Sustainable Biocement Production via Microbially Induced Calcium

Research Article pubs.acs.org/journal/ascecg

Sustainable Biocement Production via Microbially Induced Calcium Carbonate Precipitation: Use of Limestone and Acetic Acid Derived from Pyrolysis of Lignocellulosic Biomass Sun Gyu Choi,† Jian Chu,† Robert C. Brown,‡ Kejin Wang,§ and Zhiyou Wen*,∥ †

School of Civil and Environmental Engineering, Nanyang Technological University, 10 Blk N1, 50 Nanyang Ave, Singapore 639798 Bioeconomy Institute, Iowa State University, 617 Bissell Road, Ames, Iowa 50011, United States § Civil, Construction and Environmental Engineering, Iowa State University, 813 Bissell Road, Ames, Iowa 50011, United States ∥ Food Science and Human Nutrition, Iowa State University, 536 Farm House Lane, Ames, Iowa 50011, United States ‡

ABSTRACT: Biocement production from microbially induced calcium carbonate precipitation (MICP) is an environmentally friendly approach for construction works, but the use of calcium chloride (CaCl2) in the conventional MICP process is a cost-limiting factor. The aim of this work is to develop a method for producing soluble calcium ions through two waste sources, limestone powder derived from aggregate quarries and acetic acid derived from fast pyrolysis of lignocellulosic biomass, as a replacement for the reagent grade CaCl2 in the MICP process. The ratio of limestone powder to acetic acid solution was optimized for a desirable calcium concentration with an appropriate pH. Procedures for applying the urease-producing bacteria, urea, and calcium solutions were developed for a successful MICP process and were treated for sand column test. The engineering properties of the biocemented sand, including water permeability, unconfined compressive strength, and tensile strength, were evaluated as a function of the calcium carbonate content of the product. It was found that the properties of the sand treated using the limestone/acetic acid derived calcium solution were comparable to those of sand treated using reagent grade CaCl2. Collectively, the results indicate that the new MICP process is effective, more sustainable, and cheaper compared with the conventional MICP method. KEYWORDS: Biocementation, Permeability, Strength, Limestone, Acetic acid

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Ca 2 + + CO32 − → CaCO3↓

INTRODUCTION Cement-based materials (grout, mortar, and concrete) have been widely used for construction and infrastructures repair.1 The production of cement is energy-intensive and environmentally unfriendly due to the requirement for burning limestone at a very high temperature (950 °C) and the emission of carbon dioxide. It is reported that production of one ton of Portland cement generates approximately 0.814 ton of carbon dioxide (CO2) from calcining limestone and fuel use.2 Cement production contributes about 5% of global CO2 emissions. In the recent years, an environmentally friendly biobased cement material has been developed for geotechnical applications.3−5 Biocement is a construction material that can be made from calcium salt (Ca2+), a small amount of urea (CO(NH2)2), and urease-producing bacteria (UPB). The mechanism for using biocement as construction materials is called microbially induced calcite precipitation (MICP), which is described by the reactions: UPB

CO(NH 2)2 + 2H 2O ⎯⎯⎯→ 2NH

4+

+ CO3

2−

© 2017 American Chemical Society

(2)

where carbonate (CO32−) is produced from urea decomposition that is catalyzed by UPB. Carbonate then reacts with calcium ions to form calcium carbonate (CaCO3) in situ, which can fill small pores, bridge cracks, and bind loose particles.6,7 Biocement can be used for both construction and concrete repair.8,9 It can be used in a manner similar to that for cement to reduce the hydraulic conductivity and increase the shear strength of soil as well as repair cracks in concrete. Cement grout is made of cement, water, and sometimes fine aggregate. Biocement can be used to make grout in more or less the same way as for cement grout, but can increase the shear strength or decrease the hydraulic conductivity of soil.10 Various studies have been conducted on the use of biocement grouting to replace conventional cement grouting. These include dust control,11 construction of landfill for solid waste disposal, stabilization of slopes or levees,12 mitigation of liquefaction of Received: February 18, 2017 Revised: May 8, 2017 Published: May 16, 2017

