Reducing the Impacts of Biofouling in RO Membrane Systems through In Situ Low Fluence Irradiation Employing UVC-LEDs
Abstract
:1. Introduction
- Adaption of the equipment, design and operation, such as suitable pretreatment (e.g., ultrafiltration), optimizing hydrodynamic conditions, membrane surface modifications or feed flow reversal,
- Limitation of the biomass growth conditions by limiting essential resources, such as carbon or phosphorus,
2. Materials and Methods
2.1. UV Reactor and Laboratory Skid for Biofouling Experiments
2.2. Accelerated Biofouling Experiments
- Cleaning and sterilization: Membranes were stored at 4 °C in 1% NaHSO3 (Acros Organics, Geel, Belgium) until used [71]. The cleaning of the system included flushing with 0.1% NaOH (Merck, Darmstadt, Germany) to remove organic matter [71]. Sterilization was done by autoclaving at 121 °C for 20 min or soaking in 0.25% H2O2 solution (Merck, Darmstadt, Germany), analogous to [71,72,73,74,75].
- Reassembling of the skid: After cleaning and sterilization, the skid was reassembled under sterile conditions.
- Compaction: Before starting each biofouling experiment, a 16-h compaction, using an NaCl solution (Appli Chem, Darmstadt, Germany), was performed and the flux was set to 20 L∙m−2∙h−1 (LMH). Depending on the initial membrane permeability, the feed pressure varied between 3.5 and 6 bar. The crossflow through the MFS is maintained at 4.25 L∙h−1 resulting in an empty channel velocity of 0.116 m∙s−1.
- Accelerated biofouling phase: Biofouling experiments were performed by using tap water as feed with nutrient dosing to reach a target concentration of 1000:200:100 μg∙L−1 of C:N:P [40]. Temperature was maintained at 15 °C and feed pressure (set in compaction) was kept constant. When an FCPD of 0.8 bar was reached, the experiments were terminated.
2.3. Biofilm Extraction and Analysis
2.4. Analytical Methods
- Total organic carbon (TOC) was analyzed as a non-purgeable organic carbon using the Vario TOC cube analyzer (Elementar Analysensyteme, Langenselbold, Germany) [79]. Biofilm samples were diluted 1:50 prior to analysis.
- ATP was measured using the BacTiter-Glow assay (Promega, Walldorf, Germany). The manufacturer’s guideline [80] was followed using flat white 96 multiwell plates (Thermo Scientific, Langenselbold, Germany) and the Tecan Infinite M Plex reader (Männedorf, Switzerland). ATP standards were prepared using adenosine 5′-triphosphat disodium salt (Sigma-Aldrich Chemie, Taufkirchen, Germany). As inner filter effects were observed during ATP analysis, each sample was diluted 1:5, 1:10 and 1:20. The luminescence signal was interpolated to an undiluted state and converted to ATP concentrations with the standard curve.
- Total direct cell counts (TDC) was performed following the procedure of Boulos et al. [81] using the LIVE/DEAD BacLight kit (Thermo Scientific, Langenselbold, Germany). For filtration, the 0.22 µm black polycarbonate filter manufactured by Piper Filter (Bad Zwischenahn, Germany) were utilized. With this kit, it is possible to differentiate cells with intact and damaged cell membrane [81]. Images were taken using the Axioplan 2 imaging employing the Axiocam 503 color camera (Zeiss, Oberkochen, Germany). Cell counting was performed using the Matlab Version (R2018b, Mathworks, Natick, MA, USA) of the CellC software v. 1.2 [79].
- Protein analysis was done using the modified Lowry protein assay kit (Thermo Scientific, Langenselbold, Germany). Transparent 96 well flat transparent microplates (Greiner Bio-One, Frickenhausen, Germany) were used with the Infinite M Plex reader (Tecan, Männedorf, Switzerland). The protein standard curve was prepared using bovine serum albumin (Thermo Scientific, Waltham, MA, USA).
- Polysaccharides were quantified using the method described by Masuko et al. [82]. Concentrated sulfuric acid was purchased from Merck (Darmstadt, Germany) and phenol from Sigma Aldrich (St. Louis, MO, USA). Standards were prepared using d-(+)-glucose (Alfa Aesar by Thermo Fisher Scientific, Kandel, Germany). The same multiwell plates and reader as for proteins were utilized.
- Fluorescence spectroscopy was performed using the Aqualog (HORIBA Jobin Yvon, Bensheim, Germany). Two different kinds of samples were analyzed: once the biofilm sample filtered by 0.45 µm (VWR, Radnor, PA, USA) and the EPS sample unfiltered. Both samples were diluted 1:20 to reduce inner filter effects. Instrument settings are summarized in the Supplementary Materials [68]. QS high precision cell made of quartz SUPRASIL by Hellma (Müllheim, Germany) was utilized as cuvette.
