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Microalgae Recovery from Water for Biofuel Production Using CO2-Switchable Crystalline Nanocellulose Shijian Ge, Pascale Champagne, Hai-Dong Wang, Philip G. Jessop, and Michael F. Cunningham Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.6b00732 • Publication Date (Web): 17 Jun 2016 Downloaded from http://pubs.acs.org on June 17, 2016

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Environmental Science & Technology

Microalgae Recovery from Water for Biofuel Production Using CO2-Switchable Crystalline Nanocellulose Shijian Ge a, Pascale Champagne a,b,*, Haidong Wang b, Philip G. Jessop,c Michael F. Cunningham b a

Department of Civil Engineering, Queen’s University, 58 University Avenue, Kingston, Ontario K7L 3N6, Canada b Department of Chemical Engineering, Queen’s University, 19 Division Street, Kingston, Ontario K7L 3N6, Canada c Department of Chemistry, Queen’s University, 90 Bader Lane, Kingston, Ontario K7L 3N6, Canada *Corresponding author: E-mail: [email protected]; Phone: (613)533-3053; Fax: (613)533-2128.

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ACS Paragon Plus Environment


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Abstract: There is a pressing need to develop efficient and sustainable approaches to harvesting

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microalgae for biofuel production and water treatment. CO2-switchable crystalline nanocellulose

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(CNC) modified with 1-(3-aminopropyl)imidazole (APIm) is proposed as a reversible coagulant

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for harvesting microalgae. Compared to native CNC, the positively charged APIm-modified

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CNC, which dispersed well in carbonated water, showed appreciable electrostatic interaction

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with negatively charged Chlorella vulgaris upon CO2-treatment. The gelation between the

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modified CNC, triggered by subsequent air sparging, can also enmesh adjacent microalgae

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and/or microalgae-modified CNC aggregates, thereby further enhancing harvesting efficiencies.

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Moreover, the surface charges and dispersion/gelation of APIm-modified CNC could be

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reversibly adjusted by alternatively sparging CO2/air. This CO2-switchability would make the

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reusability of re-dispersed CNC for further harvesting possible. After harvesting, the supernatant

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following sedimentation can be reused for microalgal cultivation without detrimental effects on

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cell growth. The use of this approach for harvesting microalgae presents an advantage to other

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current methods available because all materials involved, including the cellulose, CO2 and air,

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are natural and biocompatible without adverse effects on the downstream processing for biofuel

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production.

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Keywords: crystalline nanocellulose, microalgae, coagulation, carbon dioxide, biofuel,

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Chlorella vulgaris

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Introduction

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Microalgae are a promising alternative third generation feedstock for the biofuel production

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industry due to their higher photosynthetic efficiency and lipid contents (15-77 % of cell mass) 1-

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5

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problematic in water systems due to their rapid increase or accumulation during algal blooms.7-9

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Thus, efficient microalgal harvesting or removal from water is not only critical for biofuel

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production, but also important in the mitigation of aquatic systems.

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than common feedstocks such as crops.6 Additionally, microalgae have been shown to be

Microalgal harvesting or separation from water still represents a major technological and

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economic barrier for both the microalgae-based biofuel and water treatment industries.

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Conventional microalgal separation methods include gravity, precipitation, centrifugation,

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microstraining, flotation and filtration.10 These methods are often energy- and/or time-consuming

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and thus undesirable for both the low-cost production of microalgal biofuels and full-scale water

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treatment.11 More recently, the application of chemical flocculants such as cationic inorganics or

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polymers,12 magnetophoretic separation using native or cationic polymer coated magnetic

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nanoparticles (NPs) 13, 14 and bio-flocculation induced by microbes (e.g. bacteria, fungi) 10, 15

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have been reported. However, these methods involve the use of additives, which have the

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potential to contaminate and have adverse effects on both microalgal cells and culture media

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when using microalgae as either inocula and/or recycling supernatant after harvesting. As such,

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approaches that are sustainable and feasible for large-scale applications are still being

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investigated, and the challenge will lie in the development of technologies that can facilitate the

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separation of microalgae in a technically, environmentally and economically viable manner.