(1) 5183

DOI: 10.1021/acssuschemeng.7b00521 ACS Sustainable Chem. Eng. 2017, 5, 5183−5190

Research Article

ACS Sustainable Chemistry & Engineering

min. The culture was maintained in a shaker (130 rpm) at 30 °C for 2 days. Cell growth was monitored by measuring the optical density (OD) of the broth at 600 nm. When ready to be used, the UPB solution had the OD600 range 1.0−1.6, similar to previous reports.26,27 The urease activity of the UPB solution was measured using an electric conductivity meter,28 resulting in a range from 8 to 15 mM/min, also similar to those reported previously.26,29 Preparation of Calcium Ion Solution. Calcium ion solution was produced by dissolving a limestone powder in an acetic acid-rich solution. The limestone powder was obtained from the Martin Marietta limestone quarry in Ames, Iowa, USA. It had a particle size passing # 200 screen (less than 0.075 mm) and a specific gravity of 2.70. The limestone contained 50.7% (by weight) CaO as a major composition, with a small amount of SiO2 (2.39%), Al2O3 (0.85%), and Fe2O3 (0.35%). The acetic acid rich stream was received from the Bioeconomy Institute at Iowa State University in Ames, Iowa, USA. The stream was a byproduct from the fast pyrolysis of lignocellulosic biomass for producing drop-in fuels.30 It contained more than 7% (w/v) acetic acid with a relatively small amount of acetol (5.06%), total phenolics (2.09%), and formic acid (1.22%). The calcium ion is produced as follows:

soil,13 seepage control for underground construction, and construction of an aquatic pond in sand.14 Compared to Portland cement, the use of biocement has several advantages. First, the production of biocement consumes much less energy. Biocement is produced at an ambient temperature, 20−40 °C, while the temperature for cement production is 950 °C. Second, the viscosity of biocement-based grout is much lower than that of Portland cement-based grout; thus, biocement can be more easily injected into the ground or mixed with soil than Portland cement. Third, the particle sizes of biocement are smaller than those of Portland cement; therefore, biogrout can be permeated into porous materials (e.g., soil and concrete) and seal finer fissures in pores and cracks than Portland cement grout. Because of these advantages, biocement has the potential to play a significant role in the next generation of sustainable construction materials. Nevertheless, it should be noted that the applications of biocement are mainly limited to geotechnical problems as described above. It is not intended as a complete replacement of Portland cement. However, the use of MICP-based biocementation also has challenges. The MICP process usually requires a large amount of calcium chloride (CaCl2) as a calcium source,15−17 which is expensive and environmentally unfriendly.18 Efforts have been made to develop alternative calcium sources, for example, a plant-induced calcite precipitation (PICP) process that used urease reactive jack bean and calcium hydroxide and/or calcium nitrate for sand cementation.19 Another piece of research used calcium nitrate and acetate as a calcium source to replace CaCl220 as calcium source using eggshell and vinegar.21 Those methods, however, are either unsuitable for large-scale application or not economically competitive. To address the above limitations, this study reports a new and cost-effective method for producing calcium ions using waste materials and its application in biocementation. A limestone powder derived from aggregate quarries and an acetic acid derived from fast pyrolysis of lignocellulosic biomass were used as raw materials for producing calcium ions. Limestone is a large quantity of waste materials in aggregate. Similarly, acetic acid is a major byproduct in fast pyrolysis of lignocellulosic biomass. Fast pyrolysis of lignocellulosic biomass is the decomposition of the organic matter in the biomass without oxygen. The process has proved a promising approach to produce drop-in fuels from lignocellulosic biomass. The pyrolysis process, however, commonly produces a significant amount of acetic acid as a byproduct.22 The disposal of this acetic acid stream is challenging for the cellulosic biofuel industry.23 In this work, we use this acetic acid stream to dissolve calcium from the limestone powder. The produced calcium ions were used for biocement production through the MICP process. The aim of the current study is to explore the feasibility of this unique approach and to optimize the reaction conditions of acetic acid and limestone for a maximum calcium solution production. A MICP process using the produced calcium ion was applied for sand cementation. The engineering properties of the biocemented sand were evaluated.

