Coagulation and disinfection by-products formation potential of extracellular and intracellular matter of algae and cyanobacteria

Journal Pre-proof Coagulation and disinfection by-products formation potential of extracellular and intracellular matter of algae and cyanobacteria Ziming Zhao, Wenjun Sun, Ajay K. Ray, Ted Mao, Madhumita B. Ray PII:

S0045-6535(19)32909-1

DOI:

https://doi.org/10.1016/j.chemosphere.2019.125669

Reference:

CHEM 125669

To appear in:

ECSN

Received Date: 15 August 2019 Revised Date:

12 December 2019

Accepted Date: 13 December 2019

Please cite this article as: Zhao, Z., Sun, W., Ray, A.K., Mao, T., Ray, M.B., Coagulation and disinfection by-products formation potential of extracellular and intracellular matter of algae and cyanobacteria, Chemosphere (2020), doi: https://doi.org/10.1016/j.chemosphere.2019.125669. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier Ltd.

CRediT author statement Ziming Zhao: Conceptualization, Conducting experiment, Data analysis and Writing; Wenjun Sun: Conceptualization, Methodology, Ajay K Ray: Funding and Facility, Reviewing, Ted Mao: Conceptualization, Reviewing, Madhumita B Ray- Conceptualization, Supervision, Reviewing and Editing.

1

Coagulation and disinfection by-products formation potential of

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extracellular and intracellular matter of algae and cyanobacteria

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Ziming Zhaoa, Wenjun Sunb,c, Ajay K Raya, Ted Maod, and Madhumita B. Raya,∗∗

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a

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Ontario, N6A 5B9, Canada

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b

School of Environment, Tsinghua University, Beijing, 100084, China

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c

Research Institute for Environmental Innovation (Suzhou), Tsinghua University,

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Jiangsu, 215163, China

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d

Department of Chemical and Biochemical Engineering, Western University, London,

Trojan Technologies, London, Ontario, N5V 4T7, Canada

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Abstract

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Coagulation and flocculation can remove particulate algal cells effectively; however, they

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are not very effective for removing dissolved algal organic matter (AOM) in drinking

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water plants. In this work, optimum coagulation conditions using alum for both

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extracellular and intracellular organic matter of six different algal and cyanobacterial

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species were determined. Different coagulation conditions such as alum dosage, pH, and

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initial dissolved organic carbon (DOC) were tested. Hydrophobicity, hydrophilicty, and

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transphilicity of the cellular materials were determined using resin fractionation method. ∗

Corresponding author. Tel. +01 519-661-2111 ext. 81273; Fax: +01 519-661-3498 E-mail address: [email protected]

1

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The removal of DOC by coagulation correlated well with the hydrophobicity of the AOM.

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The disinfection by-product formation potential (DBPFP) of various fractions of AOM

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was determined after coagulation. Although, higher removal occurred for hydrophobic

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AOM during coagulation, specific DBPFP, which varied from 10-147 µg/mg-C was

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higher for hydrophobic AOM. Of all the six species, highest DBPFP occurred for

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Phaeodactylum tricornutum, an abundant diatom species in surface water.

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Keywords: Algal organic matter, coagulation, resin fractionation, hydrophobicity,

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disinfection by-product formation potential.

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Abbreviations AG

Aulacoseira granulata f. curvatulum

AOM

algal organic matter

CV

Chlorella vulgaris

DBPFP

disinfection by-products formation potential

DOC

dissolved organic carbon

EOM

extracellular organic matter

HAA

haloacetic acids

HAAFP

haloacetic acids formation potential

HPI

hydrophilic organic fraction

HPO

hydrophobic organic fraction

IOM

intracellular organic matter

MA

Microcystis aeruginosa

Msp

Merismopedia sp.

2

NOM

natural organic matter

PT

Phaeodactylum tricornutum

SQ

Scenedesmus quadricauda

SUVA

specific ultraviolet absorbance at 254 nm

THM

Trihalomethanes

THMFP

trihalomethanes formation potential

TPI

transphilic organic fraction

UFC

uniform formation conditions

UV254

ultraviolet absorbance at 254 nm

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1 Introduction

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Due to climate change and abundance of nutrients, frequent eutrophication and outbreak

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of algal blooms and phytoplankton growth in surface water are of global concern (Chang

31

et al., 2014; Pick, 2016; Yan et al., 2017; Faruqi et al., 2018). The particulate algal cells

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are removed well (> 95%) during coagulation and flocculation processes in drinking

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water treatment (Miao and Tao, 2009; Gonzalez-Torres et al., 2014; Ma et al., 2016),

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however, dissolved algal organic matter (AOM), which includes both extracellular

35

organic matter (EOM) and intracellular organic matter (IOM), are not removed well

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during coagulation (Ghernaout et al., 2010). Classified as the autochthonous natural

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compounds in water, AOM is composed of polysaccharide, proteins and humic-like

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substances (Zhang and Fu, 2018). AOM plays an important role in the aquatic ecosystem

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(Li et al., 2011) as a substantial portion of NOM is comprised of AOM (Pivokonsky et al.,

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2016). Consequently, AOM causes a series of problems in drinking water treatment

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processes such as increased coagulant demand, growth of biofilm causing fouling of the 3

42

membrane, blocking the activated carbon adsorption sites, and increased formation of

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precursors for disinfection by-products (DBP) during chlorination (Ghernaout et al., 2010;

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Zhu et al., 2015; Pivokonsky et al., 2016; Xie et al., 2016; Zaouri et al., 2017). Majority

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of available literature focuses on the DBP formation from allochthonous natural organic

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matter (NOM) from detritus materials and vegetation, only limited studies dealt with the

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DBP formation from autochthonous NOM due to phytoplankton growth; comprehensive

48

research is required to develop treatment strategies in drinking water treatment plant

49

(Tomlinson et al., 2016).

