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The use of desalination concentrate as a potential substrate for microalgae


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DOI: 10.1016/j.algal.2016.08.003

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Algal Research

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The use of desalination concentrate as a potential substrate for


microalgae cultivation in Brazil
Ângelo P. Matos ⁎, Elisa H.S. Moecke, Ernani S. Sant'Anna
Department of Food Science and Technology, Federal University of Santa Catarina, Av. Admar Gonzaga 1346, Itacorubi, 88034-001 Florianópolis, SC, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: Desalination concentrate produced by inland desalination plants can potentially provide water and nutrients for
Received 31 March 2016 algal growth. Several studies have been conducted in Brazil to explore the use of desalination concentrate as an
Received in revised form 22 June 2016 alternative medium for microalgae cultivation. This review describes examples of microalgae cultured in desali-
Accepted 1 August 2016
nation concentrate and evaluates the effects of desalination concentrate on algal biomass productivity, lipid con-
Available online xxxx
tent, lipid productivity, protein, and fatty acids composition.
Keywords:
© 2016 Published by Elsevier B.V.
Microalgae
Inland desalination wastewater
Biomass composition
Lipid productivity
Biofuels

1. Introduction source of water and nutrients is of special interest for utilizing and
recycling inland desalination wastewater, which is loaded with microel-
Microalgae are promising sources of biomass, bioproducts, and bio- ements useful for algal biomass production [11]. Experimental studies
fuel and have become an extensive area of research [1–4]. One of the ad- on the use of DC as an alternative medium for microalgae, particularly
vantages of some microalgae species is their high content of lipids and studies that also assess variables that determine maximal algal biomass
the composition of their fatty acids, mainly medium-chain carbon (C16 production and biochemical composition, will have significant benefits
and C18), triacylglycerols (TAG), which can be chemically converted for the evaluation of wastewater-grown microalgae in Brazil.
into biodiesel [5]. The majority of commercially available biofuels in This mini-review summarizes the main results of studies in Brazil on
Brazil are currently bioethanol derived from sugar cane and biodiesel the use of DC as an alternative medium for microalgae cultivation with a
derived from oil crops, including soybean [6]. It has been proposed to focus on the physicochemical characteristics of DC, the impact of this
derive biofuels from the cultivation of algae, because of their ability to medium on algal growth, biomass productivity, and biochemical com-
grow well in marginal water resources and in non-agricultural land, position (protein, lipids and fatty acids composition) are discussed. In
and because of their greater photosynthetic efficiency compared with addition, the effects of N/P ratio and salinity parameters in the optimum
land plants. In addition, using algae cultures as a source for biofuels DC concentration for three microalgae species (Chlorella vulgaris, Spiru-
will reduce the need to compete with resources utilized in conventional lina (Arthrospira) platensis and Nannochloropsis gaditana) are also
agriculture [2,3]. discussed.
Several microalgae species can effectively grow in wastewater con-
ditions through their ability to utilize abundant organic carbon and in-
organic N and P [7]. Most of the research on algal wastewater 2. Combining desalination concentrate and microalgae cultivation
treatment has come from the analysis of laboratory-based small scale
and pilot pond-scale cultures [8]. A wide range of studies have analyzed 2.1. Desalination of brackish groundwater in Brazil
the growth of microalgae under a variety of wastewater conditions, in
particular growth in multiple municipal, industrial and agricultural South America has huge natural inland salts deposits in arid zones. In
wastewaters [2,9,10]. These studies have mainly been focused on eval- Brazil, inland deposits of brackish waters are common in the Northeast
uating the ability of algae to remove N and P, and in some instances of Brazil that has a semi-arid climate and recurrent droughts. This part
metals, from wastewater. In Brazil, desalination concentrate (DC) as a of Brazil is an exceptional example of inland desalination and brine
management, partially because of a massive governmental program
⁎ Corresponding author. launched in 2004 named ‘Água Doce’ (Fresh Water) that has benefitted
E-mail addresses: matos.a@posgrad.ufsc.br, angelosotam@gmail.com (Â.P. Matos). 150,000 inhabitants of the semiarid region of Brazil [12].

http://dx.doi.org/10.1016/j.algal.2016.08.003
2211-9264/© 2016 Published by Elsevier B.V.