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CaCO3 + 2CH3COOH → Ca 2 + + 2(CH3COO)− + CO2 + H 2O

(3)

To optimize the ratio of limestone to acetic acid, limestone powder (100 g) was mixed with acetic acid solution (200, 400, 800, and 1200 mL) at different ratios (w/v), i.e. 1:2, 1:4, 1:8, and 1:12, respectively. After a 5-day reaction at room temperature (∼25 °C), calcium concentration and pH value of the limestone/acetic acid mixture solution were determined. As shown in Table 1, the resulting solution contained calcium ion ranging from 0.83 to 0.64 M and pH from 5.2 to 4.8.

Table 1. Different Ratios of Limestone Powder to Acetic Acid Solution Used for Preparing Calcium Ion Solution Limestone powder (g)

Acetic acid Solution (mL)

Calcium ion conc (M)

pH

100 100 100 100

200 400 800 1,200

0.83 0.80 0.76 0.64

5.2 5.1 5.0 4.8

Our previous research has demonstrated that the raw acetic acid stream derived from biomass pyrolysis contains various compounds, such as acetol, 5-hydroxymethylfurfural (HMF), phenolics, and furfural, which are strong inhibitors for bacterial growth.22,23 Considering the case that 800 mL of acetic acid solution resulted in a relatively high calcium concentration with a large volume, and the fact that 1,200 mL of acetic acid contains substantial inhibitory compounds, the 800 mL of acetic acid solution was selected for producing calcium ions in the following MICP process development. The calcium solution prepared from 800 mL of acetic acid solution was further added with distilled water to adjust the final calcium ion concentration to 0.3 M. The pH of this solution was further adjusted to 7.0−7.5 using ∼4.5 g of sodium hydroxide pellets. The solution was then centrifuged at 4,000 rpm for 20 min to obtain supernatant, which serves as the final calcium ion solution in the following MICP processes in both free solution and sand column tests. Development of MICP-Based Biocementation Process in Free Solution Tests. The MICP process for biocementation was illustrated in Scheme 1. The UPB culture broth (30 mL) grown for 2 days with a density of OD600 = 0.8−1.2 was mixed with 0.3 M urea solution (30 mL) at a ratio of 1:1 (v/v). The mixture had a pH 7.0− 7.5 and was stored in a beaker for 1 day, and then added with calcium solution (30 mL) which was prepared based on the procedures

EXPERIMENTAL SECTION

Urease-Producing Bacteria (UPB) Culture. Sporosarcina pasteurii (ATCC 11859) was used as the urease-producing bacterium (UPB).5,24 The bacterial cells were grown in medium containing (per liter) 20 g of yeast extract, 10 g of ammonium sulfate, and 0.13 M Tris buffer (pH = 9.0).25 The medium was autoclaved at 121 °C for 15 5184


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column.31 The recirculation procedure was continued for another 3 days. After being treated for a total of 10 days, the outlet from the column was blocked completely. The cemented sand column was then washed with distilled water, and the outer cylinder layer was removed. Evaluation of the Properties of the Biocemented Sand Columns. The cemented sand columns were tested to evaluate their engineering properties, including water permeability, unconfined compressive stress (UCS), tensile stress (TS), microstructure image, and CaCO3 content. To carry out the permeability tests, the sand column (both before and after MICP treatment) was soaked in distilled water for 24 h and then subjected to a constant head based on the ASTM D 2434 method.32 The sand columns were then placed at 23 °C and 50% RH conditions for two-days prior to the UCS and TS tests based on the ASTM D 4219 and ASTM C 496 methods, respectively.33,34 Among six sand columns tested, three were used for UCS tests (designated as UCS1, UCS2, and UCS3) and the other three for TS tests (designated as TS1, TS2, and TS3). About 5 g of biocemented sand samples were collected from the centers of the failed sand columns for the microstructure image observation through a scanning electron microscope (SEM) and for the determination of the CaCO3 content using the ASTM D4373 method.35

Scheme 1. Schematic Illustration of the MICP Process in Free-Solution Tests

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described in the previous section Preparation of Calcium Ion Solution). Precipitation was observed immediately after addition of the calcium solution. This precipitated material was filtered out by FG/C filter paper and dried at 115 °C for 1 day. The dried material was then analyzed using X-ray diffraction (XRD). Development of MICP-Based Biocementation in Sand Column Tests. A total of six sand columns were tested for MICPbased biocementation. The schematic setup of the MICP-based sand column biocementation test is shown in Scheme 2. As shown in the

