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  1. Membrane surface roughness promotes rapid initial cell adhesion and long term microalgal biofilm stability
    Tong CY, Derek CJC
    Environ Res, 2022 Apr 15;206:112602.
    PMID: 34968430 DOI: 10.1016/j.envres.2021.112602
    In biofilm membrane photobioreactors development, conscientious works revolving around the effect of external environment factors on microalgal biofilm growth were assessed but more comparative research about the role of carrier surfaces properties such as surface roughness is necessary. Thus, commercial polyethersulfone (PES) membranes with two different molecular-weight-cut-offs (1 kDa and 30 kDa) were selected as the main representatives of surface roughness in a 20 days long-term biofilm cultivation experiment under dynamic flow condition for the biofilm evolvement of three benthic diatoms (Amphora coffeaeformis, Cylindrotheca fusiformis and Navicula incerta). Results depicted that rougher 30 kDa PES enable higher cell attachment degree for C. fusiformis (25.85 ± 2.75 × 109 cells m-2), followed by A. coffeaeformis (11.86 ± 2.76 × 109 cells m-2) and N. incerta (10.10 ± 0.65 × 109 cells m-2). Bounded extracellular polymeric substances (bEPS) gathered were relatively higher than soluble EPS (sEPS) while bEPS accumulated at least 10% higher on smooth 1 kDa PES than rough 30 kDa PES for the purpose of enhancing the biofilm disruption resistivity under liquid flow. Moreover, cell adhesion mechanism was proposed via computational fluid dynamics in parallel with EPS analysis. Copious amount of asperities and stagnant zones present on rough 30 kDa surfaces accelerated biofilm development and the consistency of the results have a great valence for interpretation of microalgal biofilm lifestyle on porous surfaces.
  2. Marine microalgal biofilm development and its adhesion propensities on commercial membrane via XDLVO approach
    Tong CY, Derek CJC
    J Biotechnol, 2022 Dec 10;360:37-44.
    PMID: 36272576 DOI: 10.1016/j.jbiotec.2022.10.012
    An emerging biofilm immobilization method has enabled effortless biomass harvesting and promoted economic feasibility. The current limitation towards the adaptation of this technology is the inadequate understanding of the biofilm interaction towards microporous membrane. Cell adhesion is recognized as the most important step towards the immobilized cultivation of microalgae. Cell attachment kinetic was studied in a short-term batch culture of three marine diatoms, Amphora coffeaeformis, Cylindrotheca fusiformis and Navicula incerta over 96 h on submerged commercial polyvinylidene fluoride (PVDF) membrane under swirling motion of culture medium. Both the evolution of cell adhesion intensity and compositional changes of the extracellular polymeric substances (EPS) released were quantified throughout the cultivation period. To delve into the cell-substratum interactions, existing thermodynamics and colloidal extended Derjaguin, Landau, Vervey, and Overbeek (XDLVO) theory were employed. As a result, A. coffeaeformis and N. incerta recorded a higher cell colonization percentage than C. fusiformis being the lowest about 2.16±0.17% cell colonization due to their respective species-dependent EPS variation. Polysaccharide contents were at least two times higher than protein contents for both C. fusiformis and N. incerta except for A. coffeaeformis depicting a lower polysaccharide-to-protein ratio whereby the protein contents were maximized at 1.03 × 103 ± 64.14 pg m-2 cell-1 at 6th h. From the surface free energy point of view, both thermodynamics and XDLVO model elucidated that cells adhered reversibly in the secondary energy minimum and ranked C. fusiformis the lowest adhesion tendency among three. These findings establish fundamental knowledge about biofilm formation in porous substrate bioreactors.
  3. Bio-coatings as immobilized microalgae cultivation enhancement: A review
    Tong CY, Derek CJC
    Sci Total Environ, 2023 Aug 20;887:163857.
    PMID: 37149157 DOI: 10.1016/j.scitotenv.2023.163857
    Bio-coatings serve as artificial scaffolds for immobilizing microalgae to facilitate cell concentration and harvesting. It has been used as an additional step to enhance the natural microalgal biofilm cultivation and to promote new opportunities in artificially-immobilize cultivation technology of microalgae. This technique is able to enhance biomass productivities, enable energy and cost saving, water volume reduction and ease of biomass harvesting since the cells are physically isolated from the liquid medium. However, scientific discoveries of bio-coatings for process intensification are still lacking and their working principles remained unclear. Therefore, this critical review aims to shed light on the advancement of cell encapsulation systems (hydrogel coating, artificial leaf, bio-catalytic latex coating, and cellular polymeric coating) over the years and aid in the selection of appropriate bio-coating techniques for various applications. Discussion on the different preparation routes of bio-coatings, as well as the exploration towards the potential of bio-based coating materials such as natural/synthetic polymers, latex binders, and algal organic matters are also included, with a focus on sustainable pursuits. This review also presents in-depth investigations into the environmental applications of bio-coatings in wastewater remediation, air purification, carbon bio-fixation, and bio-electricity. The field of bio-coating in microalgae immobilization gives rise to a new ecofriendly strategy with scalable cultivation footprint and a balanced environmental risk aligning with the United Nation's Sustainable Development Goals with potential towards the contribution of Zero Hunger, Clean Water and Sanitation, Affordable and Clean Energy, and Responsible Consumption and Production.
