli pathogenic O157:H7 and E. coli nonpathogenic K12 increased by 15.4 and 68.7 eV, respectively, and the increase of electrostatic repulsion between bacteria and porous media promoted their transport. Zhang et al. (2021b) reported that the breakthrough percentage of E. coli phages in quartz sand columns (particle size in 0.425 mm) at pH 5.0, 7.4, and 9.0 was 6.52, 11.36, and 38.78%, respectively. In addition, pH value may also affect the transport ability of E. coli phages by affecting their stability. In the coarse sand column, when the pH value was neutral, the number of collisions between E. coli phages increased, resulting in the formation of aggregates that increased their particle sizes, ultimately reducing their breakthrough percentage (Zhang et al. 2021b).
The ionic strength and species of the water
According to the classical Derjagin-Landau-Verwey-Overbeek (DLVO) theory, with the increase of ionic strength, the double electric layer on pathogenic microorganisms and porous media surface will be compressed, thereby reducing the energy barrier of interaction and ultimately increasing the deposition of pathogenic microorganisms on the porous media surface (Walshe et al. 2010; He et al. 2019; Zhang et al. 2021a). For example, in quartz sand columns at a flow rate of 0.2 cm/min, the breakthrough percentage of Cryptosporidium parvum oocysts under NaCl concentrations of 0.1, 1, and 100 mM were 50.6, 26.2, and 1.1%, respectively (Kim et al. 2010). He et al. (2019) reported that in saturated quartz sand columns, when NaCl concentration increased from 10 to 25 mM, the breakthrough percentage of Gram-negative E. coli BL21 decreased from 73.9 to 54.0%. Walshe et al. (2010) demonstrated that the breakthrough percentage of MS2 phage gradually decreased from 31 to 20% when CaCl2 concentration increased from 0 to 0.72 mM. However, studies on Dictyostelium discoideum spores had an opposite conclusion (Jin et al. 2021, 2022). When KCl concentration increased from 1 to 100 mM, the breakthrough percentage of Dictyostelium discoideum spores in quartz sand columns increased from 21.4–33.4 to 78.6–83.2%. It might be because the EPS surrounding Dictyostelium discoideum spores might shrink and form a more condensed outer layer under high ionic strength conditions due to compression of the electrical double layer, thereby reducing the deposition of Dictyostelium discoideum spores on the surface of the media (Jin et al. 2021).
Compared with monovalent cations, multivalent cations have a stronger ability to neutralize the negative charges on the surface of pathogenic microorganisms and porous media due to the cationic bridges, which are more likely to cause the deposition of bacteria and viruses on the surface of porous media (Zhang et al. 2021b). For example, the breakthrough percentage of E. coli MG1655 was 69.5% in 1 mM CaCl2 solution, which was significantly lower than the breakthrough percentage of 80.5% in 5 mM NaCl (Zhang et al. 2021a). He et al. (2019) reported that the breakthrough percentage of Gram-negative E. coli BL21 in 5 mM CaCl2 solution was significantly lower than that in 10 mM NaCl solution. This might be because the negative zeta potential of porous media in 5 mM CaCl2 solution (−21.90 ± 1.00 eV) was less than that in 10 mM NaCl solution (−35.48 ± 2.01 eV). Zhang et al. (2021b) reported that under the ionic condition of 10 mM CaCl2 or 10 mM NaCl, the breakthrough percentage of E. coli phage was lower in CaCl2 solution.
DOM in the water
The presence of DOM such as amino acid, lipid, protein, and humic acid can promote the transport of pathogenic microorganisms by competing with them for adsorption sites on porous media (Abudalo et al. 2010; Aiken et al. 2011; Zhou & Cheng 2018). Abudalo et al. (2010) found that the breakthrough percentage of Cryptosporidium parvum oocysts increased by 66% in quartz sand columns treated with fulvic acid compared with no treatment. The C/C0 of the breakthrough plateau of Rhodococcus sp. QL2 and E. coli BL21 in quartz sand columns pretreated with Suwannee River humic acid increased by 40 and 20%, respectively (Yang et al. 2012a). Weaver et al. (2013) showed that the breakthrough percentage of E. coli J6-2 in quartz sand columns pretreated with DOM of wastewater source was increased by 69.5% compared with the untreated group. Walshe et al. (2010) showed that as the pretreatment concentration of fulvic acid increased from 0.1 to 30 mg/L, the breakthrough percentage of MS2 phage in aquifer sand columns increased from 26–31 to 61–67%.