- For 16S rRNA amplicon sequencing, 1.5 mL of sample was freeze dried, resuspended in 50 µL nuclease-free water (Promega, Walldorf, Germany) and DNA was extracted using the DNeasy PowerSoil kit (Qiagen, Hilden, Germany). The rRNA sequencing was performed by ZIEL—Institute for Food & Health (Freising, Germany) using the primers 341F/806R and a MiSeq Reagent Kit v3 on an Illumina MiSeq benchtop sequencer (Illumina, San Diego, CA, USA). Raw reads were uploaded to the European Nucleotide Archive (ENA) database (PRJEB41202 (ERP124942)).
2.5. Summary of the Performed Biofouling Experiments
2.6. Actinometry
2.7. Data Analysis
3. Results and Discussion
3.1. Characterization of the UVC-LED Reactor
3.2. Impact of UVC Pretreatment on the Biofilm Formation and Hydraulic Resistance
- Reduction of viable bacteria in the feed: UV disinfection using UVC light is a process known for its capability to inactivate microorganisms [45,46,47,48]. Inactivation was observed in studies investigating the potential of UV pretreatment for biofouling control [58,60,61]. Li et al. [115] reported that during UV disinfection of Escherichia coli, irradiation using a 278 nm wavelength LED inhibited photoreactivation and dark repair, probably caused by impairment of protein activities.
- Changed adhesion properties: RO membranes are commonly negatively charged and rather hydrophobic at pH 7 and becoming more hydrophilic with increasing ion concentrations [116]. During UVA disinfection a depolarization of the cells’ membrane potential was observed [56]. Similar effects are assumed to happen while using 278 nm UV-LEDs, with potential effects on the proteins of the cells [115]. On the one hand, a reduction in cell membrane potential would lead to a lower electric repulsion with the membrane which could lead to better adhesion. On the other hand, according to Otto and Silhavy [117], the outer membrane lipoprotein NlpE is required for activation of the cpxR system and a successful attachment of cells to hydrophobic surfaces. In case the NlpE protein of the cell membrane is damaged due to the UV treatment, it could possibly lead to a reduced adhesion. However, the CpxRA system is complex and can be affected by multiple causes [118,119]. Whereas Kolappan and Satheesh [62] observed a reduced attachment of Alteromonas sp. cells to hard surfaces due to UV treatment, Friedman et al. [120] rather linked a reduced viable cell count to a reduced cell abundance on surfaces within their experiments.
3.3. Membrane Autopsy and Biofilm Analysis
3.4. Fluorescence Spectroscopy and PARAFAC Modeling
3.5. 16S rRNA Amplicon Sequencing
3.6. Correlation of Hydraulic Resistance to the Main Biofilm Attributes
- Different quantity in EPS production: As reported in the literature [40,122], polysaccharides and proteins are linked to hydraulic resistance. Even though no significant change for EPS content of treated and untreated biofilms could be revealed, a consistent trend for a reduced average in EPS and TOC quantities for the UV pretreated biofilm could be seen (11, 8, 14 and 19% for TOC, TOCEPS, Proteins and Polysaccharides, respectively). A significant difference in EPS quantity could probably not be detected due to the low number of replicates (n = 6) or because there exists an interplay among those parameters, making a simple comparison difficult.
- Changed EPS composition/quality and biofilm morphology due to changed biodiversity: UV pretreatment seems to alter the microbial community present in biofilms. Interestingly, the genera that showed a significantly differential abundance did not correlate with the biofilm resistance. Furthermore, within the PARAFAC analysis, at least no differences for expression of tyrosine- or tryptophan-like proteins was found. Still, a change in the microbial community could lead to different EPS quality [20]. A difference in EPS composition could also be polysaccharide-related or not be detected with fluorescence measurements.