  4. Novel Extrapolymeric Substances Biocoating on Polyvinylidene Fluoride Membrane for Enhanced Attached Growth of Navicula incerta
    Tong CY, Derek CJC
    Microb Ecol, 2023 Jul;86(1):549-562.
    PMID: 35978183 DOI: 10.1007/s00248-022-02091-9
    Cell adhesion is always the first step in biofilm development. With the emergence of attached cultivation systems, this study aims to promote a cost-effective approach for sustainable cultivation of microalgae, Navicula incerta, by pre-coating the main substrates, commercial polyvinylidene fluoride (PVDF) membranes with its own washed algal cells and self-produced soluble extracellular polymeric substances (EPS) for strengthened biofilm development. The effects of pH value (6 to 9), cell suspension volume (10 to 30 mL), and EPS volume (10 to 50 mL) were statistically optimized by means of response surface methodology toolkit. Model outputs revealed good agreement with cell adhesion data variation less than 1% at optimized pre-coating conditions (7.20 pH, 30 mL cell suspension volume, and 50 mL EPS volume). Throughout long-term biofilm cultivation, results demonstrated that EPS pre-coating substantially improved the attached microalgae density by as high as 271% than pristine PVDF due to rougher surface and the presence of sticky exopolymer particles. Nutrients absorbed via the available EPS coating from the bulk medium made the immobilized cells to release less polysaccharides on an average of 30% less than uncoated PVDF. This work suggests that adhesive polymer binders derived from organic sources can be effectively integrated into the development of high-performance novel materials as biocoating for immobilized microalgae cultivation.
  5. Enhancing organic matter productivity in microalgal-bacterial biofilm using novel bio-coating
    Tong CY, Honda K, Derek CJC
    Sci Total Environ, 2024 Jan 01;906:167576.
    PMID: 37804964 DOI: 10.1016/j.scitotenv.2023.167576
    Research on renewable energy from microalgae has led to a growing interest in porous substrate photobioreactors, but their widespread adoption is currently limited to pure microalgal biofilm cultures. The behavior of microalgal-bacterial biofilms immobilized on microporous substrates remains as a research challenge, particularly in uncovering their mutualistic interactions in environment enriched with dissolved organic matter. Therefore, this study established a novel culture platform by introducing microalgal-derived bio-coating that preconditioned hydrophilic polyvinylidene fluoride membranes for the microalgal-bacterial biofilm growth of freshwater microalgae, Chlorella vulgaris ESP 31 and marine microalgae, Cylindrotheca fusiformis with bacteria, Escherichia coli. In the attached co-culture mode, the bio-coating we proposed demonstrated the ability to enhance microalgal growth for both studied species by a range of 2.5 % to 19 % starting from day 10 onwards. Additionally, when compared to co-culture on uncoated membranes, the bio-coating exhibited a significant bacterial growth promotion effect, increasing bacterial growth by at least 2.35 times for the C. vulgaris-E. coli co-culture after an initial adaptation phase. A significant increase of at least 72 % in intracellular biochemical compounds (including chlorophyll, polysaccharides, proteins, and lipids) was observed within just five days, primarily due to the high concentration of pre-coated organic matter, mainly sourced from the internal organic matter (IOM) of C. fusiformis. Higher accumulation of organic compounds in the bio-coating indirectly triggers a competition between microalgae and bacteria which potentially stimulate the production of additional intra-/extra-organic substances as a defensive response. In short, insight gained from this study may represent a paradigm shift in the ways that symbiotic interactions are promoted to increase the yield of specific bio-compounds with the presence of bio-coating.
  6. A review on microalgal-bacterial co-culture: The multifaceted role of beneficial bacteria towards enhancement of microalgal metabolite production
    Tong CY, Honda K, Derek CJC
    Environ Res, 2023 Jul 01;228:115872.