INFLUENCING FACTORS OF BIOCHAR INHIBITING THE TRANSPORT OF PATHOGENIC MICROORGANISMS
The ability of biochar to inhibit the transport of pathogenic microorganisms
| Pathogenic microorganism | Raw material | Pyrolysis temperature (oC) | Particle size (mm) | Inhibition efficiency | Reference | |
|---|---|---|---|---|---|---|
| Bacterium (CFU/mL) | E. coli | Pine chip | 350, 700 | / | 15–58% | Abit et al. (2012) |
| Forestry wood | 700 | / | 52.9–62.9% | Lau et al. (2017) | ||
| Softwood | 550–600 | 0.425 | 0.2–2.3 log10 | Bolster (2019) | ||
| Hardwood | / | 1.4, 2.8, 5 | / | Fernando Perez-Mercado et al. (2019) | ||
| Poultry litter feed stock | 300, 700 | / | −68 to 52% | Bolster & Abit (2012) | ||
| Poultry litter | 350, 700 | / | −27 to 45% | Abit et al. (2012) | ||
| E. coli (NCM 4236) | Softwood | 815–1,315 | 0.125–1 or <1 | 27.2–60.6% | Mohanty & Boehm (2014) | |
| <1 | / | Mohanty & Boehm (2015) | ||||
| Mixed plant | 180–395 | 0.595 | / | Afrooz et al. (2018) | ||
| E. coli K-12 | Wood chips | 350, 700 | / | 0.6–3.3 log10 | Mohanty et al. (2014) | |
| Pine wood, pine bark | 350, 600 | / | / | Suliman et al. (2017) | ||
| Maize straw | 300–700 | / | 2.0–4.7 log10 | Sun et al. (2019) | ||
| E. coli O157:H7 | Pine wood, pine bark | 350, 600 | / | / | Suliman et al. (2017) | |
| E. coli (ATCC® No. 8739) | Wheat straw, willow wood | 500–560 | 1–4 | −9 to −4% | Guan et al. (2020) | |
| E. coli 13706 | Plant | 450–650 | 0.06–2 | −20.7 to 55.0% | Sasidharan et al. (2016) | |
| K. pneumonia K-6 | Maize straw | 300–700 | / | 5.2–6.3 log10 | Sun et al. (2019) | |
| Corynebacterium variabile HRJ4 | Poplar sawdust, corn straw | 300, 600 | / | 2.2–45.2% | Guo et al. (2021b) | |
| Salmonella | Softwood | 550–600 | 0.425 | 0.2–4.4 log10 | Bolster (2019) | |
| Enterococcus spp. | Hardwood | / | 1.4, 2.8, 5 | / | Fernando Perez-Mercado et al. (2019) | |
| Saccharomyces cerevisiae | Hardwood | / | 1.4, 2.8, 5 | / | Fernando Perez-Mercado et al. (2019) | |
| Salmonella enterica | Mixed plant | 180–395 | 0.595 | / | Afrooz et al. (2018) | |
| Virus (PFU/mL) | MS2 phages | Mixed plant | 180–395 | 0.595 | / | Afrooz et al. (2018) |
| Hardwood | / | 1.4, 2.8, 5 | / | Fernando Perez-Mercado et al. (2019) | ||
| ΦX174 phages | Plant | 450–650 | 0.06–2 | −71.5 to −52.3% | Sasidharan et al. (2016) | |
| Hardwood | / | 1.4, 2.8, 5 | / | Fernando Perez-Mercado et al. (2019) | ||
| F + coliphage | Mixed plant | 394 | 0.595 | / | Kranner et al. (2019) | |
| PRD1 phages | Plant | 450–650 | 0.06–2 | −87.4 to −48.6% | Sasidharan et al. (2016) | |