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Cellulose is the most abundant natural and renewable organic polymer on Earth,16 and it is

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regarded as an almost infinite source of raw material.17 Moreover, crystalline nanocellulose

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(CNC), derived from the acid hydrolysis of cellulose fibers, has attracted significant interest

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from both researchers and engineers due to its environmentally benign nature (biodegradability)

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and physicochemical properties such as nanoscale dimensions, high specific surface area and

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unique optical properties.18 In general, CNC properties can be manipulated for a variety of

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purposes through modification of the hydroxyl groups on the CNC surface.19 Kan et al 20

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proposed a pH-responsive P4VP-g-CNCs grafted using the surface-initiated polymerization of 4-

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vinylpyridine (P4VP) with a ceric(IV) ammonium nitrate initiator, which showed reversible

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flocculation and sedimentation properties with changes in pH. Recently, Vandamme et al.21, 22

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demonstrated the applicability of CNC functionalized with cationic pyridinium and imidazole

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groups for microalgal flocculation, and also noted that in contrast to conventional polymer

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flocculants, the flocculation efficiency of cationic CNC was relatively unaffected by algal

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organic matter. In their studies, however, the recovery and reuse of the CNC and the culture

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medium were not investigated. Such recycling could be an important consideration in the

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development of a sustainable and economic technology. Moreover, further optimization of CNC

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dosage requirement is essential to minimize the cost of the CNC.

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To allow for the recovery and reuse of flocculants or coagulants, detachment of the

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flocculants or coagulants from the microalgae must be achieved, for example by inducing

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changes in their surface properties, such as surface charge and wetting properties.13, 23-25 Such

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changes may be triggered by the presence of switchable or stimuli-responsive groups on the

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surface of the flocculants or coagulants. We recently reported a new CNC which is a CO2-

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switchable nanomaterial prepared by surface modification with 1-(3-aminopropyl)imidazole 4


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(APIm).26 Such APIm-modified CNC was positively charged in the presence of CO2 resulting

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from the protonation of the APIm groups by the carbonated water (Equation 1), which can

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probably promote the coagulation or attachment of microalgae cells carrying negative charges.21

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Additionally, the chemically bonded imidazole groups on the CNC surface can respond to the

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CO2 stimulus in an effective and repeatable manner. Specifically, the APIm-modified CNC

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disperses well in water in the presence of CO2, while subsequent removal of CO2 through

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sparging of the dispersion with N2 gives rise to the formation of aggregates. This

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dispersion/aggregation cycle can be performed repeatedly by alternating treatments with CO2

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and N2, which could allow for the recovery of the CNC, potentially resulting in a decrease in the

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economic and ecological cost of the microalgal harvesting process.

(1)

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In this study, the APIm-modifed CNC was synthesized as previously reported 26. The

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following questions were then addressed: (1) does surface modification of the CNC with APIm

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create a CO2-switchable surface charge and reversible size changes in contrast to native CNC; (2)

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can the APIm-modified CNC be used to harvest a model biofuel-producing microalgal species,

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Chlorella vulgaris (C. vulgaris) with a reduced dose demand and harvesting time compared to

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the native CNC; (3) can the process be modified to improve the harvesting efficiency, for

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example by changing the method or flow rate of inert gas introduction; (4) are the colloidal

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interactions between CNC particles and microalgae consistent with the

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Derjaguin−Landau−Verwey−Overbeek (DLVO) theory; and (5) can the culture medium, as well 5



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as the harvested and concentrated microalgae-CNC aggregates, be recycled to decrease

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operational costs and increase the sustainability of this CNC-based microalgal separation process?

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Materials and methods

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Microalgal culture. A 25 L glass carboy was used to grow C. vulgaris in modified Bold's

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Basal Medium (MBBM) at room temperature (23.0 ± 0.5°C).10 The MBBM contained the major

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ions of Na+, K+, Mg2+, Ca2+, Fe2+, Zn2+, Mn2+, Cu2+, Co2+, H+, NO3- , H2PO4- , HPO42-, BO33-,

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SO42-, Cl-, OH-, MoO42-, and EDTA2- with a total ionic strength of 10.4 mM. The molarity of

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each ion is listed in Table S1. The initial solution pH, dissolved oxygen, and oxidation reduction

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potential of the culture medium were 6.8 ± 1.0, 12 ± 2 mg·L-1, and 170 ± 31 mV, respectively.

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The system was aerated with filtered ambient air (0.039 % CO2) at a rate of 200 mL·min-1.

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Continuous irradiation (27.4 µmoles·m-2·s-1) was applied. During cultivation, samples were

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collected to measure optical density at 680 nm (OD680) using a spectrophotometer (Hach Method

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8171).27 Biomass concentration (g·L-1) was gravimetrically quantified by dry cell weights

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(DCW), which was performed by drying 0.45 µm membrane-filtered microalgae in an oven at

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105 oC to a constant weight.10

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Preparation and characterization of APIm-modified CNC. The native CNC was

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provided by FPInnovations, Canada. The APIm-modified CNC was synthesized as previously

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reported by our group, which used 1,10-carbonyldiimidazole (CDI, reagent grade, Sigma-Aldrich)

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and 1-(3-aminopropyl)imidazole (APIm, ≥ 97 %, Sigma-Aldrich).26 Zeta potentials, average

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hydrodynamic diameters, and particle size distributions (PSD) of both native and APIm-modified

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CNC suspended in water, under the various experimental conditions mentioned below, were

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characterized at 25 oC by dynamic light scattering (DLS) on a Zetasizer Nano ZS instrument 6


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(Malvern Instruments, UK) using DTS 160 disposable folded capillary cells. Refractive indices

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of 1.500 and 1.347 were used, respectively, for APIm-modified CNC and C. vulgaris cells for

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calculating the scattering wave vector.