    PMID: 37054838 DOI: 10.1016/j.envres.2023.115872
    Mass microalgal-bacterial co-cultures have come to the fore of applied physiological research, in particularly for the optimization of high-value metabolite from microalgae. These co-cultures rely on the existence of a phycosphere which harbors unique cross-kingdom associations that are a prerequisite for the cooperative interactions. However, detailed mechanisms underpinning the beneficial bacterial effects onto microalgal growth and metabolic production are rather limited at the moment. Hence, the main purpose of this review is to shed light on how bacteria fuels microalgal metabolism or vice versa during mutualistic interactions, building upon the phycosphere which is a hotspot for chemical exchange. Nutrients exchange and signal transduction between two not only increase the algal productivity, but also facilitate in the degradation of bio-products and elevate the host defense ability. Main chemical mediators such as photosynthetic oxygen, N-acyl-homoserine lactone, siderophore and vitamin B12 were identified to elucidate beneficial cascading effects from the bacteria towards microalgal metabolites. In terms of applications, the enhancement of soluble microalgal metabolites is often associated with bacteria-mediated cell autolysis while bacterial bio-flocculants can aid in microalgal biomass harvesting. In addition, this review goes in depth into the discussion on enzyme-based communication via metabolic engineering such as gene modification, cellular metabolic pathway fine-tuning, over expression of target enzymes, and diversion of flux toward key metabolites. Furthermore, possible challenges and recommendations aimed at stimulating microalgal metabolite production are outlined. As more evidence emerges regarding the multifaceted role of beneficial bacteria, it will be crucial to incorporate these findings into the development of algal biotechnology.
  7. Microalgal extract as bio-coating to enhance biofilm growth of marine microalgae on microporous membranes
    Tong CY, Chua MX, Tan WH, Derek CJC
    Chemosphere, 2023 Feb;315:137712.
    PMID: 36592830 DOI: 10.1016/j.chemosphere.2022.137712
    Microalgal biofilm is a popular platform for algal production, nutrient removal and carbon capture; however, it suffers from significant biofilm exfoliation under shear force exposure. Hence, a biologically-safe coating made up of algal extracellular polymeric substances (EPS) was utilized to secure the biofilm cell retention and cell loading on commercial microporous membrane (polyvinylidene fluoride), making the surfaces more hydrophobic (contact angle increase up to 12°). Results demonstrated that initial cell adhesion of three marine microalgae (Amphora coffeaeformis, Cylindrotheca fusiformis and Navicula incerta) was enhanced by at least 1.3 times higher than that of pristine control within only seven days with minimized biofilm exfoliation issue due to uniform distribution of sticky transparent exopolymer particles. Bounded extracellular polysaccharide gathered was approximately 23% higher on EPS-coated membranes to improve the biofilm's hydraulic resistance, whereas bounded extracellular protein would only be substantially elevated after the attached cells re-accommodate themselves onto the EPS pre-coating of themselves. In accounting the rises of hydrophobic protein content, biofilm was believed to be more stabilized, presumably via hydrophobic interactions. EPS biocoating would generate a groundswell of interest for bioprocess intensifications though there are lots of inherent technical and molecular challenges to be further investigated in future.
  8. Bio-coatings in permeated cultivation systems: Unprecedented impacts on microalgal monoculture growth and organic matter yield
    Tong CY, Kee CY, Honda K, Derek CJC
    Environ Res, 2023 Dec 15;239(Pt 2):117403.
    PMID: 37848079 DOI: 10.1016/j.envres.2023.117403
    Bio-coating, a recent and promising approach in attached microalgal cultivation systems, has garnered attention due to its efficiency in enhancing immobilized algal growth, particularly in submerged cultivation systems. However, when the cells are cultured on thin solid microporous substrates that physically separate them from the nutrient medium, it remains unclear whether the applied bio-coatings still have a significant impact on algal growth or the subsequent rates of algal organic matter (AOM) release. Therefore, this current work investigated the role of bio-coatings on the microalgal monoculture growth of one freshwater species, Chlorella vulgaris ESP 31, and one marine species, Cylindrotheca fusiformis on a hydrophilic substrate, polyvinylidene fluoride membrane in a permeated cultivation system. Wide range of bio-coating sources were adapted, with the result demonstrating that bacteria-derived coating promoted algal growth by as high as 140% when compared with the control group for both species. Interestingly, two distinct adaptation mechanisms were observed between the species, with only C. fusiformis demonstrating a positive correlation between cell growth and AOM productivity, particularly in its extracellularly bound fractions. It is worth noting that despite this specific fraction exhibiting the lowest content among all; it displayed significant relevance in terms of AOM productivity. High extracellular protein-to-polysaccharide ratio (>5.7 fold) quantified on bacterial intracellular exudate-coated membranes indirectly revealed an underlying symbiotic microalgal-bacterial interaction. This is the first study showing how bio-coating influenced AOM yield without any physical interaction between microalgae and bacteria. It further confirms the practical benefits of bio-coating in attached cultivation systems.