Please cite this article as: Â.P. Matos, et al., The use of desalination concentrate as a potential substrate for microalgae cultivation in Brazil, Algal
Res. (2016), http://dx.doi.org/10.1016/j.algal.2016.08.003
2 Â.P. Matos et al. / Algal Research xxx (2016) xxx–xxx

Desalination through reverse osmosis is the most suitable solution to may affect C. vulgaris growth, while DC can contain resides of pretreat-
provide water supply in the semiarid region of Brazil. It is estimated that ment and cleaning chemicals, and their reaction byproducts which
there are 1500 desalination installations in this part of Brazil [13]. All de- may also have adverse affects on aquatic organisms [23].
salination technologies produce a stream of fresh water and a highly When DC was tested in the same way mixed with Paolettic Synthetic
concentrated stream of minerals and contaminants [13,14]. In the semi- Medium as an alternative culture medium to grow Spirulina platensis, it
arid region of Brazil, DC from inland desalination of brackish groundwa- was found that the optimal DC concentration for S. platensis growth is
ter is mainly used for aquaculture (fish farming), for hydroponic and soil 50% DC (~ 2.5 mS cm− 1) [21]. On the other hand, marine
cultivation (lettuce, tomatoes, beetroot, cotton and sunflower) and for Nannochloropsis gaditana performed well when exposed to a high DC
direct irrigation of halophyte forage shrubs (Atriplex nummularia) [12, concentration of 75% (~8.0 mS cm−1) [11], at which lipid productivity
15,16]. The fact that part of the DC flow can be used for algaculture is (12.10 mg L−1 day−1) was higher than lipid productivity of C. vulgaris
an additional and promising opportunity to exploit the valuable compo- (7.37 mg L−1 day−1) and S. platensis (6.97 mg L−1 day−1). These exam-
nents in desalination wastewater. ples of the influence of DC on algal growth suggest that DC is a good me-
It is well known that microalgal growth is influenced by environ- dium for marine algae strains such as N. gaditana, but that the ionic
mental parameters, such as salinity [17]. A change in salinity in algal cul- concentration of DC is too high for the cultivation of the freshwater C.
tivation can have positive effect on the metabolism of algae [18], vulgaris and S. platensis. The results of studies on the optimal DC concen-
especially on important cell membrane constituents, such as lipids and tration for cultivation of three microalgae species are summarized in
fatty acids [19]. The salt concentration influences algae via effects on os- Table 2.
motic stress, salt stress, and cellular ionic ratios [20]. Each microalgal Different salinities in terms of NaCl concentration in the optimum
strain grows optimally at a specific salinity, but some microalgae can DC medium for three algae species have been reported in the literature,
take advantage of different salinities. For example, the halophilic for C. vulgaris (0.01 M NaCl) [22], S. platensis (0.05 M NaCl) [21] and N.
chlorophyte genus Dunaliella viridis can grow at low (0.3 M NaCl) and gaditana (0.17 M NaCl) [11]. Among the three microalgae species tested
at high (2.3 M NaCl) salinity [18]. in optimum DC concentration, marine N. gaditana has better ability to
cope with osmotic changes and alterations in the salt ratios than fresh-
2.2. Desalination concentrate and algal cultivation water algae species, because it has the capability to tolerate a broader
range of DC-salinities with a satisfactory growth. For example, when
Desalination concentrate is rich in inorganic minerals, such as Cl−, marine N. gaditana was cultured in F/2-seawater medium (0.5 M
Na+ and Ca2+, contains other nutrients (N and P) and trace elements NaCl) and induced to a hypotonic salinity, i.e. to brackish DC medium
necessary for microalgae growth, including Si, K+, Mg+ 2, Fe+3, and (0.17 M NaCl), biomass concentration and lipids enhanced from 0.71
electrical conductivity normally ranges from 4.0 to 5.5 mS cm− 1 to 0.96 g L−1 and 4.7 to 12.6%, respectively. These results suggest that
(Table 1). Since it is known that DC contains abundant amounts of min- marine N. gaditana production for lipids work well when exposed to
eral salts, DC has been tested for stimulating microalgae growth [11,21, suboptimal salinity.
22]. To be able to assess the applicability of DC as a culture medium for Taking into consideration that microalgae generally consume the
algal cultivation, the desalination wastewater needs to be mixed with a majority of the nutrients, notably N and P, in the growth medium,
conventional medium, since some microalgae cannot grow in DC due to Park et al. [8] reported that in wastewaters used for algae cultivation
the high mineral salts strength. For example, cultivation of freshwater the N:P ratio ranges from 4:1 to almost 40:1. Matos et al. [11] reported
Chlorella vulgaris, which cannot grow normally in DC, was performed an initial N:P ratio for marine N. gaditana cultivation of 18:1
in dilutions of 25%, 35%, 45% and 55% DC mixed with Bold Basal Medium (415.0 mg N/22.5 mg P), which is marginally higher than the theoretical
(BBM) [22]. DC concentrations below 25% had no effect on C. vulgaris N:P ratio of 16:1 (7.3 g N/1.0 g P) required for the growth of algae, based
growth compared to cultivation in control medium (BBM), both yield- on the assumption that algal biomass has the typical composition
ing a maximum biomass concentration of 0.40 g L−1. However, incubat- C106H108O45N16P [9,24]. In addition, for N. gaditana growth the N:P
ing C. vulgaris with the higher DC concentrations of 35–55% ratio in DC (18:1) was almost 3-fold higher than the N:P ratios in the
(conductivities between 2.0 and 2.8 mS cm−1) resulted in growth-salt DC-based culture medium for the freshwater species C. vulgaris (5:1)
stress, and a proportional decrease in biomass yield (to 0.27 and and S. platensis (7:1) [21,25 (Table 2)]. Given the effect of N:P ratios
0.13 g L−1). Thus, the optimal DC concentration for C. vulgaris growth on algae growth, we conclude that a culture medium based on DC is
is 25% (~1.6 mS cm−1) and at higher concentrations growth is reduced, more suitable for marine algae than freshwater algae strains.
probably due to the high Na+ and Cl− concentrations in DC. In addition,
small quantities of ammonia and sulphate have been detected in DC that 3. Effect of desalination concentrate on algal biomass composition