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Microalgae separation with APIm-modified CNC. Harvesting experiments began once C.

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vulgaris had reached their exponential growth stage. The APIm-modified CNC stock dispersion

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in water (～10.5 g·L-1, 35 mL) was vortexed (3 times at 3000 rpm for 2 min each, with 30 s

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intervals), sparged with CO2 (99.995%, MEGS) for 10 min, and briefly centrifuged (15,000 ×g,

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20oC, 1 min) to remove floating particles. Then the supernatant containing well-dispersed APIm-

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modified CNC was mixed into the 20 mL suspension of C. vulgaris in a 50 mL glass specimen

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bottle or falcon tube at room temperature with an initial microalgal concentration of 0.2-0.4 g·L-1.

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Afterwards, CO2 was sparged into the suspension for 1 min. After sparging with air (lab air

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system) or N2 (99.9999%, MEGS) gas for a specified time (5-10 min), microalgae-CNC

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aggregates were allowed to flocculate and settle for 10 min. The gas sparging was conducted

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under 1 atm of CO2, N2 or air. Finally, liquid samples were taken from 1.0 cm below the surface

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of the microalgal suspension for an optical absorbance measurement at 680 nm using a Hach

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Method 8171 spectrophotometer. Three indicators including harvesting efficiency (HE) for the

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evaluation of the efficiency of proposed harvesting technique, recovery efficiency (RE) for

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efficiency of the coagulant (native or modified CNC), and recovery capacity (RC) for the

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harvesting performance as attributed to microalgal quantities (gram algae) per gram CNC, were

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used to evaluate microalgal separation performance:28, 29

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HE (%)=[1-(C t /C0 )]×100%

(2)

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C t C0 )]×100% C't C'0 ( C − Ct )V RC (g-algae ⋅ g-CNC-1 ) = 0 m

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where C0 and Ct are the microalgal concentrations in the supernatant before and after separation

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(g·L-1), C0’ and Ct’ are the microalgal concentrations without addition of native or APIm-

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modified CNC in the control group (g·L-1), V is the volume (20 mL) of microalgal suspension

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and m is the mass of APIm-modified CNC added (g). APIm-modified CNC concentrations were

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gravimetrically quantified by dry cell weights (g·L-1). Microalgal separation was studied by

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varying the APIm-modified CNC dosage, non-acidic gas (pure N2 or air) addition, and air

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sparging time as described below. All experiments below were performed in duplicate or

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triplicate.

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Effect of CNC surface modification. Different quantities of native or APIm-modified CNC were

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added to the C. vulgaris suspensions at 0.2～0.4 g-DCW·L-1 to achieve different mass ratios of

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coagulant to microalgal biomass (0.01, 0.02, 0.05, 0.1, 0.2, 0.3, 0.4, and 0.5 g-CNC·g-algae-1).

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All doses were calculated based on the dry weights of both microalgae and CNC. The mixtures

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were then sparged with CO2 for 1 min followed by air alone at a gas flow rate of 140 mL·min-1

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for 10 min.

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Effect of inert gas and flow rates. The sparging of nitrogen-containing gas (either pure N2 gas or

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air) was used to flush CO2 from the aqueous phase. These two nitrogen-containing gases (N2 or

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air) were compared to evaluate their effectiveness for microalgal separation. In addition, three

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flow rates (25, 80 and 140 mL·min-1) were applied. The separation experiments were performed

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with an optimized dose (0.05 g-CNC·g-algae-1) of APIm-modified CNC determined above.

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(3)

RE (%)=[1-(

(4)

8


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Effect of air sparging time. After 1 min of CO2 sparging, different air sparging times (0, 1, 3, 5,

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7, 10, 13, 20 min) were investigated to optimize the sparging time required for coagulation.

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These were performed at two APIm-modified CNC doses (0.05 and 0.49 g-CNC·g-algae-1) for

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comparison.