RESULTS Confirmation of the MICP Process from Limestone and Acidic Acid in Free Solution Tests. The precipitated material was produced from the MICP process using acetic acid and limestone. These precipitated materials were analyzed by XRD (Figure 1). The XRD pattern of the precipitated materials (Figure 1A) perfectly matched that of the pure reagent grade of calcium carbonate (CaCO3) (Figure 1B). The result confirms that the precipitate was indeed CaCO3, and validated the use of acetic acid derived from biomass fast pyrolysis and the limestone to produce calcium carbonate in the MICP process. In the following work, sand column tests were conducted to evaluate the effectives of the this unique MICP process. CaCO 3 Content and Permeability of the Sand Columns. The CaCO3 content of the cemented sand ranged from 5.67% to 8.19%. This was within the CaCO3 content range used in previous studies where reagent grade CaCl2 was used in the MICP process.31 The variation in the CaCO3 contents in the six sand columns was due to the experimental variations such as the liquid flow patterns inside the sand columns, the surface areas of the sands in each column, etc. The water permeability of the cemented sand is plotted as a function of the CaCO3 content in Figure 2, along with the permeability of the untreated sand as a comparison. It can be seen that the permeability has reduced from 1 × 10−4 m/s for untreated sand to 8.17−1.52 × 10−6 m/s for MICP treated sand. This is similar to the observation made in previous studies31 that the permeability of the MICP treated sand decreases with the CaCO3 content nonlinearly. Strength of the Sand Columns. Figure 3 shows unconfined compressive stress (UCS) and tensile stress (TS) as functions of the axial strain of the cemented sand columns. As shown in the figure, the stress−strain behaviors were similar for each set of UCS or TS tests. Based on the data in Figure 3, the strength values obtained from the UCS and TS tests are plotted as a function of CaCO3 contents, respectively. As shown in Figure 4A, both the UCS and TS strengths of the cemented sand increased with calcium carbonate content, which is similar to the previous studies.6,21 The trend lines of the UCS and TS vs CaCO3 contents were also determined with high correlation coefficients (R2) obtained within the calcium carbonate content range 5.5−8.5% (Figure 4A).

Scheme 2. Experimental Setup for MICP-Based Biocementation in Sand Column Tests

scheme, sands (U.S. Silica Company‘s Ottawa plant in Ottawa, IL) were placed in a PVC cylinder (5 cm diameter and 10 cm length) in 10 layers with a density of approximately 1.70 g/cm3. Two pieces of 3 M Scotch-Brite scouring pads were placed at each end of the sand column as filters. The PVC cylinder was placed on a funnel filled with gravel. A beaker was used to collect the solution penetrating through the sand column, which was then circulated to the top of the column. To implement the MICP process, 80 mL of UPB seed solution was placed in the beaker and recirculated through a peristaltic pump to the top of the sand column (Scheme 2). The pumping rate was controlled at 1.5−2.0 mL/min. The liquid circulation was run for 3 h to ensure the UPB cells were evenly distributed within the column. Then, the solution in the beaker was replaced with a mixture of fresh UPB seed solution (30 mL), urea solution (150 mL at 0.3M), and calcium solution (150 mL at 0.3 M). The calcium solution was prepared based on the procedures described in the previous section, Preparation of Calcium Ion Solution). This mixed solution was recirculated through the column for 9 h. The above recirculation procedure (3 h of UPB seed and 9 h of UPB/urea/calcium solution) was repeated twice a day for 7 days, at which point calcium carbonate began to precipitate in the 5185


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Figure 1. XRD results of the materials precipitated from the MICP process (A), and pure reagent grade calcium carbonate (B). The MICP process was performed in free solution with limestone powder and acetic acid solution derived from lignocellulosic biomass.

