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development and testing of a 3d-printable polylactic acid

In the present work, a remediation bioprocess based on the use of a native isolate of Chlorella vulgaris immobilized in an alginate matrix inside a polylactic acid (PLA) device is proposed. This microalga immobilized in alginate beads was previously shown to be useful for the reduction of several chemical and microbial contaminants present in the highly polluted water from the Matanza–Riachuelo watershed. However, these beads had a relatively short shelf life in the natural environment. To overcome this limitation, a 3D-printed PLA device was designed. PLA is a biocompatible and biodegradable material suitable for biotechnological applications. We used Erlenmeyers and stirred-tank bioreactors fed batch with Murashige Skoog (MS) culture medium or water from the Cildáñez stream (one of the water bodies of the aforementioned watershed) to estimate the growth kinetics parameters and the bioremediation capacity of immobilized-microalgal cells as an unconfined system (UcS) or a confined system (CfS) inside PLA devices on Cildáñez water. Although alga’s growth parameters were maximum in the UcS fed with MS medium as substrate, successful bioremediation of the target water was possible using the CfS: all inorganic nitrogen forms and total phosphorus were reduced at least by 90% after 5 days of bioprocess in an agitated bioreactor, whereas aerobic mesophilic bacteria decreased by about 85%. The number of coliforms also decreased. Standardized cytotoxicity tests using Allium cepa seeds carried out to prove the effectiveness of the bioremediation process, confirmed the high degree of decontamination achieved by the use of immobilized microalga confined in a 3D-printable PLA-device

The anthropogenic impact on the Matanza–Riachuelo watershed (MRW) is critical and converts this area in one of the most polluted in Latin America (Guida-Johnson and Zuleta 2019). The Cildáñez stream is part of this watershed and presents a heavy contamination load, mainly composed of by-products of agriculture and waste materials derived from industries settled in the surroundings. Common ionic forms of dissolved inorganic nitrogen in aquatic ecosystems, including ammonium (NH4+), nitrite (NO2−), nitrate (NO3−), and phosphorus, as well as saprophytic and pathogenic bacteria from highly urbanized riversides, are the main Cildáñez stream contaminants (APRA 2016; ACUMAR 2017). It is essential to maximize research efforts directed to develop cleaning up technologies for this water body, close to which large populations are settled. In particular, reductions of nitrites and nitrates are of paramount significance, taking into account the serious health problems that these ions may generate, including methemoglobinemia and cancer (Ward et al. 2018; WHO 2011)

In a previous study, a native strain of the microalgae Chlorella vulgaris immobilized in alginate beads was tested and found to be a successful bioremediation agent (Trentini et al. 2017). Those results demonstrated the potential of this simple and cost-effective technology to remove several urban-water contaminants, offering as an additional advantage the possibility of microalga biomass recovery, which may serve as a source of third-generation biofuel. However, some field observations at the Cildáñez stream showed that alginate beads were degraded in a short time, limiting their applicability and efficiency (unpublished data)

development and testing of a 3d-printable polylactic acid

In the present study, we describe a proof-of-concept assessment of an improved bioremediation technology based on the use of a 3D-printed device manufactured in an eco-friendly polymer: polylactic acid (PLA). This polymer allows gas diffusion and is stable at physiological temperatures and pH ranges, with the advantage of reduced weight and high mechanical strength resistance, among other interesting properties (Rosenzweig et al. 2015; Seol et al. 2018). Printing systems build 3D structures following a layer-by-layer approach, and PLA filaments are available in over 90 colors (Serra et al. 2014; Letcher and Waytachek 2014). 3D-PLA-printing filaments allow a versatile-design geometry and a customized architecture, able to fulfill specific biotechnological requirements such as those needed to improve bioremediation procedures. Here, we developed and tested a 3D-printed PLA device able to retain the alginate matrix in which alga cells can be immobilized and multiply, thus carrying out the target bioprocess of water decontamination, reaching high durability

A unialgal culture of C. vulgaris strain LMPA-40 was obtained from the culture collection belonging to the Natural Science Faculty of the National University of Patagonia San Juan Bosco (Biological Data National System, SNDB-173). This culture was maintained on Murashige Skoog (MS) synthetic culture medium supplemented with sucrose (3% w/v) and indoleacetic acid (1 mg/L) as a growth regulator (Murashige and Skoog 1962) in Erlenmeyers of 250 mL containing 50 mL of culture media. Cultures were kept at 24 ± 2 °C in a shaker at 100 rpm, with mixotrophic conditions and a photoperiod of 16 h PAR (14,000 k, 400 μmol photon/m2/s)