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Effect of pH adjustment. Different pH cycles (4.9/7.9, 4.6/7.8 and 4.2/7.2) were artificially

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generated through the addition of 1 M HCl and 1 M NaOH to mimic the CO2/air-treated samples

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for three APIm-modified CNC doses (0.05, 0.29 and 0.49 g-modified CNC.g-1-algae). In another

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pH adjustment experiment, the use of HCl/air treatment was compared. A control experiment

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having only a pH adjustment of 4.6/7.8 (with 1 M HCl and 1 M NaOH), but without any APIm-

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modified CNC was also tested.

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Assessment of supernatant and APIm-modified CNC reuse. After harvesting the

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microalgae with APIm-modified CNC, concentrations of nitrate and phosphorus in the used

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medium were adjusted to the levels in the MBBM. The medium was then reused to cultivate C.

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vulgaris. For comparison, another two microalgal culture supernatants were used, which were

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obtained after harvesting by either centrifugation (as a control) or coagulation using alum (20

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mg·L-1). Both recycled supernatants were then reused for microalgal cultivation. In all three

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cases, the biomass growth in the recycled medium was monitored for 7 days in 250 mL flasks.

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Cultivation conditions were previously described.30

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To determine the recyclability of APIm-modified CNC (0.49 g-modified CNC.g-1-algae), the

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collected microalgae-CNC aggregates (～2.0-2.5 g-algae·L-1 in ～3 mL) were reused to harvest

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new microalgae batches following the same harvesting procedures as noted above. The process

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was repeated for five cycles to further assess the recyclability. 9



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Comparison of colloidal interaction. Quantitative information on the nonspecific interactive

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forces between CNC particles and microalgal cells can be directly obtained with Ohshima’s soft-

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particle DLVO theory assuming that Lifshitz-van der Waals and electrostatic forces are the

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dominant forces.31, 32 The computation methods for the van der Waals and electrostatic forces

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vary with the geometry of the interacting entities. The diameter of spherical microalgal cells is

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approximately 2-5 µm, 33 and the CNCs are usually 100–300 nm in length and 10-20 nm in

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width. In this study, the CNC was assumed to be spherical to simplify the analysis to sphere-to-

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sphere geometry, as was employed in other studies and to allow for comparison of the interaction

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between microalgae and flocculants such as metal oxide NPs, or bacteria. 10, 29, 34, 35 The retarded

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Lifshitz-van der Waals and the electrostatic interaction energy (the linearized version of the

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Poisson−Boltzmann expression) for sphere-to-sphere geometry were calculated as per Equations

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(5) and (6) when h95 % RE was achieved with

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each cycle, indicating that following CO2 sparging, the re-dispersed APIm-modified CNC

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particles have sufficient adsorption sites to coagulate additional microalgal cells. The pKa of the

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imidazole functionalities have been reported to be in the range of 6.0-6.5.40, 41 In our previous

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study,26 it was calculated that up to 94 % of imidazole rings could be protonated upon exposure

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to CO2, while sparging N2 reduced this value to 26%. These results imply that over the pH range

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obtained with CO2/air sparging, the imidazole groups on the APIm-modified CNC can switch

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from being almost fully protonated to only partially protonated, which directly influences the

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attachment or detachment of CNC and microalgae, and the ability to reuse the APIm-modified

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CNC.

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Such CO2-switchable APIm-modified CNC has been demonstrated to be greener than the

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recyclable polyampholytic flocculants which require the addition of acid and base,25 is likely to

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be more energy-efficient than the magnetic Fe3O4-ZnO nanocomposites which require UV

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irradiation,23 and more beneficial for the microalgae harvesting process than single-use

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commercial flocculants.42 As such, this recyclable CO2-switchable APIm-modified CNC has the

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potential to provide a sustainable solution to microalgal harvesting and cultivation. Moreover, 23



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the saturated microalgae-modified CNC aggregates have the potential for use in biofuel

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production through subsequent anaerobic digestion, hydrothermal liquefaction or other

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conversion technologies. To some extent, such recycling and biofuel conversion could

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compensate for the use of more expensive CNC materials as coagulants, requiring considerably

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higher initial capital investment, which would otherwise hamper their application in industry. A

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life cycle assessment (LCA) of such an integrated process would also be highly valuable in

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assessing its water, energy and environmental footprint, as well as its techno-economic viability.

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Supporting Information

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Additional information includes Table S1-S8, and Figures S1−S5. This material is available free

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of charge via the Internet at http://pubs.acs.org.

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Acknowledgements

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The authors thank the Ontario Ministry of Research Innovation – Ontario Research Fund, the

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National Science and Engineering Research Council (NSERC), the Canada Research Chairs

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program (PC, PGJ) and the Ontario Research Chairs program (MFC).

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Microalgae Recovery from Water for Biofuel ... - ACS Publications

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