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The EOM is present at all stages of growth of the phytoplankton, chemical coagulants

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such as alum and pre-oxidation using chlorine (to facilitate better removal by coagulation)

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may cause damage to algal cell integrity leading to the release of IOM, which cause taste,

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odor and toxicity to water (Chow et al., 1999). Higher amount of THM formation

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occurred due to the release of IOM during pre-oxidation before coagulation (Lin et al.,

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2017). IOM can also be released to treated water if coagulated species remain in the

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bottom of sedimentation basin. However, the role of IOM vs EOM on the coagulation

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and DBPFP is

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Contradictory results are reported in literature on the nature of EOM and IOM and their

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performance in water treatment processes. It was reported that algal IOM to be mostly

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hydrophilic (Zhang and Fu, 2018) indicating low removal potential during coagulation,

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while IOM of Microcystis aeruginosa was reported to be more hydrophobic than EOM

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(Li et al., 2014). Conversely, algal EOM can act as flocculation aid improving the

63

coagulation efficiency (Wan et al., 2015). EOM also can form chelate complexes with

64

metal coagulants, significantly increasing the required dosage and reducing the treatment

not well established due to lack of comprehensive control studies.

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efficiency (Takaara et al., 2007; Garzon-Sanabria et al., 2013; Ghernaout, 2014).

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Therefore, the effect of AOM on coagulation in water treatment is still contradictory and

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specific to algal species (Tang et al., 2017) as the distribution of HPO and HPI fractions

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of AOM varies depending on the type of algae and stage of growth (Leloup et al., 2015).

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To the best of our knowledge, there has been no systematic comparison of DBP

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formation

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species of algae and cyanobacteria. An earlier research investigated DBP formation from

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only EOM of three cyanobacteria, one diatom and one green algae (Goslan et al., 2017).

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However, they did not study the effect of coagulation on the removal of EOM.

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Comprehensive control studies are needed to determine the roles of specific AOM

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originating from commonly found, abundant algal species in surface water, their removal

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using coagulant dosages relevant to drinking water treatment, and subsequent DBPFP

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evaluation. The objectives of this study were to: (i) optimize the coagulation conditions to

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remove AOM originated from four species of algae Chlorella vulgaris (CV),

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Scenedesmus quadricauda (SQ), Phaeodactylum tricornutum (PT), and Aulacoseira

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granulata f. curvata. (AG), and two cyanobacteria Microcystis aeruginosa (MA),

81

Merismopedia sp. (Msp), (ii) determine the IOM and EOM fractions of AOM for a

82

known concentration of algal/cyanobacterial cells, (iii) determine HPO, HPI and TPI

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fractions of the AOM, and their effect on the coagulation performance, and (iv)

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determine DBPFP after coagulation of the AOM of individual species. An attempt was

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undertaken to determine whether the common water quality parameter, SUVA can be

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used as an indicator for both coagulation performance and DBPFP of algal matter.

followed by coagulation under identical treatment conditions for different

5

87

Cyanobacteria (Microcystis aeruginosa, Merismopedia sp.) and green algae (Chlorella

88

vulgaris, Scenedesmus quadricauda) are the most abundant freshwater photosynthetic

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species in surface water during a bloom (Henderson et al., 2008; Ou et al., 2012;

90

Naceradska et al., 2017). Diatoms such as Phaeodactylum tricornutum, Aulacoseira

91

granulata f. curvata contributing to high concentration (> 10 mg/L) of DOC, are the

92

indicators of surface water quality, causing significant problems in water treatment

93

plants (Plummer and Edzwald, 2001; Smol and Stoermer, 2010). While nitrogenous

94

DBPs are potentially more genotoxic than carbonaceous DBP, they are formed at a much

95

lower concentration (Table S1). For example, Microcystis aeruginosa formed only 0.95

96

µg/mg- C haloacetonitriles (HANs) and 0.017 µg/mg-C NDMA compared to 18 µg/mg-C

97

and 13.65 µg/mg-C of HAA and THM, respectively (Zhou et al., 2015), and therefore

98

was not determined in this work. For brevity, hereafter, the test species will be designated

99

by the abbreviated names only.

100

2 Materials and methods

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2.1 Cultivation of algae and cyanobacteria

102

The four algal species and two cyanobacteria were purchased from Canadian

103

Phycological Culture Centre (CPCC) at Waterloo University (Waterloo, ON, Canada).