Three water samples randomly obtained were collected from September 2017 to January 2018 from Cildáñez stream (34° 67′ 60.00″ S; 58° 44′ 37.06″ W) and analyzed in the laboratory of APRA (Agencia de Protección Ambiental, Ciudad Autónoma de Buenos Aires)

development and testing of a 3d-printable polylactic acid

The design and manufacture of the 3D-printed devices were made using specific software and a plotter (Crealty CR-10S, Shenzen Creality 3D Technol. Co., China). The polylactic acid (PLA) thread (diameter: 1.75 mm) was dispensed through a bronze needle (Volcano, internal diameter: 6 µm, at 220 °C); the plotting speed and the temperatures were 100 mm/seg and 55 °C, respectively. Figure 1 shows the device prototype, which had a torpedo shape opened at both ends. Five internal flaps to retain the alginate matrix and 5 external caudal flaps were included in the design. Size: 5 cm long, 1 cm internal diameter, basal aperture: 0.8 cm, apical aperture: 0.6 cm. The approximate volume and weight of the device were 3.93 cm3 and 0.738 g, respectively. The 3D device walls, of 4 mm thickness, were porous and rough. Devices were made in three colors: red, white, and translucent. Given the importance of light access through the PLA devices walls for the microalga growth, the transmittance (%T) of 8 × 8 mm fragments of the wall device was measured in a spectrophotometer Shimadzu UV1280 at different wavelengths. Transmittance (%T) was then calculated

Before use, the PLA devices were autoclaved at 0.1 MPa for 20 min in an equipment Chamberland (Arcano 80 L®). The process was repeated three times. A sterile alginate solution was mixed with a cellular suspension of C. vulgaris grown in MS medium with sucrose, at a rate of 2 × 106 cells/mL of alginate. The mixture obtained was dropped on a stirred solution of CaCl2 (0.1 M) using a 50 mL syringe (8.9 mm diameter outlet). The beads thus obtained were incubated for 1 h and then washed with saline solution (NaCl 0.9% w/v). To prepare the PLA units, the mixture of alginate and C. vulgaris cells was injected into each device simultaneously with the cross-linking solution of CaCl2 (0.1 M) using peristaltic pumps (10 mL/min) with a cannula from each solution. The PLA devices thus prepared were incubated for 1 h and then washed with saline solution (NaCl 0.9% w/v) three times

Two bioremediation models were compared: C. vulgaris cells immobilized in alginate beads functioning as an unconfined system (UcS) versus immobilized C. vulgaris cells (same matrix) confined inside PLA devices (CfS). The synthetic culture medium MS and the target water from the Cildáñez stream (Cil.W) were used as substrates to compare the alga’s growth dynamics before defining the best bioremediation strategy. The assays were conducted as batch systems in 250 mL Erlenmeyers containing 50 mL of MS medium/Cildáñez water and 25 beads/5 PLA devices (obtained as described before) or in stirred-tank bioreactors (Minifors, Infors HT®, Switzerland) with a working volume of 1.5 L and an initial algal inoculum of 2% (w/v) contained in 100 beads/25 PLA devices. The bioreactor includes mechanical agitation achieved by a marine Rushton propeller (100 rpm) and a porous metal sparger to supply bubble aeration (0.5 vvm). The growth of C. vulgaris along the culture period was assessed by counting algae cells in a Neubauer chamber after dissolving the alginate matrix, as previously described (Trentini et al. 2017)

development and testing of a 3d-printable polylactic acid

Once found the best conditions for algal growth, the bioprocess was scaled-up to be carried out in the bioreactors in the target water of the Cildáñez stream. The bioprocess lasted 5 days; the experimental units were kept at 24 ± 2 °C in autotrophic conditions, with a photoperiod of 16 h and the same PAR as that used for culture maintenance. Before and after each assay, the microalgal growth along time was assessed by counting C. vulgaris cells in a Neubauer chamber. The specific growth rate (µ) and the duplication time (dT) were calculated as described in Groppa et al. (2019). Water samples were filtered through a 0.45 μm membrane filter before physicochemical analysis. This analysis included pH, turbidity (NTU), electrical conductivity, nitrate, nitrite, ammonium, and total phosphorus determination. All analyses including microbial standard parameters (aerobic mesophyll bacteria and total coliforms) were performed according to the American Public Health Association (APHA) methods (2005) at the analytical service laboratory of APRA (Agencia de Protección Ambiental, Buenos Aires Ciudad). Heavy metals were also assessed by atomic absorption spectrometry (Analyst 800, Perkin Elmer, USA) using nitric acid-digested samples. Lead (Pb), cadmium (Cd), and arsenic (As) were determined using an electrothermal procedure (graphite oven). Chromium (Cr), copper (Cu), and zinc (Zn) were analyzed by flame spectrometry. Additionally, we calculated the denitrification rate (DR) as defined by Wang and Wu (2016):

where (NO −3  + NO −2 )i are the initial nitrate and nitrite concentrations, (NO −3 + NO −2 )f are the final nitrate and nitrite concentration (both in mg/L), and HRT is the hydraulic retention time of the bioprocess (5 day). The percentage of remediation was calculated as follows:

Seeds of Allium cepa (about 300 seeds) were placed in Petri plates containing a filter paper imbibed with: i. 20 mL of water from the Cildáñez stream before the bioprocess (untreated water, UW), ii. 20 mL of water from the Cildáñez stream after the bioprocess (treated water, TW); and iii. 20 mL of distilled water (control, DW). The plates with the seeds were kept at 24 ± 2 °C for 48 h. Four days later, emerging seeds (uniform in size) were transferred to 200 cc-plastic pots containing perlite and went on growing by watering with the same water treatment. On day 6 from transplanting, 10 seedlings per treatment were removed from the pots to determine the mitotic index in isolated meristematic root cells (tip region) as follows: root tips were fixed for 24 h in acetic Carnoy, and chromosomes were stained with Orcein in 2% acetic acid (Basilico et al. 2017). The mitotic index (MI) was calculated by counting cells undergoing mitotic stages respect to the total number of cells observed using a microscope Olympus BX40 (Olympus ®). Finally, on day 12, all seedlings were harvested, and roots and shoots length was determined

development and testing of a 3d-printable polylactic acid

Three independent experiments, including each four treatments (MS in Erlenmeyers, Cil.W in Erlenmeyers, MS in the bioreactor, Cil.W in the bioreactor), were carried out. Physicochemical and microbiological analyses were performed before and after the bioprocess (day 5), as already described. Experiments and analytical determinations were performed by triplicate. The cytotoxicity test was carried out using 100 onion seeds (10 independent experiments, 10 replicates each). The results were evaluated by ANOVA with post hoc Tukey test for multiple comparisons, or by Kruskal–Wallis test for non-normal variables, using Infostat software (Tukey 1953; Di Rienzo et al. 2013)

As it may be noticed in Fig. 2, C. vulgaris cell numbers significantly increased after 5 days of cultivation when this microalga was entrapped in alginate beads and placed in MS culture medium as substrate, without any confinement. When the microalga cells were entrapped in the alginate matrix and confined inside the PLA scaffolds, algal growth was notoriously diminished. In addition, we verified that the red device allowed higher growth than the white one and the translucent one (which allowed similar alga growth). On the other hand, when we used water of the Cil.W to feed the system, the microalga number increased after 5 days but in a very limited extent (about 20% as compared to that observed in the synthetic culture medium), possibly due to the competence imposed by the presence of other microbial populations in this non-sterile substrate (Fig. 2)

Cell number of C. vulgaris growing in Erlenmeyers. Initial and final cell numbers after a growth period of 5 days were determined as described in “Materials and methods”. MS UcS unconfined system in Murashigue Skoog (MS) growth medium, MS CfS (w) confined system in MS growth medium (white PLA device), MS CfS (t) confined system in MS growth medium (translucent PLA device), MS CfS (r) confined system in Cidáñez stream water (red PLA devices), Cil.W UcS unconfined system in Cidáñez stream water, Cil.W CfS (r) confined system in Cidáñez stream water (red PLA devices). Mean data from three independent experiments are shown. Letters indicate significant differences for the same substrate (p < 0.05)

development and testing of a 3d-printable polylactic acid

We also estimated the number of C. vulgaris cells released from the alginate matrix in the systems under analysis and found no significant differences between them. A control treatment using distilled water demonstrated that microalgae could not multiply without the supply of inorganic nutrients, independently of its disposition (data not shown)

As the next step, we compared the growth kinetics of C. vulgaris cultivated as unconfined beads versus the confined system. These results are shown in Table 1. C. vulgaris cells achieved the highest growth rate (µ) and the lowest duplication time (dT) when cultivated as alginate beads in the synthetic medium without any physical confinement. When the alginate beads containing algae cells were incubated in the target substrate (Cil.W), the growth rate diminished by about 75%. On the other hand, it is important to note that in the target substrate, the difference between the unconfined system and the confined system becomes not significant

Another important point to be considered is light access. Since our PLA-devices had opaque walls, photosynthetically active radiation (PAR) was expected to be a limiting factor. In this regard, we assessed the percentage of transmittance (%T) of the PLA walls manufactured in different colors at different wavelengths (Fig. 3)

development and testing of a 3d-printable polylactic acid

It may be noticed that these values were very low irrespective of the color of the device, which corroborates the opacity of PLA and light availability inside the device as a limiting factor for alga growth. On the other hand, it is observed that the %T tend to increase at higher wavelengths, reaching the white device the maximum value at 720 nm and the red device the maximum values between 680 and 720 nm (similar %T, lower than the white one), coinciding with one of the absorption peaks of chlorophyll a and chlorophyll b. Also, it may be appreciated that at lower wavelengths (under 580 nm), the red PLA device has slightly higher transmittance than the white one

The mechanical resistance of the PLA devices was checked by successive autoclaving cycles. We verified that these devices resisted a pressure of 0.11 MPa (15.95 psi) during 20 min, which is equivalent to 110 kN/m2 (11,200 kg/m2). Our devices did not undergo any deformation during the first and the second autoclaving cycles. After three autoclaving cycles, these devices tended to disaggregate, turning into a fine, crystalline sand-like stuff (data not shown)

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