A series of hypothetical CaCO3 contents (5%−9%) were selected to cover the true CaCO3 contents in this work. Under each hypothetical CaCO3 content, the UCS and TS strength values were determined based on their corresponding regression equations in Figure 4A. The UCS/TS strength ratio was then calculated and plotted as a function of the corresponding CaCO3 contents (Figure 4B). As shown in Figure 4B, the strength ratio increased with calcium carbonate content. At 9% of CaCO3, the column has a strength ratio of 6.87. It should be noted that the UCS/TS strength ratio can be extrapolated as 7.3−7.6 at a calcium carbonate content of 11− 13%, which is almost the same strength ratio as reported at the same calcium carbonate content but using calcium chloride for the MICP process.31 The results in Figure 4B also suggest that when the calcium carbonate content of the MICP-treated sand is within 5−9%, the brittleness of the MICP-treated sand is less than that of the rock materials. Microstructure of MICP Treated Sand Columns. The microstructures of the biocemented sand columns are shown in Figure 5. Figure 5a shows that, after the MICP treatment, sand particle surfaces were covered with CaCO3. Clumps of CaCO3 also filled the spaces between the sand particles (area “A”). Figure 5b illustrates the particles bridged by CaCO3. Figure 5c indicates that CaCO3 covered the sand surface with a size approximately ranging from 5 to 20 μm, which is comparable to

Figure 2. Permeability of MICP-treated sand as a function of CaCO3 content in the sand column. Permeability of untreated sands is also presented as a baseline.

The UCS/TS strength ratio of the treated sand is also presented to monitor its brittleness (Figure 4B). In general, the higher the UCS/TS strength ratio, the more brittle the material. The strength ratio can change with rock types from 2.7 to 39 with an average of 14.7.36 Here the strength ratio was determined based on the two regression curves in Figure 4A. 5186


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Figure 3. Strain−stress relationship of the sand columns cemented with the MICP process using limestone powder and acetic acid solution derived from lignocellulosic biomass: (A) unconfined compression (UC); (B) splitting tensile (TS).

Figure 4. Strength (maximum unconfined compressive stress (UCS) and tensile stress (TS)) of the sand columns as functions of the CaCO3 content in the columns (A) and strength ratio of UCS to TS (B).

those observed from the previous MICP study where reagent grade CaCl2 was used as the calcium source.31 In some other areas of the sand column, precipitated CaCO3 with different morphologies was observed. For example, loosely packed, smaller size sphere-shaped CaCO3 crystals with radial striations were observed (Figures 5d−f. The different morphologies of the CaCO3 crystals might be related to bacteria types, calcium sources, and medium types.20 Further study is needed to study the factors affecting the formation of CaCO3 morphologies in different MICP processes.

aggregate quarries, are capable of producing soluble calcium ions. The XRD curve of the precipitated materials in the free solution test confirmed the successful implementation of the MICP process based on these two waste materials. It should be noted that this lab-scale feasibility study did not provide a thorough analysis of production costs. With the optimization of various operation procedures, the cost of biocement production proposed in this work can be competitive to the conventional CaCl2-based biocement. For example, centrifugation was used to prepare a clean calcium ion solution in this lab-scale study. In the large-scale operation, the centrifugation operation can be replaced by cost-effective solid−liquid separation methods such as filtration or sedimentation. The particle size of limestone powder can also be optimized to produce a best calcium ion dissolving efficiency. The biocement production reported in this work also represents a more sustainable approach to producing biocement. For example, chloride ions (Cl−) derived from the CaClbased biocement production can negatively affect freshwater microorganisms and natural plants and also induce the corrosion of the steels reinforcement of construction works.39 Producing calcium ions by limestone derived from aggregate quarries and acetic acid derived from lignocellulosic biomass

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DISCUSSION Portland cement is the most common material used for soil improvement. However, use of Portland cement has severe environmental issues, such as greenhouse gas emission and high energy consumption. The development of quarries for cement materials also damages the natural forest and inhabitants. Biocement produced through the MICP process is a new and eco-friendly cementation material that can reduce the problems related to the use of Portland cement.37 Currently, the commercialization of biocement production is facing several challenges, such as high material costs. For example, calcium chloride is commonly used as a source of calcium ion in the MICP process at a price of about $20−60/ m3.38 This study confirmed that the acetic acid derived from biomass fast pyrolysis, together with the limestone waste from 5187


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Figure 5. SEM images of MICP-based cemented sand columns. The MICP process was prepared in free solution with limestone powder and acetic acid solution derived from lignocellulosic biomass.