  9. A microscale system for in situ investigation of immobilized microalgal cell resistance against liquid flow in the early inoculation stage
    Tong CY, Li HZ, Derek CJC
    Lab Chip, 2023 Sep 13;23(18):4052-4066.
    PMID: 37609763 DOI: 10.1039/d3lc00415e
    In attached microalgae cultivation systems, cell detachment due to fluid hydrodynamic flow is not a subject matter that is commonly looked into. However, this phenomenon is of great relevance to optimizing the operating parameters of algae cultivation and feasible reactor design. Hence, this current work miniaturizes traditional benchtop assays into a microfluidic platform to study the cell detachment of green microalgae, Chlorella vulgaris, from porous substrates during its early cultivation stage under precisely controlled conditions. As revealed by time lapse microscopy, an increase in bulk flow velocity facilitated nutrient transport but also triggered cell detachment events. At a flow rate of 1000 μL min-1 of growth medium for 120 min, the algal cell coverage was up to 5% lower than those at 5 μL min-1 and 50 μL min-1. In static seeding, the evolution of attached cell resistance toward liquid flows was dependent on hydrodynamic zones. The center zone of the microchannel was shown to be a "comfortable zone" of the attached cells to sequester nutrients effectively at lower medium flow rates but there was a profile transition where outlet zones favored cell attachment the most at higher flow rates (1.13 times higher than the center zone for 1000 μL min-1). Besides, computational fluid dynamics (CFD) simulations illustrated that the focusing band varied between cross-sections and depths, while the streamline was the least concentrated along the side walls and bottom plane of the microfluidic devices. It was intriguing to learn that cell detachment was not primarily happening along the symmetry streamline. Insight gained from this study could be further applied in the optimization of operating conditions of attached cultivation systems whilst preserving laminar flow conditions.
  10. Fulltext Uncovering the role of algal organic matter biocoating on Navicula incerta cell deposition and biofilm formation
    Tong CY, Lim SL, Chua MX, Derek CJC
    Bioengineered, 2023 Dec;14(1):2252213.
    PMID: 37695682 DOI: 10.1080/21655979.2023.2252213
    Spontaneous natural biofilm concentrates microalgal biomass on solid supports. However, the biofilm is frequently susceptible to exfoliation upon nutrient deficiency, particularly found in aged biofilm. Therefore, this study highlights a novel biofilm cultivation technique by pre-depositing the algal organic matters from marine diatom, Navicula incerta onto microporous polyvinylidene fluoride membrane to further strengthen the biofilm developed. Due to the improvement in membrane surface roughness and hydrophobicity, cells adhered most abundantly to soluble extrapolymeric substances-coated (sEPS) (76×106±16×106 cells m-2), followed by bounded EPS-coated (57.67×106±0.33×106 cells m-2), internally organic matter (IOM)-coated (39.00×106±5.19×106 cells m-2), and pristine control the least (6.22×106±0.77×106 cells m-2) at 24th h. Surprisingly, only bEPS-coated membrane demonstrated an increase in cell adhesion toward the end of the experiment at 72 h. The application of the bio-coating has successfully increased the rate of cell attachment by at least 45.3% upon inoculation and achieved as high as 89.9% faster attachment at 72 hours compared to the pristine control group. Soluble polysaccharides and proteins might be carried along by the cells adhering onto membranes hence resulting in a built up of EPS hydrophobicity (>70% in average on bio-coated membranes) over time as compared with pristine (control) that only recorded an average of approximately 50% hydrophobicity. Interestingly, cells grown on bio-coated membranes accumulated more internally bounded polysaccharides, though bio-coating had no discernible impact on the production of both externally and internally bounded protein. The collective findings of this study reveal the physiological alterations of microalgal biofilms cultured on bio-coated membranes.
  11. KEIO knockout collection reveals metabolomic crosstalk in Chlorella spp.-Escherichia coli co-cultures
    Tong CY, Tomita H, Miyazaki K, Derek CJC, Honda K
    J Phycol, 2025 Mar 12.