Table 1 3.1. Effect of desalination concentrate on protein content


Typical compositions of groundwater and desalination concentrate (DC) obtained from
the Community of Uruçu (semiarid region of Paraíba state, Brazil).
Various studies have measured the amount of protein in Chlorella sp.
Parameters Brackish groundwater DC and C. vulgaris in culture media based on 25% DC under batch, semi-
pH 7.3 ± 0.5 8.5 ± 0.3
Electrical conductivity (EC, mS cm−1) 3.0 ± 0.8 4.5 ± 1.0
Salinity (M NaCl) ~0.02 ~0.04 Table 2
TDS (mg L−1) 1823.8 ± 94 2190.5 ± 78 Optimal physicochemical parameters of culture media based on desalination concentra-
Cl (mg L−1) 720.7 ± 35 1691.3 ± 114 tion for three different algae species.
Na (mg L−1) 464.0 ± 66 987.5 ± 110
C. vulgaris S. platensis N. gaditana
CaCO3 (mg L−1) 506.5 ± 97 985.2 ± 112
Ca (mg L−1) 74.0 ± 10 126.5 ± 21 DC proportion (%) 25 50 75
Mg (mg L−1) 77.2 ± 21 80.7 ± 10 Culture medium BBM (fresh water) Paoletti (fresh water) F/2 (seawater)
SiO2 (mg L−1) 48.2 ± 11 82.4 ± 24 EC (mS cm−1) 1.0–2.2 2.0–3.2 8.0–10.0
SO2−
4 (mg L−1) 15.6 ± 0.6 138.0 ± 14 NaCl (g L−1) 0.66 3.21 10.45
K (mg L−1) 7.0 ± 2 47.0 ± 8 Salinity (M NaCl) 0.01 0.05 0.17
NO− 3 - N (mg L
−1
) 8.2 ± 0.1 30.0 ± 5 pH 8.1–9.0 9.4–10.5 8.0–9.0
−1
NH+ 4 (mg L ) 0.59 ± 0.3 1.35 ± 0.7 N:P ratio 5:1 7:1 18:1
3− −1
PO4 - P (mg L ) 0.20 ± 0.1 0.70 ± 0.3 Reference Matos et al. [22] Volkmann et al. [21] Matos et al. [11]
Fe (mg L−1) 0.05 ± 0.1 0.13 ± 0.1
DC = desalination concentrate, EC = electrical conductivity.