104

They were cultivated in 2 L conical flasks using specific medium (shown in Table S2)

105

for each species at 23 ± 2 oC using humidified air flow of 2 L/min. All solutions were

106

prepared from reagent-grade chemicals and Milli-Q water. Intermittent illumination

107

(3000 lx) at a light/dark cycle (16/8 hours shift) was provided to simulate natural light

108

condition (Villacorte et al., 2015). The growth of each species was monitored by cell

109

counting using hemocytometer under microscopy. Algae and cyanobacterial cultures 6

110

were harvested at the stationary growth phase (25-30 days, depending on the species)

111

(Wang et al., 2012) when the final cell concentrations were approximately 0.24-6.5 × 107

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cells/ml.

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2.2 AOM extraction

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EOM of algae was separated from the harvested cell suspension using a centrifuge

115

(Thermo Scientific Sorvall, Legend T Plus) at 3700 rpm and 30 min centrifugation time.

116

Subsequently, a 0.45 µm filter (hydrophilic acrylic copolymer, Pall Corporation) was

117

used to separate the supernatant containing EOM. The deposited algae on the filter was

118

washed three times using Milli-Q water. Four different methods were attempted for lysis

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of the algal cells to obtain IOM as: (i) using a bead-beater at a frequency of 3500 rpm for

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2 min mixing with silica beads (Geciova et al., 2002); (ii) applying ultrasonication at a

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frequency of 50 Hz for 10 min (Wang et al., 2007); (iii) autoclaving at 120 oC (Singha

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and Muthukumarappan, 2016) for 15-30 min (Prabakaran and Ravindran, 2011); (iv) 3

123

cycles of freeze (-18 oC) and thaw (40 oC) (Li et al., 2012). The resultant solution was

124

then filtered using 0.45 µm membrane disc filters to obtain the IOM. The EOM and IOM

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stock solutions were stored at 4 oC for no more than 48 hours before characterization or

126

preparing the feed water with a DOC concentration of approximately 10 mg/L for

127

coagulation. This concentration was chosen to make the water quality comparable to

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NOM concentration in drinking water plants, which is around 2-10 mg/L (Baghoth, 2012).

129

2.3 Characterization of AOM

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DOC of EOM and IOM was measured using a Shimadzu TOC–VCPN analyzer. Glucose

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solution was used as the standard to obtain the calibration curve with the detection limit

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of 0.1 mg/L. Temperature and pH were measured using a pH meter (Orion Model STAR 7

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A111). The UV/Vis spectrophotometer (Shimadzu Model 3600) was used to scan a range

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of absorbance values from 200 to 300 nm with a 1 cm quartz cell to obtain the UV

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absorbance at 254 nm (UV254). The specific UV absorbance (SUVA = UV absorbance at

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254 nm/DOC mg/L) (L·mg-1·cm), the widely used parameter for characterizing

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aromaticity of organics was determined for all AOM samples.

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2.4 Determination of HPI and HPO fractions

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The resin fractionation method had been used to separate organic matter of the source

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water into HPO, TPI, and HPI fractions by adsorption using DAX-8 (Supelite, USA) and

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XAD-4 (Amberlite, USA) resins in a column successively (Chen et al., 2007; Qu et al.,

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2012; Su et al., 2017) (Figure 1). The process is based on surface adsorption equilibrium

143

between the resin and the organic matter in water. The column capacity factor
 shown in

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the equation (1) (Labanowski and Feuillade, 2011) is the ratio of the amount of organic

145

 matter retained by resin ( ) to the concentration of initial organic matter

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influent (   ),

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  =
 ×   

(1)

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The volume of influent passed through the column can be calculated using equation (2)

149

(Labanowski and Feuillade, 2011), where the void volume  =  × ,  is the bed

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volume of resin and P is the resin porosity (0.65).

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 = 2 (1 +
 )

(2)

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Where V is the volume of AOM solution passed through the column. A value of 50 for

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 was generally accepted to be the column capacity for humic substances separation in

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several investigations (Marhaba et al., 2003; Chow, 2006; Piper, 2010; Lin et al., 2014; 8

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Ma et al., 2014; Pivokonsky et al., 2014). It was demonstrated that increasing the column

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capacity factor
 would cause lower retention of the HPO fraction on the column due to

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higher flow rate causing decreased yield of HPO fraction (Orr, 2009; Labanowski and

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Feuillade, 2011; Shapiro and Karavanova, 2014). Therefore, a lower column capacity of

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30 was applied in order to adsorb most of the HPO fraction in AOM solutions by DAX-8

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resin. About 310 mL EOM or IOM solution with initial DOC of 10.43 ± 0.80 mg/L, and

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pH 2 (adjusted by 10 M HCl) was passed through two 20 mm length glass columns

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connected in series and filled with 8 mL of DAX-8 and XAD-4 resin (Fig. S1)

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respectively, using a constant flowrate of 3 mL/min. While HPI fraction passes through

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both DAX-8 and XAD-4 columns, HPO and transphilic fractions are adsorbed onto

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DAX-8 resin and XAD-4 resin, respectively. Thereafter, same volume (310 mL) of 0.1 M

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NaOH as the initial water sample, was applied to elute the HPO and TPI fractions from

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DAX-8 and XAD-4 column, respectively using the same flowrate (3 mL/min). DOC of

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each fraction was measured using the TOC analyzer described earlier. Before

169

fractionation, the resins were rinsed with methanol, 0.1 M NaOH, 0.1 M HCl and Milli-Q

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water until the DOC of the effluent was same as that of Milli-Q water. Recovery of each

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fractionation determined from the DOC values was within 95-108%.