- Reduced ATP levels impact quorum sensing or vice versa: The ATP/TDClive ratio correlates with the hydraulic resistance and seems to be changed by the UV treatment. Still the cause for a reduced ATP level and the effects for the biofilm resistance are not clear. Yang et al. [135] observed an ATP reduction over time for UV-irradiated bacteria, especially for medium pressure UV lamps. Thus, cells irradiated and subsequently adhered to the biofilm could exhibit lower ATP levels. Furthermore, different kinds of microorganisms could show different levels of ATP [136]. Jiang and Liu [137] recognized that if ATP production is limited in aerobic granules, the amount of AHL messenger molecules and EPS is reduced. Vice versa, Zhang et al. [138] showed in their study that with increasing concentration of quorum sensing molecules (AHLs), ATP levels rose. The reduced ATP levels in the UV treated biofilms could, therefore, indicate less quorum sensing. Additionally, Zhang et al. [138] observed that ATP needs to be present in a sufficient amount for EPS production. A reduction of quorum sensing could also be caused by an altered microbial community [39,138,139]. Not only microorganisms showing increased AHL production could show a changed abundance, but also those quenching AHL signals. According to the review of Uroz et al. [39], Delftia acidovorans [140], Ralstonia sp.XJ12B [141] and Sphingomonas [142] could degrade or modify AHL signal molecules. Whereas a Delftia strain was found with reduced abundance in the UV treated biofilms, the Ralstonia and Sphingomonas strains were increased. Unfortunately, in this study, it was beyond the scope to directly elucidate how the AHL concentration affects the ATP levels. Nevertheless, AHL expression might not only impact the quantity of EPS but also correlate with the production of tightly and loosely bound EPS [139]. This could possibly affect the resistance of the formed biofilm.
- Introduction of prophage: Stress conditions, such as DNA damage, are known to lead to prophage induction to biofilms, which can further lead to biofilm dispersal or disruption [118,143]. Biofilm dispersal could not only lead to a delayed build-up but also create a more open structure, leading to lower resistance.
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Parameter | Biofilm Property |
---|---|
TOC/TOCEPS | Total organic mass/Total EPS |
ATP | Active biomass [78] [15] (p. 26) |
Total direct cell counts (TDC) | Dead and living cells |
Proteins and polysaccharides | EPS composition |
Excitation emission matrix (EEM) using fluorescence spectroscopy | Differentiation tyrosine- and tryptophan-like proteins |
16S rRNA amplicon sequencing | Microbial community composition |
Experiment No. | Line with UV Treatment | UV Dummy 1 | LED Current [mA] | Membrane Performance Data | Biofilm Analysis |
---|---|---|---|---|---|
1 | 1 | Yes | 360 | Yes | 16S |
2 | 1 | Yes | 360 | Yes | All |
3 | 2 | Yes | 360 | No | All |
4 | 1 | No | 360 | Yes | All |
5 | 2 | No | 360 | Yes | All |
6 | 2 | No | 360 | Yes | All |
7 | 1 | No | 360 | Yes, intermittent permeate production | All |
8 | 1 | No | 180 | Yes | No |
FCPD Delay | FCPD Delay | Difference Hydraulic Resistance | Difference Hydraulic Resistance | |
---|---|---|---|---|
Mean | 2.0 d | 16.5% | 3.4 1013 m−1 | 48.8% |
95% confidence-t interval | 1.0 d | 10.0% | 2.7 1013 m-1 | 34.9% |
p-value one sided Wilcoxon signed-rank test | 0.016 *1 | 0.016 *1 | 0.031 *2 | 0.031 *2 |
Wilcoxon test statistic W | 21 *1 | 21 *1 | 1 *2 | 1 *2 |
ASV | Family | Genus | Base Mean | Log 2 Fold Change | p Adjusted | Abundance |
---|---|---|---|---|---|---|
45 | Sphingomonadaceae | Novosphingobium | 139 | 25.8 | 8 × 10−17 | ↑ |
46 | Comamonadaceae | Delftia | 101 | −24.8 | 7 × 10−16 | ↓ |
2 | Comamonadaceae | Acidovorax * | 21,435 | 4.0 | 0.01 | ↑ |
60 | Sphingomonadaceae | Sphingomonas | 80 | 4.5 | 0.03 | ↑ |
4 | Burkholderiaceae | Ralstonia | 5957 | 3.5 | 0.03 | ↑ |
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Sperle, P.; Wurzbacher, C.; Drewes, J.E.; Skibinski, B. Reducing the Impacts of Biofouling in RO Membrane Systems through In Situ Low Fluence Irradiation Employing UVC-LEDs. Membranes 2020, 10, 415. https://doi.org/10.3390/membranes10120415
Sperle P, Wurzbacher C, Drewes JE, Skibinski B. Reducing the Impacts of Biofouling in RO Membrane Systems through In Situ Low Fluence Irradiation Employing UVC-LEDs. Membranes. 2020; 10(12):415. https://doi.org/10.3390/membranes10120415
Chicago/Turabian StyleSperle, Philipp, Christian Wurzbacher, Jörg E. Drewes, and Bertram Skibinski. 2020. "Reducing the Impacts of Biofouling in RO Membrane Systems through In Situ Low Fluence Irradiation Employing UVC-LEDs" Membranes 10, no. 12: 415. https://doi.org/10.3390/membranes10120415