Please cite this article as: Â.P. Matos, et al., The use of desalination concentrate as a potential substrate for microalgae cultivation in Brazil, Algal
Res. (2016), http://dx.doi.org/10.1016/j.algal.2016.08.003
Â.P. Matos et al. / Algal Research xxx (2016) xxx–xxx 3

batch and continuous culture conditions and found that the protein con- changes in salinity that are associated with algae-cell-membrane per-
tent ranged from 45.3% to 51.0% dry matter [22,25,26]. In one study [22], meability [19].
the authors observed that intracellular protein content of C. vulgaris de- The fatty acid profile of C. vulgaris, cultivated at optimal 25% DC in
creased from 51.6% to 15.7% when the DC concentration was increased batch and continuous autotrophic cultures [22,26], showed that the
in the culture medium from 25% (1.2 mS cm− 1) to 55% DC most abundant fatty acids were (in percentage of the total fatty acids
(3.5 mS cm−1). The reduced protein content in Chlorella cultures at content) α-linolenic acid (C18:3 ɷ3, 18.0–24.6%), palmitic acid (C16:0,
high DC concentrations is most likely due to a redirection of available 17.3–20.0%) and linoleic acid (C18:2 ɷ6, 9.2–15.5%). C. vulgaris cultured
energy towards processes such as osmoregulation rather than towards in 25% DC supplemented with glucose (2.0 g L−1) under mixotrophic
the synthesis of proteins [27,28]. and heterotrophic conditions [31], contained more oleic acid (C18:1,
There is significant interest in using of DC to cultivate Spirulina 31.5–35.6%) than cultures developed under autotrophic mode [22],
platensis for agricultural purposes aimed at the production of algal bio- which is advantageous for biodiesel production [4,32]. Volkmann et al.
mass with high protein content for human food and animal feed [12]. [21] reported that the main constituents of the lipids extracted from S.
Studies carried out in photobioreactors with S. platensis cultured in op- platensis cultivation in 50% DC under photoautotrophic condition,
timal 50% DC, showed a protein content of 49.6% which is comparable to were palmitic acid (C16:0, 36.1%), oleic acid (C18:1, 20%) and γ-
the protein content (56.1%) obtained in cultures of S. platensis devel- linolenic acid (C18:3 ɷ3, ~14.0%). When marine N. gaditana was culti-
oped in conventional Zarrouk medium [29]. Another advantage of the vated in optimum 75% DC medium under two-stage photoautotro-
optimal DC concentration in culture media for S. platensis is that all es- phic-mixotrophic mode utilizing either glucose (1.0 g L−1) or glycerol
sential amino acids required for human health were found in higher (1.0 mL L−1), C16:0 was the most abundant fatty acid found, ranging
concentrations than required by the Food and Agriculture Organization, from 50.5% to 56.8% of the total fatty acids [11]. In general, the studies
except lysine and tryptophan [29]. on the use of optimal DC as an alternative culture medium find that
With regard to the protein content in marine N. gaditana, recent freshwater and marine microalgae are virtually devoid of long-chain
studies showed that when N. gaditana is cultured in conventional fatty acids (e.g. C20 and C22) and show a trend towards the increased for-
media, the protein content is 41.6% and the lipid content is 4.9%, but mation of medium-chain (C16 and C18) fatty acid methyl esters, which is
when grown in optimal 75% DC medium, the protein and lipid contents an ideal lipid source for biodiesel production [4,32].
were 27.0% and 12.6%, respectively [11]. Thus, the protein content de-
creased 1.5-fold, while the lipid content increased 2.5-fold compared 3.3. Reuse of desalination concentrate in microalgal cultivation
to cultivation in a conventional medium. The shift from protein produc-
tion to accumulation of lipids is a typical response of algae to stress con- Water recycling in microalgae cultivation is desirable not only to re-
ditions, such as nutrient depletion or salt-osmotic stress (e.g. [27,30]). duce the water demand, but also to improve the economic feasibility of
algal biofuels that will save nutrients and energy [33–35]. An analysis of
3.2. Effect of desalination concentrate on lipid content and fatty acids the reuse of the medium with the optimum DC concentration (75% DC)
composition in successive N. gaditana cultivation cycles [11] found that the medium
could support three successive cultivation cycles of N. gaditana (each
A number of recent laboratory-based studies have examined the ef- cycle involved 7 days of cultivation, 21 days in total). It was also ob-