fast pyrolysis is a cost-effective and environmentally friendly method for providing these important materials for the MICP process. Unlike chloride, acetate ion has a less negative impact on the environment and can be readily degraded by natural microorganisms. Another suitable characteristics of this work is the use of acetic acid byproduct derived from biomass fast pyrolysis. Fast pyrolysis of lignocellulosic biomass has been widely studied as an effective approach for producing bio-oil that can be upgraded into drop-in fuels.40 During the biomass pyrolysis process, however, acetic acid is produced as one major chemical constituent of pyrolysis-derived bio-oil, and is often viewed as a corrosive contaminant rather than a valuable product. The coupling of using this waste acetic acid with biocement production can not only produce an environmentally friendly construction material, but more importantly, can provide an outlet for using acetic acid rich byproducts of the biomass fast pyrolysis process. In general, factors such as urease activity,26 concentrations of chemicals used,27 degrees of saturation,41 and types of calcium19,20 were all influencing the engineering properties of the cemented sand columns. The engineering properties of the sand column obtained from the acetic acid and limestone waste materials were compared to those of the sand columns using the reagent grade CaCl2. For example, Figure 6 demonstrates the UCS values of sand columns cemented from different MICP processes. As shown in Figure 6, the UCS values increased with increasing calcium carbonate content for all the cases. Feng and Montoya reported that engineering properties (cohesion, friction angle, and shear strength) of cemented sands increased compare to the untreated sand due to the bonding of the sand particles by calcium carbonate precipitation, and high calcium carbonate content led to a stronger bonding.42 The UCS vs calcium carbonate trend line obtained in this work was in a similar range as those for other sand columns and was, in particular, similar to the column reported by Al Qabany and Soga (Figure 6).27 From these comparisons, it can be concluded that the sand column

Figure 6. Comparison of UCS values obtained from this study with the UCS values reported from other studies. All the columns were treated using similar chemical concentrations (0.2−0.5 M) of urea and calcium solution.

cemented from waste limestone powder acetic acid can be an effective approach for MICP-based biocementation. This work has demonstrated a novel approach to produce biocement materials using limestone waste and acetic acid byproducts derived from lignocellulosic biomass pyrolysis. However, it should be noted that MICP-based biocementation also has other challenges, such as emission of ammonia due to high pH, and difficulty to apply fine soil (silt or clay) due to the small particle size of bacteria and precipitated calcium carbonate.3 More research is needed to solve those problems so the MICP biocementation can be applied in various soil types and real ground, and this is underway.43

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CONCLUSIONS This paper reported the development and evaluation of a new MICP process using waste limestone from an aggregate quarry and acetic acid from the fast pyrolysis of lignocellulosic 5188


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(14) Chu, J.; Ivanov, V.; Stabnikov, V.; Li, B. Microbial method for construction of an aquaculture pond in sand. Geotechnique 2013, 63 (10), 871−875. (15) Dejong, J.; Fritzges, M.; Nüsslein, K. Microbially Induced Cementation to Control Sand Response to Undrained Shear. J. Geotech. Geoenviron. Eng. 2006, 132 (11), 1381−1392. (16) Cheng, L.; Cord-Ruwisch, R. Upscaling Effects of Soil Improvement by Microbially Induced Calcite Precipitation by Surface Percolation. Geomicrobiol. J. 2014, 31 (5), 396−406. (17) Burbank, M. B.; Weaver, T. J.; Lewis, R.; Williams, T.; Williams, B.; Crawford, R. Geotechnical Tests of Sand Following Bio-induced Calcite Precipitation Catalyzed by Indigenous Bacteria. J. Geotech. Geoenviron. Eng. 2013, 139 (6), 928−936. (18) Chung, J. S.; Kim, B. H.; Kim, I. S. A case study on chloride corrosion for the end zone of concrete deck subjected to de-icing salts added calcium chloride. J. Korean Society of Safety 2014, 29 (6), 87−93 (In Korean).. (19) Park, S. S.; Choi, S. G.; Nam, I. H. Effect of Plant-Induced Calcite Precipitation on the Strength of Sand. J. Mater. Civ. Eng. 2014, 26 (8), 06014017. (20) Zhang, Y.; Guo, H. X.; Cheng, X. H. Influences of calcium sources on microbially induced carbonate precipitation in porous media. Mater. Res. Innovations 2014, 18 (2), 79−84. (21) Choi, S. G.; Wu, S.; Chu, J. Biocementation for sand using eggshell as calcium source. J. Geotech. Geoenviron. Eng. 2016, 142 (10), 06016010. (22) Liang, Y.; Zhao, X. F.; Chi, Z.; Rover, M.; Johnston, P.; Brown, R.; Jarboe, L.; Wen, Z. Utilization of acetic acid-rich pyrolytic bio-oil by microalga Chlamydomonas reinhardtii: Reducing bio-oil toxicity and enhancing algal toxicity tolerance. Bioresour. Technol. 2013, 133, 500−506. (23) Zhao, X. F.; Davis, K.; Brown, R.; Jarboe, L.; Wen, Z. Alkaline treatment for detoxification of acetic acid-rich pyrolytic bio-oil for microalgae fermentation: effects of alkaline species and the detoxification mechanisms. Biomass Bioenergy 2015, 80, 203−212. (24) Choi, S. G.; Park, S. S.; Wu, S.; Chu, J. Methods for calcium carbonate content measurement of biocemented soils, J Mater. Civil Eng. 2017 (In press). (25) Li, M.; Li, L.; Ogbonnaya, U.; Wen, K.; Tian, A.; Amini, F. Influence of Fiber Addition on Mechanical Properties of MICPTreated Sand. J. Mater. Civ. Eng. 2016, 28 (4), 04015166. (26) Zhao, Q.; Li, L.; Li, C.; Li, M.; Amini, F.; Zhang, H. Factors Affecting Improvement of Engineering Properties of MICP-Treated Soil Catalyzed by Bacteria and Urease. J. Mater. Civ. Eng. 2014, 26 (12), 04014094. (27) Al Qabany, A.; Soga, K. Effect of chemical treatment used in MICP on engineering properties of cemented soils. Geotechnique 2013, 63 (4), 331−339. (28) Stabnikov, V.; Chu, J.; Ivanov, V.; Li, Y. Halotolerant, alkaliphilic urease-producing bacteria from different climate zones and their application for biocementation of sand. World J. Microbiol. Biotechnol. 2013, 29 (8), 1453−1460. (29) Harkes, M. P.; van Paassen, L. A.; Booster, J. L.; Whiffin, V. S.; van Loosdrecht, M. C. M. Fixation and distribution of bacterial activity in sand to induce carbonate precipitation for ground reinforcement. Ecological Engineering 2010, 36 (2), 112−117. (30) Pollard, A. S.; Rover, M. R.; Brown, R. C. Characterization of bio-oil recovered as stage fractions with unique chemical and physical properties. J. Anal. Appl. Pyrolysis 2012, 93, 129−138. (31) Choi, S. G.; Wang, K.; Chu, J. Properties of Biocemented, Fiber Reinforced Sand. Construction and building materials 2016, 120, 623− 629. (32) ASTM D 2434. Standard Test Method for Permeability of Granular Soils (Constant Head); ASTM International: West Conshohocken, PA, 2006. (33) ASTM D 4219. Standard Test Method for Unconfined Compressive Strength Index of Chemical- Grouted Soils; ASTM International: West Conshohocken, PA, 2008.

biomass. A new soluble calcium source has been obtained from a mixture of limestone powder and acetic acid with pH adjustment. Such a calcium solution can replace CaCl2 for production of precipitated CaCO3 via MICP. The sand columns treated using the new calcium sources demonstrated similar engineering properties as those treated using CaCl2.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. ORCID

Zhiyou Wen: 0000-0002-6135-246X Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The authors would like to thank the Midwest Transportation Center, the U.S. Department of Transportation Office of the Assistant Secretary for Research and Technology for sponsoring this research. All experiments were performed at Iowa State University. Special thanks are given to Xuefei Zhao, Yu Tian, and Huahua Ouyang, all from Iowa State University, for their assistance with some of the presented experimental work.

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REFERENCES

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Sustainable Biocement Production via Microbially Induced Calcium

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