    PMID: 40074247 DOI: 10.1111/jpy.70001
    The interdependence between microalgae and bacteria has sparked scientific interest over years, primarily driven by the practical applications of microalgal-bacteria consortia in wastewater treatment and algal biofuel production. Although adequate studies have focused on the broad interactions and general behavior between the two entities, there remains a scarcity of study on the metabolic role of symbiotic bacteria in promoting microalgal growth. Here, we use the KEIO Knockout Collection, an Escherichia coli gene knockout mutant library, to systematically screen for genes involved in the interdependence of Chlorella sorokiniana and E. coli. By co-cultivating C. sorokiniana and E. coli knockout mutants in 96-well microplates (200 μL medium per well) under white light at 25°C, 31 potential algal growth-promoting and 56 growth-inhibiting genes out of 3985 genes were identified that enhanced (≥1.25-fold) and diminished (≤0.8-fold) the production of algal chlorophyll-a content, respectively. Kyoto Encyclopedia of Genes and Genomes (KEGG) mapping of these growth-regulating genes suggested a metabolic symbiosis involving bacteria-derived cobalamin (cobU, cobC), biotin (bioB, bioF, bioC, bioD, fabF, fabH), riboflavin (fbp, guaB, gnd, guaA, zwf, purA), and 2,3-butanediol (fumB, adhE, mdh, frdB, pta, sdhC). The effects of these metabolites were further validated by supplementing the agents into the axenic algal cultures; Dose-dependent trends were observed for each metabolite, with a maximum four-fold increase in algal biomass productivity over the control. The specific growth rate of algae was increased by ≥1.27-fold and doubling time was shortened by ≥22.5%. The present results, obtained through genome-wide analyses of interdependence between microalgae and bacteria, reveals multiple interactions between organisms via metabolites.
  12. Fulltext Lacertus Syndrome: an Outcome Analysis After Lacertus Release
    Ahmad AA, Abdullah S, Thavamany AS, Tong CY, Ganapathy SS
    J Hand Surg Glob Online, 2023 Jul;5(4):498-502.
    PMID: 37521562 DOI: 10.1016/j.jhsg.2023.03.001
    PURPOSE: The lacertus fibrosus or bicipital aponeurosis is a sheet of ligamentous tissue just distal to the elbow joint and can be a compression point for the median nerve. Essentially, lacertus syndrome is a subset of pronator syndrome and an uncommon diagnosis by itself. Surgical release of the lacertus consists of a small 2-cm incision that can be performed under local anesthesia. This study aimed to evaluate the outcome of lacertus release in resolving median nerve symptoms.

    METHODS: This retrospective study was performed at Prince Court Medical Centre, Kuala Lumpur, Malaysia, from January 2020 until June 2021. Ninety-three patients who presented with numbness of fingers, hand, or upper limb; forearm pain; and muscle weakness. They were diagnosed with lacertus syndrome on the basis of local tenderness at the lacertus fibrosus with either weakness of flexor pollicis longus and flexor digitorum profundus of the index finger or paresthesia over the thenar eminence. The patients underwent 3 months of hand therapy, and those with no symptom improvement were offered lacertus release performed by a single surgeon. The surgical technique consists of a surgical incision starting from a point 2 cm distally and 2 cm radially to the medial epicondyle. The incision projects 2 cm distally in an oblique fashion toward the radial styloid. A wide-awake local anesthesia no tourniquet (WALANT) technqiue was utilized and 20 mL of local anesthesic was injected subcutaneously around this region at least 20 minutes before the surgery. Careful dissection was made subcutaneously, and the lacertus fibrosus was identified as a thickened, shiny white structure and released. The Quick Disabilities of the Arm, Shoulder, and Hand (QuickDASH) score, grip strength, and pinch strength were tested before and after surgery. At 6 months after surgery, the QuickDASH score was again assessed with a WALANT satisfactory questionnaire.

    RESULTS: A total of 93 patients were included in the study. The mean age of the patients was 38.7 years, and most were women (77.4%). The mean operating time was 70 minutes. The mean preoperative QuickDASH score was 53, which significantly reduced immediately after surgery to 7.8 (P < .001) and remained low at 6 months after surgery (10.6). The mean grip strength showed a significant increase from a preoperative mean of 16 kg to a postoperative mean of 24 kg (P < .001). Pinch strength also significantly increased from a preoperative mean of 9 kg to 13 kg after surgery (P < .001).

    CONCLUSIONS: Lacertus syndrome remains an underdiagnosed disease that can be treated efficiently with a directed minimal surgical incision under wide-awake local anesthesia. Lacertus release appears to significantly reduce pain and numbness with markedly improved hand grip and pinch strength. The corresponding QuickDASH scores also improved significantly after surgery. This study is vital to our understanding of proximal median nerve entrapment and to accurately diagnose it.

    TYPE OF STUDY/LEVEL OF EVIDENCE: Therapeutic III.

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