fects of DC on the lipid content of microalgae, grown either in small served that biomass productivity of N. gaditana is directly correlated
batches and semi-continuous cultures or in continuous with lipid productivity, but does not necessarily correlate with lipid
photobioreactors [11,21,22]. Reasonable lipid accumulation was report- content. For example, biomass (151 mg L− 1 day− 1) and lipid
ed in DC-grown microalgae, ranging from low (b 10% dry matter) to (14.3 mg L−1 day−1) productivities were higher in the first cultivation
moderate (15–20% dry matter) lipid content, which in some cases trans- cycle (7 days of cultivation). The second cultivation cycle presented
lated to a relatively high lipid productivity when coupled to high bio- lipid content (13.6%) higher than the first cultivation cycle (9.5%)
mass productivity [11]. Lipid productivities of C. vulgaris, S. platensis, while the highest lipid content (14.4%) was reached in the third cultiva-
and N. gaditana cultured in optimal DC concentration are shown in tion cycle. In the first cultivation cycle, N. gaditana cells consumed 60%
Table 3. A recent study [11] found that the lipid content in N. gaditana of the total N (initial concentration 415 mg L−1) and 71.1% of the total
cells increased from 5.9% to 12.6% dry matter when the DC concentra- P (initial concentration 22.5 mg L−1) available in the culture medium.
tion increases from 25% to 75% DC in the culture medium. More impor- After three cultivation cycles N. gaditana cells had consumed 80% and
tantly, at higher DC concentrations N. gaditana tends to synthesize more 86%, of total N and total P, respectively. Because of N and P were totally
saturated fatty acids (SFAs, C14:0 and C16:0) accompanied with a lower depleted over the course of the cultivation cycles, the lipid content
production of polyunsaturated fatty acids (PUFAs, C18:2, C18:3 and tends to increase with consecutive reuses of the recycled 75% DC medi-
C20:5 ɷ3). For example, increasing the DC concentration from 0% (con- um. A similar pattern was reported by Matos et al. [25] in studies on the
trol test) to 100% DC in the culture medium for N. gaditana, the percent- algal biomass productivity and lipid content of Chlorella sp. in the
age of palmitic acid (C16:0) increased from 29.4% to 53.4%, and the recycled medium with an optimal DC concentration of 25%. These find-
percentage of eicosapentaenoic acid (EPA, C20:5 ɷ3) dropped from ings are in good agreement with reports by Griffiths and Harrison [1],
12.2% to 0.2% of the total fatty acids. Functionally, increased intracellular who also found that high lipid content in microalgae does not necessar-
lipid content and higher SFAs in N. gaditana can be explained by an ily represent high lipid productivity. Lipid content alone is therefore not
adaptive osmoregulatory mechanism to cope with rapid or gradual a good indicator of the suitability of microalgae for biodiesel production.
In order to exploit water recycling to maximize algal biomass, lipid con-
tent and lipid productivity, we need to better understand the relation-
Table 3 ship between these three parameters.
Biomass concentration and lipid productivity of microalgae grown in different proportion
of desalination concentrate (DC).
4. Concluding remarks and future directions
Biomass Lipid prod.
Species DC (%) Lipid (%) Reference
(g L−1) (mg L−1 day−1) In our recent study on extracting lipids from dried Chlorella sp. cul-
C. vulgaris 25 0.59 ± 0.12 12.5 ± 0.2 7.37 ± 0.7 [22] tured in optimal 25% DC [36], we applied a single pre-treatment step
S. platensis 50 1.55 ± 0.10 4.5 ± 0.3 6.97 ± 0.8 [21]a (ultrasonication) and compared the performance of dynamic hexane
N. gaditana 75 0.96 ± 0.15 12.6 ± 0.5 12.10 ± 0.5 [11] extraction (using a Soxhlet apparatus) with that of dynamic Supercriti-
a
Modified Volkmann et al. [21]. cal-CO2 (SCCO2) extraction. The efficiency of microalgal lipid extraction

Please cite this article as: Â.P. Matos, et al., The use of desalination concentrate as a potential substrate for microalgae cultivation in Brazil, Algal
Res. (2016), http://dx.doi.org/10.1016/j.algal.2016.08.003
4 Â.P. Matos et al. / Algal Research xxx (2016) xxx–xxx

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Please cite this article as: Â.P. Matos, et al., The use of desalination concentrate as a potential substrate for microalgae cultivation in Brazil, Algal
Res. (2016), http://dx.doi.org/10.1016/j.algal.2016.08.003
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