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2.5 Coagulation of AOM

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Coagulation experiments were conducted using a Phipps & Bird programmable apparatus

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(Model PB900) with six stainless steel paddles at room temperature (~24 oC) in 500 mL

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beakers. Commonly used coagulant (Al2(SO4)3·18H2O) was added with a dosage varying

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from 30 to 60 mg/L (2.4-4.8 mg/L of Al3+) at a pH between 5.0-8.0 (adjusted by adding

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either 1N HCl or 1N NaOH); a relatively higher dosage than usual 30 mg/L in drinking 9

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water treatment plant was tried for enhanced coagulation. Coagulation experiments

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included rapid coagulation at 150 rpm for 2 minutes, followed by a slow stirring at a

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speed of 25 rpm for 20 minutes for floc growth. Thereafter, a settling time of 30 minutes

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was applied to precipitate the formed flocs, and the supernatant was analyzed to

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determine the residual DOC and UV254 values after coagulation.

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2.6 Chlorination and DBPs analysis

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Chlorination of the coagulated water was conducted according to the uniform formation

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conditions (UFC) at pH 8.0 ± 0.2 with a borate buffer solution (Summers et al., 1996).

186

Subsequently, a combined hypochlorite-buffer dosing solution was added to the water

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samples with the free chlorine dosage of 1.8 times initial DOC of the water sample (Hu,

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2016) and stored in headspace-free amber glass bottles in dark at ambient temperature

189

(20 ± 1 oC) for 24 hours and keep the residual free chlorine within 1.0 ± 0.4 mg/L. After

190

24 hours of incubation, stoichiometric amount of ammonium chloride was added to

191

quench the free residual chlorine in water to obtain the THMFP and HAAFP. The

192

formation

193

bromodichloromethane (BDCM), dibromochloromethane (DBCM) and tribromomethane

194

(TBM), extracted with methyl tert butyl ether (MTBE) by liquid-liquid extraction

195

following the method of USEPA 551.1 were determined. The six HAA6,

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monochloroacetic acid (MCAA), monobromoacetic acid (MBAA), dichloroacetic acid

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(DCAA), dibromoacetic acid (DBAA), bromochloroacetic acid (BCAA), and

198

trichloroacetic acid (TCAA) were extracted from water samples following the modified

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USEPA method 552.3. The DBPs were determined using a GC-ECD (Shimadzu GC-

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2014) with BPX5 capillary column (30 m× 0.25 mm ID, 0.25 µm film thickness).

potentials

of

four

major

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THM4,

trichloromethane

(TCM),

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DBPFP (µg/mg- C) yields were normalized by dividing the concentration of DBP (in

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µg/L) by the DOC (in mg/L).

203

3 Results and discussion

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3.1 Cell growth and EOM, IOM separation

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All the algae and cyanobacteria (axenic cultures) were harvested at their stationary

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growth stage after 25-30 days of cultivation using condition mentioned earlier. The

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maximum specific growth rates (µmax, d-1) of CV, SQ, MA, Msp, PT and AG were 0.514

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day-1, 0.362 day-1, 0.553 day-1, 0.602 day-1, 0.869 day-1 and 0.585 day-1, respectively,

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which are comparable with earlier studies at similar condition (Li et al., 2013; Li et al.,

210

2014; Singh and Singh, 2015; Podevin et al., 2017). In the stationary phase, the algal

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population reached the maximum cell concentration of about 21.75 × 106 cell/mL for PT,

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9.26 × 106 cell/mL for SQ, 9.30 × 106 cell/mL for Msp, 65.38 × 106 cell/mL for CV,

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36.69 × 106 cell/mL for MA, and 2.35 × 106 cell/mL for AG. Of the two diatoms, PT and

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AG, PT grew much faster than AG, followed by the two cyanobacteria.

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In order to obtain the IOM, several cell disintegration methods mentioned earlier were

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applied using ubiquitous green algae, CV, and the results are shown in Fig. S2. Of the

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various methods applied for extraction of IOM, autoclaving produced the maximum DOC

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and SUVA, followed by 3 cycles of freeze and thaw. However, autoclaving was not used

219

in further experiments as some alteration (hydrolysis) and degradation of organics

220

structure may occur during autoclaving (Barsanti and Gualtieri, 2014). It should be noted

221

that the chemical composition and microstructure can also be affected by the rate of

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freezing and thawing (Singha and Muthukumarappan, 2016), however, may not be as

11

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drastic as autoclaving. For consistency, freezing and thawing time was kept constant at

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12 h at -18 C and 4 h at 25 C, respectively (Li et al., 2012). Production of both EOM and

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IOM increased with cultivation time until the stationary phase was reached for all six

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species. DOC of EOM and IOM extracted from each species with cultivation days are

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shown in Fig. S3. The constituents of cellular matter such as protein, carbohydrate and

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lipid vary significantly based on the species and their growth phase. Therefore, harvesting

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of the algae and cyanobacteria was conducted once they all reached stationary stage for

230

consistency and the final values are summarized in Table S2.