| Pathogenic microorganism | Raw material | Pyrolysis temperature (oC) | Particle size (mm) | Inhibition efficiency | Reference | |
|---|---|---|---|---|---|---|
| Bacterium (CFU/mL) | E. coli | Pine chip | 350, 700 | / | 15–58% | Abit et al. (2012) |
| Forestry wood | 700 | / | 52.9–62.9% | Lau et al. (2017) | ||
| Softwood | 550–600 | 0.425 | 0.2–2.3 log10 | Bolster (2019) | ||
| Hardwood | / | 1.4, 2.8, 5 | / | Fernando Perez-Mercado et al. (2019) | ||
| Poultry litter feed stock | 300, 700 | / | −68 to 52% | Bolster & Abit (2012) | ||
| Poultry litter | 350, 700 | / | −27 to 45% | Abit et al. (2012) | ||
| E. coli (NCM 4236) | Softwood | 815–1,315 | 0.125–1 or <1 | 27.2–60.6% | Mohanty & Boehm (2014) | |
| <1 | / | Mohanty & Boehm (2015) | ||||
| Mixed plant | 180–395 | 0.595 | / | Afrooz et al. (2018) | ||
| E. coli K-12 | Wood chips | 350, 700 | / | 0.6–3.3 log10 | Mohanty et al. (2014) | |
| Pine wood, pine bark | 350, 600 | / | / | Suliman et al. (2017) | ||
| Maize straw | 300–700 | / | 2.0–4.7 log10 | Sun et al. (2019) | ||
| E. coli O157:H7 | Pine wood, pine bark | 350, 600 | / | / | Suliman et al. (2017) | |
| E. coli (ATCC® No. 8739) | Wheat straw, willow wood | 500–560 | 1–4 | −9 to −4% | Guan et al. (2020) | |
| E. coli 13706 | Plant | 450–650 | 0.06–2 | −20.7 to 55.0% | Sasidharan et al. (2016) | |
| K. pneumonia K-6 | Maize straw | 300–700 | / | 5.2–6.3 log10 | Sun et al. (2019) | |
| Corynebacterium variabile HRJ4 | Poplar sawdust, corn straw | 300, 600 | / | 2.2–45.2% | Guo et al. (2021b) | |
| Salmonella | Softwood | 550–600 | 0.425 | 0.2–4.4 log10 | Bolster (2019) | |
| Enterococcus spp. | Hardwood | / | 1.4, 2.8, 5 | / | Fernando Perez-Mercado et al. (2019) | |
| Saccharomyces cerevisiae | Hardwood | / | 1.4, 2.8, 5 | / | Fernando Perez-Mercado et al. (2019) | |
| Salmonella enterica | Mixed plant | 180–395 | 0.595 | / | Afrooz et al. (2018) | |
| Virus (PFU/mL) | MS2 phages | Mixed plant | 180–395 | 0.595 | / | Afrooz et al. (2018) |
| Hardwood | / | 1.4, 2.8, 5 | / | Fernando Perez-Mercado et al. (2019) | ||
| ΦX174 phages | Plant | 450–650 | 0.06–2 | −71.5 to −52.3% | Sasidharan et al. (2016) | |
| Hardwood | / | 1.4, 2.8, 5 | / | Fernando Perez-Mercado et al. (2019) | ||
| F + coliphage | Mixed plant | 394 | 0.595 | / | Kranner et al. (2019) | |
| PRD1 phages | Plant | 450–650 | 0.06–2 | −87.4 to −48.6% | Sasidharan et al. (2016) | |
w/w, weight/weight; v/v, volume/volume. Inhibition efficiency was obtained by the following equation: Inhibition efficiency (%) = Breakthrough percentage of pathogenic microorganisms in columns without biochar – Breakthrough percentage of pathogenic microorganisms in biochar amended columns.