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The diatom PT had the highest EOM excretion followed by the two species of

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cyanobacteria MA and Msp for equivalent cell density, and DOC of EOM from each

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species was higher than that of IOM at the stationary phase, which compares with the

234

results from (Li et al., 2018). SUVA varied between 0.263 and 0.861 L/mg-m, as shown

235

in Table S2; showing relatively lower aromaticity compared to NOM which can range

236

from 1.8 to 4.4 L/m-mg (Edris et al., 2012). SUVA values for the IOM were slightly

237

higher than that of the EOM, except for PT, which showed slightly higher SUVA for

238

EOM than IOM. The IOM of diatom AG showed the highest SUVA value. The SUVA

239

followed the similar trend as the DOC, and compared well with literature (Hansen et al.,

240

2016). A low SUVA also suggests that IOM from CV is more of hydrophilic in nature

241

(Yang et al., 2011) and mainly comprised of protein-like substances, instead of humic

242

like matters (Li et al., 2012).

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3.2 Removal of EOM and IOM by Coagulation

244

A relatively wide range of alum dose (30-60 mg/L) was tested for the removal of DOC

245

and UV254 of EOM and IOM (initial DOC of 8.5 ± 1.5 mg/L) of each species. Although 12

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the dosage of alum depends on initial DOC concentration, a typical dosage of 30 mg/L is

247

quite common in a water treatment plant. The higher dosage was used to test whether

248

enhanced coagulation could be achieved using 40-60 mg/L (Fig. S4). The results

249

indicated that DOC removal efficiency generally increased with increasing alum dosage,

250

but it reached a plateau around 40 mg/L for most cases with the exception of IOM of CV,

251

EOM of SQ and EOM of Msp. Hence, there was no benefit in increasing alum dosage

252

beyond this dosage for most of the cases. DOC removal efficiency of EOM followed the

253

order of PT (82.69 ± 3.43%) > AG (69.90 ± 4.48%) > MA (65.29 ± 0.76%) > Msp (59.99

254

± 4.42%) > CV (24.95 ± 0.83%) > SQ (21.55 ± 0.77%). Comparing the results with EOM,

255

removal of IOM was slightly lower than EOM and varied between 19.31 ± 3.84% and

256

59.09 ± 2.41 with highest removal occurred for MA and the lowest removal occurred for

257

SQ. The removal efficiency of IOM at optimum condition of alum dosage of 40 mg /L

258

and pH 5 followed the order of MA (58.93 ± 0.29%) > Msp (49.28 ± 0.32%) > AG

259

(47.50 ± 1.24%) ≈ PT (47.27 ± 0.32%) > CV (37.67 ± 2.11%) > SQ (20.54 ± 2.01%).

260

Thus, removal of AOM of CV and SQ by coagulation was not very effective.

261

The UV254 removal followed very similar trend as that of DOC removal. In most cases,

262

DOC removal was correlated to the SUVA value of the species with some exceptions. In

263

general, aromatic compounds were better removed during coagulation. It was reported

264

that for SUVA < 3, DOC is hydrophilic, low in molecular weight and in charge density,

265

and only slightly affected by coagulation (Edzwald, 1993). This could explain the

266

deviation in coagulation performance for both EOM and IOM with respect to SUVA as

267

the SUVA of all cellular materials of AOM varied only from 0.24 to 0.861 L/m-mg. The

13

268

results of coagulation of DOC and UV254 at alum dose of 30 mg/L are presented in Table

269

1.

270



271

The effect of pH on coagulation in the range of 5-8 was tested and the results presented in

272

Fig. 1 indicate that the DOC removal for AOM decreased with increasing pH, which is

273

consistent with an earlier study (Shu-xuan et al., 2014). Maximum DOC removal for

274

EOM occurred at pH 5-6; at pH 5 and at a coagulant dose of 30 mg/L, monomeric Al

275

(OH)2+and polynuclear Al ((OH)! ) are the dominant species involved in charge

276

neutralization of negative (especially carboxyl-) groups of AOM (Hu et al., 2006). At pH

277

≥ 6.0, the Al (OH)4- species are dominant causing decreased DOC removal efficiency

278

(Lee et al., 2012).

279

At pH 6 and a higher coagulant dose, restabilization may occur decreasing the removal of

280

both DOC and UV254. Since most of the dose-response curves remained flat at higher

281

Al-dosage, charge reversal did not occur during AOM coagulation. The effect of pH is

282

more significant for the DOC removal than UV254 as can be seen in Fig. 1.

283



284

Aromaticity of algal matter is primarily due to proteins and amino acids, and pKa1 of

285

many aromatic acids is in the range of 1.82-2.83, with isoelectric points around 5.07-7.59

286

(Hunt and Spinney, 2006). Therefore, in the test pH range, compounds contributing to

287

aromaticity probably remained neutral and their removal was not affected significantly by

288

pH. Interaction of EOM with soluble aluminum ions may cause EOM-metal complexes

14

289

that will remain in solution until either the binding capacity of the EOM is satisfied, or

290

the solubility of the metal-AOM complex is exceeded (Gregor et al., 1997). However, the

291

complex formation potentially decreases the coagulation efficiency. The increase in DOC

292

removal was incremental for an increase in pH from 5.0 to 6.0, with a maximum of 20%

293

increase in EOM removal for Msp. For other algae, the increase in DOC removal was

294

less than 8% when pH was decreased from 6.0 to 5.0. Conversely, low pH will require

295

pH adjustment before final distribution of water. Considering the possibility of corrosion

296

at lower pH and higher chemical consumption, although pH 5.0 and 40 mg/L may be

297

considered as the enhanced coagulation condition for removal of both EOM and IOM, pH

298

6.0 was chosen for further experiments. During NOM coagulation, better performance

299

was observed for HPO fraction of the DOC (Ghernaout, 2014). Therefore, an effort was

300

made to fractionate the cellular materials of all six species and determine the effect of

301

hydrophobicity on coagulation.

302

3.3 Hydrophobicity of AOM and correlation with coagulation

303

The HPO, HPI and TPI contents of EOM and IOM are shown in Fig.2. The HPI fraction

304

was the dominant fraction for all species and varied between 50 and 70%, consistent with

305

the earlier published results (Her et al., 2004; Henderson et al., 2008; Li et al., 2012;

306

Zhang et al., 2016). Green algae has more HPI fraction than cyanobacteria, which is in

307

accordance with Zhang et al. (Zhang et al., 2016), where only 11% AOM of CV was

308

HPO compared to 30% of MA (Henderson et al., 2010). In our work, the relatively higher

309

HPO fraction in AOM of MA and MSP, 35.17±3.01% and 46.16 ±1.41%, respectively,

310

compared to 30% HPO in MA-EOM (Henderson et al., 2008; Zhang et al., 2013) is

311

probably due to lower column capacity of 30 used as explained earlier. The HPO and 15

312

HPI contents of EOM and IOM for various species were quite similar, except for PT and

313

Msp as shown in Figure 2. The HPO fraction was higher for both EOM and IOM of PT,

314

and it was higher for the IOM of Msp. Therefore, the highest removal of AOM by

315

coagulation occurred for PT. Similarly, IOM removal of Msp was the second highest at

316

49.28 ± 0.32%, indicating the importance of hydrophobic fraction in coagulation.

317

The TPI of EOM/IOM from each species varies between 8.71 ± 0.95% and 14.98 ±

318

0.66%. TPI is of intermediate polarity isolated from the XAD-4 resin, and although the

319

exact chemical identity of TPI is not known, they are similar to HPI with a high

320

proportion of carboxylic acid functionality (Aiken et al., 1992) and may not be removed

321

well due to coagulation. Except for PT, all the other species investigated in this work had

322

higher HPO fraction in IOM than that in EOM, which is in agreement with the results

323

from (Fang et al., 2010), where IOM from MA contained more HPO fraction with higher

324

MW than EOM.

325



326

The cellular composition of each species obtained from literature is presented in Table

327

S3. The HPI fraction including carbohydrates and proteins are dominant constituents of

328

each species. All AOM investigated was predominately HPI with low SUVA except PT.

329

It has the highest amount of protein and lipid percentage than other algae, which may

330

account for its relatively higher HPO ratio (Prestegard et al., 2015).

331

It was reported that the ratio of HPO and HPI organic matter can be used as an indicative

332

parameter to quantify the treatability of NOM, especially DOC (Xing et al., 2012;

333

Ghernaout, 2014). During coagulation-flocculation process, AOM can also act as a ligand

334

to bind hydrous aluminum in-situ forming gelatinous precipitate, which can act as 16

335

adsorption sites for further AOM (Chithra and Balasubramanian, 2010). Since the TPI

336

fractions with carboxylic acid are more hydrophilic than hydrophobic, the DOC removal

337

of AOM for all six species was plotted with the ratio of HPO to (HPI +TPI) (Fig. 3).

338



339

The DOC removal increased with the increase of HPO/(HPI+TPI) ratio until the value

340

reached 0.8 showing a non-linear behavior (fitted using Origin Pro 9.0 LangmuirEXT1

341

with the parameters shown in Table S4) (Jin et al., 2012). Equation (3) shown below

342

fitted the experimental data well with correlation co-efficient R2 ≥ 85% (Table S4) for

343

alum dosage of 30 and 40 mg/:  ∙ $ (%&')

" = (! $ (%&')

344

(3)

345

where, y represented the DOC removal percentage, which is equivalent to fractional

346

coverage, θ, in the most used Langmuir adsorption isotherm ) =

347

2017). The x is the ratio of HPO/(HPI+TPI), which indicates the hydrophobicity of AOM

348

solution, and b is equal to the equilibrium constant K (K = ka/kd), where ka and kd are the

349

rate constants for adsorption and desorption, respectively. The value of b in Equation (3)

350

illustrates how the coagulant flocs or particulates surface sites become saturated as the

351

hydrophobicity of the solution rises. The magnitude of b quantifies the affinity of the

352

AOM for surface adsorption. The a and c are fitting parameters without much physical

353

significance.

354

The removal of AOM varies from 53.36% to 64.89% with the increase of alum dosage

355

from 30 to 50 mg/L (Fig. 3), more scatter in data can be seen at alum dosage of 50 mg/L.