Influencing factors of biochar inhibiting the transport of pathogenic microorganisms in porous media.
Influencing factors of biochar inhibiting the transport of pathogenic microorganisms in porous media.
Raw materials
Raw materials such as rice straw, wood, corn stalk, sludge, livestock, and poultry manure have been widely used to produce biochar to inhibit the transport of pathogenic microorganisms in porous media (Yuan et al. 2019). Plant-derived biochar is often better than sewage sludge or manure-derived biochar in inhibiting the transport of pathogenic microorganisms due to its higher C/N ratio and larger SSA (Lei & Zhang 2013). Abit et al. (2012) showed that the breakthrough percentage of E. coli SP2BO7 and SP1HO1 in the 700 °C pine chip biochar amended sand columns with a mass ratio of 2% was 36 and 0%, respectively. However, the breakthrough percentage of these two bacteria in the poultry litter biochar amended sand columns was 60 and 23%, respectively. This might be because the abundant pores in the 5–10 μm range in pine chip biochar were very suitable for retaining bacteria through pore filling.
Pyrolysis temperature
Pyrolysis temperature is a key factor affecting the physical and chemical properties of biochar. With the increase of pyrolysis temperature, properties such as carbon content, aromaticity, pH value, ash content, SSA, and stability of biochar increase, while properties such as yield, hydrogen content, oxygen content, H/C ratio, and O/C ratio decrease (Xiao et al. 2018). High-temperature biochar has a larger SSA and roughness, and fewer negatively charged oxygen-containing functional groups (such as –COOH), so it has stronger adsorption with pathogenic microorganisms and is more conducive to inhibiting their transport (Bolster & Abit 2012; Suliman et al. 2017). For example, the SSA of 700 °C pine chip biochar was 37 m2/g higher than that of 350 °C pine chip biochar. Moreover, the breakthrough percentage of E. coli SP2BO7 and SP1HO1 in the 700 °C pine chip biochar amended sand columns with a mass ratio of 1% was 33.0 and 32.8% lower than that in the 350 °C pine chip biochar amended sand columns, respectively (Abit et al. 2012). The negative zeta potential of 700 °C cellulose biochar was reduced by 13.0 mV due to the decrease of the surface negatively charged functional groups (e.g., –COOH). Therefore, the breakthrough percentage of E. coli and Bacillus subtilis in the 700 °C cellulose biochar amended sand columns was 16.7 and 17.4% lower than that in the 400 °C cellulose biochar amended sand columns (Zhang et al. 2022). Suliman et al. (2017) found that the isoelectric point of 700°C pine biochar was 2.6 higher than that of 300°C pine biochar, which resulted in a smaller electrostatic repulsion between E. coli K12 and 700 °C pine biochar, making it easier to adsorb on the surface of 700 °C pine biochar. Guo et al. (2021b) also showed that a typical Gram-positive petroleum degradation bacteria – Corynebacterium variabile HRJ4 – was more likely to be retained in large and abundant round pores of 600°C poplar straw biochar through pore filling compared to 300°C poplar straw biochar.
Particle size
In general, the smaller the particle size of biochar, the larger the SSA, the more adsorption sites are provided, and the stronger the inhibition ability on the transport of pathogenic microorganisms (Mohanty & Boehm 2014). For example, when the size of hardwood biochar was reduced from 2.8 to 1.4 mm, the removal rates of Saccharomyces cerevisiae (simulated Cryptosporidium parvum oocysts), bacteria (E. coli and Enterococcus spp.), and bacteriophages (ΦX174 and MS2 phages) in hardwood biochar amended sand columns were increased by 0.5–0.9 log10, 0.4–2.8 log10, and 0.3–1.3 log10, respectively (Fernando Perez-Mercado et al. 2019). Another study stated that E. coli had a breakthrough percentage of 4.8 ± 1.0% in softwood biochar amended sand columns containing a particle size range of less than 125 μm, and the breakthrough percentage significantly increased to 38.2 ± 4.9% when the part of biochar with a particle size range of less than 125 μm was removed (Mohanty & Boehm 2014).