17

*+ (!*+

(Ayawei et al.,

356

Such high alum dosage is not advised due to adverse effect of Al3+ in treated water. The

357

higher value of constant “b” (Table S4) at 30 mg/L indicates greater dependence of

358

coagulation performance on dosage at lower HPO/(HPI+TPI) ratios. It is interesting to

359

see that higher than 65% AOM removal was not possible even at HPO/(HPI+TPI) ≥1.0

360

and at a higher alum dosage, and overdosing was not achieved, indicating charge reversal

361

or restabilization of polymeric species were not factors, and no precipitation also can be

362

observed.

363

3.4 DBP formation potential of various fractions of AOM

364

After chlorination using UFC method (described in the methods section), the specific

365

DBPs produced by EOM and IOM from six species are shown in Fig. S5. In agreement

366

with the coagulation results presented earlier, specific THM and HAA formation

367

potential remained constant for different doses of alum for all species. This is expected as

368

the DBPFP was normalized with the corresponding DOC values; constant values indicate

369

good reproducibility of coagulation and DBPFP experiments. A small increase/decrease

370

in formation potential is mostly due to analytical error. Despite higher removal of DOC

371

for PT, it showed (Table 2) the highest amount of DBP formation potential with 146.0 ±

372

16.64 µg/mg-C of HAAs and 124.01 ± 11.07 µg/mg-C of THM from the EOM, and 91.80

373

± 1.02 µg/mg -C HAAs and 75.91 ± 2.50 µg/mg-C THM from the IOM, respectively. PT

374

produced large amount of AOM, especially relatively higher percentage of lipids causing

375

higher amount of polyunsaturated fatty acids released by autolysis of the cells. Except PT

376

and MA, IOM from four other species (CV, SQ, Msp and AG) presented higher specific

377

HAAFP and THMFP than the corresponding EOM probably due to the higher aromatic

378

and aliphatic proteinaceous substances in IOM with higher activity for chlorine 18

379

substitution. Amino acids as the important constituents of algal organic matter have been

380

reported for HAA formation (Bond et al., 2011), whereas carboxylic moieties in EOM

381

likely to be unfavorable for substitution reaction with chlorine (Hua et al., 2017).

382

The DBPFP values produced in this work are in the range of limited values found in

383

literature for different algae. Relatively higher proportion of HPO fraction in IOM than

384

EOM from MA was also reported by (Li et al., 2018). Higher THM formation for the

385

MA-IOM as 20 µg/mg- C as compared to 10 µg/mg- C for the MA-EOM was reported

386

(Ali et al., 2015). Another study reported specific yields of chloroform, chloroacetic acid

387

to be 32.44, 54.58 µg/mg-C, respectively for MA-EOM, and 21.46, 68.29 µg/mg-C for

388

MA-IOM (Li et al., 2018). The two cyanobacteria (MA and Msp), with higher nitrogen

389

fixation capability and releasing up to 45% of organic nitrogen (Westerhoff and Mash,

390

2002), caused substantial amount of THM and HAA formation. Both MA and Msp

391

contain significant amount of proteins in their AOM (Table S3); organic nitrogen also

392

contributes to a large amount of active sites to derive THM and HAA (Huang et al., 2009;

393

Hwang et al., 2011). Amino acids can

394

dichloroacetonitrile to react with chlorine and form THMs an HAAs (Reckhow et al.,

395

2001).

396

The correlation between SUVA and specific DBP formation potential (HAAPF and

397

THMPF) from AOM is presented in Fig. 4 with the correlation coefficients of 0.718 and

398

0.662 for specific HAAFP and specific THMFP, respectively.

399

produce an unstable intermediate



19

400

Higher correlation coefficients 0.83 and 0.81 for HAAFP and THMFP, respectively with

401

SUVA were obtained by (Park et al., 2019), for NOM in algal-rich water with a DOC

402

solution of much higher SUVA of 2-5 L/m·mg. Generally, DBPFP prediction capability

403

of SUVA is weak in water with low SUVA values (Ates et al., 2007). An attempt was

404

made to evaluate the DBPFP of each fraction (HPI, TPI and HPO) from AOM, following

405

the UFC method and the results are shown in Fig. 5.

406



407

It can be seen that the HPO fractions are the dominant DBP precursors, only exception of

408

EOM of SQ, which had one of the lowest SUVA value. The results are consistent with an

409

earlier study where more reactive HPO materials in water resulted higher DBPFP (Golea

410

et al., 2017). These results suggest that HPO/HPI ratio is a good indicator for THMFP for

411

DOM irrespective of the nature and source of DOM.