Functionalized modification
Functionalized modification can change the SSA, surface functional groups, zeta potential, and other properties of biochar, which is expected to improve the ability of biochar to inhibit the transport of pathogenic microorganisms in porous media (Chu et al. 2018; Wang et al. 2019). However, research on inhibiting the transport of pathogenic microorganisms through functionally modified biochar is still in its infancy. Sporadic studies found that H2SO4 modification can increase the SSA of biochar by increasing the micropores on the surface of biochar through oxidation. Therefore, the breakthrough percentage of E. coli decreased from 3.4% in quartz sand columns to 1.3% in H2SO4-modified biochar amended sand columns (Lau et al. 2017). Modification of positively charged arginine decreased the negative zeta potential of biochar from −19.8 ± 2.0 to −8.9 ± 3.6 mV. The results showed that the breakthrough percentage of E. coli and Bacillus subtilis in the arginine-modified biochar amended sand columns was 26.9 and 9.8% lower than that in the original biochar amended sand columns, respectively (Zhang et al. 2022).
It should be noted that most studies on the application of biochar to inhibit the transport behavior of pathogenic microorganisms are short-term laboratory-scale experiments. Therefore, the impact of long-term changes in the physical and chemical properties of biochar on the transport inhibition ability and the possible environmental risks, such as the transport and diffusion risk of broken biochar colloid itself, have not been systematically explored (Zhao & Shang 2023). In addition, to improve the application performance of biochar, a variety of functionalized modification methods have been introduced, including treatment with acid, base solutions, or reducing agents, modification with minerals and nanoparticles, and functionalization with specific functional groups. However, the chemical modifiers (or loaded components) used for functionalized modification may pose secondary pollution risks to the environment, owing to their instability from pH changes, turbulence, and aging (Tan & Yu 2023). Therefore, when considering the application of original biochar or functionalized modified biochar to inhibit the transport behavior of pathogenic microorganisms, potential environmental risks need to be considered and appropriate risk management and careful evaluation need to be carried out.
CONCLUSION
In this review article, the transport rules and influencing factors of pathogenic microorganisms in porous media were carefully reviewed, as well as the capability of biochar with different properties for inhibiting the transport of pathogenic microorganisms was summarized. The following conclusions are obtained: (1) The transport behavior of pathogenic microorganisms in porous media is affected by biological, physical, and chemical factors. To evaluate the transport risk of pathogenic microorganisms in the process of reclaimed water reuse, it is necessary to comprehensively analyze the types and characteristics of pathogenic microorganisms and diverse environmental conditions; (2) Biochar, especially plant-derived biochar, can effectively inhibit the transport of pathogenic microorganisms because of its well-developed pore structure and huge SSA. Moreover, the higher the pyrolysis temperature, the smaller the particle size, the fewer negatively charged surface functional groups, and the stronger the ability of biochar to inhibit the transport of pathogenic microorganisms; (3) Although the research on inhibiting the transport of pathogenic microorganisms through functionalized modification of biochar (such as acid modification and organic modification) is still in its infancy, preliminary studies have proved its feasibility. Appropriate risk management and careful evaluation are also essential when considering the use of biochar and functionalized modified biochar. This review article is helpful to understand the transport rules and mechanisms of pathogenic microorganisms in porous media and biochar-based remediation technology, to improve the ecological and health safety of reclaimed water reuse.
ACKNOWLEDGEMENTS
This study was supported in part by the Natural Science Foundation of Shandong Province (ZR2021QD063), the Natural Science Foundation of Hainan Province (423CXTD384), the National Natural Science Foundation of China (42207297), Key Research and Development Program of Shandong Province (2022SFGC0302), Fundamental Research Funds for the Central Universities (No. 202261071), and Qingdao Postdoctoral Application Research Project.
DATA AVAILABILITY STATEMENT
All relevant data are included in the paper or its Supplementary Information.
CONFLICT OF INTEREST
The authors declare there is no conflict.