20

412

4 Conclusions

413

Coagulation performance and DBPFP for both extra- and intra-cellular materials of four

414

algae and two cyanobacteria were determined. The work conclusively has shown that at

415

optimum coagulation condition of pH 6 and alum dosage of 40 mg/L, an average of 47.43%

416

and 40.43% AOM removal in terms of DOC and UV254 could be achieved. The DOC

417

removal correlated well with the HPO/(HPI +TPI) ratio and SUVA. The DBPFP was

418

determined using uniform formation condition and the specific DBP value varied from

419

14.83 ± 0.56 µg/mg-C to 146.26 ± 16.64 µg/mg-C. The diatom, PT, produced the highest

420

amount of DBP followed by the cyanobacteria Msp. The HPO fractions of cellular

421

material contributed maximum to the DBPFP, which is moderately correlated to SUVA

422

(R2 ≈ 0.662-0.718), probably due to low SUVA values of AOM. Although, HPO fraction

423

of the cellular material was removed better during coagulation, higher specific DBPFP

424

also occurred for this fraction for most species. Similar to NOM, SUVA and

425

hydrophobicity of AOM can be used as surrogate parameters to predict the coagulation

426

performance and DBPFP from AOM. Although, IOM produces higher amount of DBP,

427

their concentration in natural water is low except for massive algal bloom collapse or

428

during pre-oxidation before coagulation.

429

Acknowledgment

430

This work was financially supported by the Ontario-China Research and Innovation Fund

431

(OCRIF) “Ensuring Water Supply Safety in Beijing: Water Diversion from South to

432

North China” (No.2015DFG71210). This work was also supported by grants from the

433

China National Water Major Project (No. 2012ZX07404-002, 2017ZX07108-003,

434

2017ZX07502003). 21

435

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List of Table captions

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Table 1 The AOM removal by coagulation with an alum dosage of 30 mg/L and 23 oC

695

without pH control

696

Table 2 Average Specific DBPFP for various species after coagulation

697

34

698 699

List of Figure captions

700

Fig. 1 Effect of pH on DOC and UV254 removal of EOM (a, b), of IOM (c, d) with alum

701

dosage of 40 mg/L and initial DOC 8.5 ± 1.5 mg/L from individual algae and

702

cyanobacteria.

703

The error bar represents the standard deviation of triplicate experiments.

704

Fig. 2 Resin fractionation results of EOM and IOM for the six species (DOC recovery

705

varied from 95-108%)

706

Fig. 3 Correlation of HPO/(HPI+TPI) with DOC removal at different alum dosages. The

707

error bar represented the standard deviation of triplicate experiments.

708

Fig. 4 Correlation between SUVA of AOM and formation of HAAPF(a),THMFP (b).

709

The error bar represented the standard deviation of triplicate experiments.

710

Fig. 5 HAAFP and THMFP percentage of HPI, TPI and HPO fractions of different

711

species.

35

Algal species

EOM

IOM

DOC

UV254

DOC

UV254

CV

36.07 ± 1.30

43.75 ± 2.42

35.12 ± 0.32

43.41 ± 1.17

SQ

16.96 ± 0.84

19.35 ± 1.52

20.75 ± 0.31

19.83 ± 1.49

MA

76.40 ± 0.91

56.71 ± 1.49

61.81 ± 0.26

47.83 ± 2.05

Msp

59.62 ± 1.15

29.55 ± 3.21

41.42 ± 0.29

26.36 ± 1.29

PT

61.56 ± 7.29

32.60 ± 1.89

52.82 ± 7.17

82.00 ± 2.83

AG

70.51 ± 2.13

40.00 ± 4.95

36.07 ± 1.30

43.75 ± 2.42

*The values are shown as mean ± standard deviation (n=3).

Specific HAAFP (µg/mg-C)

Specific THMFP (µg/mg-C)

Algae species EOM

IOM

EOM

IOM

CV

14.83 ± 0.56

22.20 ± 2.86

12.66 ± 1.74

17.68 ± 0.77

SQ

23.36 ± 0.29

25.77 ± 0.41

14.17 ± 0.42

22.67 ± 2.83

MA

28.46 ± 3.74

30.52 ± 3.13

21.34 ± 2.98

24.44 ± 0.83

Msp

62.98 ± 4.82

65.30 ± 4.99

54.66 ± 4.78

62.61 ± 10.37

PT

146.26 ± 16.64

91.80 ± 1.02

124.01 ± 11.07

75.91 ± 2.50

AG

56.80 ± 14.83

66.30 ± 3.36

72.91 ± 2.50

56.92 ± 5.58

*The values are shown as mean ± standard deviation (n=3)

Highlights

Coagulation and disinfection by-products formation potential of extracellular and intracellular matter of algae and cyanobacteria Ziming Zhaoa, Wenjun Sunb,c, Ajay K Raya, Ted Maod, and Madhumita B. Raya,∗∗

a

Department of Chemical and Biochemical Engineering, Western University, London, Ontario, N6A 5B9, Canada b

School of Environment, Tsinghua University, Beijing, 100084, China

c

Research Institute for Environmental Innovation (Suzhou), Tsinghua University, Jiangsu, 215163, China d

Trojan Technologies, London, Ontario, N5V 4T7, Canada

•

Only a maximum of 60% removal of algal organic matter (AOM) occurred by coagulation.

∗

•

AOM removal by coagulation correlated well with the hydrophobicity of AOM.

•

The hydrophobic fractions of AOM contributed maximum to the DBP formation.

•

DBP formation potential is moderately correlated to SUVA values of AOM.

Corresponding author. Tel. +01 519-661-2111 ext. 81273; Fax: +01 519-661-3498 E-mail address: [email protected]

Declaration of interests ☒ The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. ☐The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: