Bioresource Technology 241 (2017) 1084–1093

Contents lists available at ScienceDirect

Bioresource Technology
journal homepage: www.elsevier.com/locate/biortech

Design of marine macroalgae photobioreactor integrated into building to

support seagriculture for biorefinery and bioeconomy
Alexander Chemodanov, Arthur Robin, Alexander Golberg ⇑
Porter School of Environmental Studies, Tel Aviv University, Israel

h i g h l i g h t s g r a p h i c a l a b s t r a c t

Indoors macroalgae photobioreactor

(MPBR) was developed.

MPBR integrated in LEED building.

Macroalgae ash, energy density,
carbohydrates and protein content
was measured.

Macroalgae accumulated energy was
calculated.

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

Article history: Seagriculture, which can provide offshore grown macroalgae biomass would play a significant role in
Received 13 April 2017 bioeconomy. Nevertheless, seagriculture development has been hindered by the lack of laboratory pho-
Received in revised form 9 June 2017 tobioreactors that enable fundamental and pilot scale macroalgae research. In this work, a macroalgae
Accepted 10 June 2017
photobioreactor (MPBR) was developed and integrated into the building. The MPBR operation was
Available online 13 June 2017
demonstrated for 6 months with cultivation of Cladophora sp., Ulva compressa and Ulva rigida green
macroalgae species isolated from 3 sites at the Eastern Mediterranean coast. The growth rate, protein,
Keywords:
ash, specific energy density, rhamnose, xylose, arabinose, glucose, galactose and glucuronic acid content
Macroalgae
Photobioreactor
of the cultivated species were quantified. The maximum accumulated energy rates were
Seagriculture 0.033 Wh L1 d1 for Cladophora sp., 0.081 Wh L1 d1 for U. compressa and 0.029 Wh L1 d1 for U. rigida.
Bioeconomy This work provides a detailed design of an indoor, urban photobioreactor for cultivation, maintenance
Bioenergy and energy balance analysis of macroalgae biomass for biorefinery.
Ó 2017 Elsevier Ltd. All rights reserved.

1. Introduction 2008; Höök and Tang, 2013). However, climate change, environ-
mental pollution and food/energy security questions challenge
Growing population, longevity and desire for a better quality of the capacity of current infrastructures and supply chains to provide
life put ever-increasing pressure on energy, food and chemicals for sustainable development (Haberl et al., 2011). An alternative,
infrastructures (Sherbinin et al., 2007). Currently, this growth yet undeveloped, approach to produce biomass for food,
translates worldwide to the increased consumption of fossil fuels chemicals and fuels, is to use seas and oceans (Chen et al., 2015;
and conversion of land for agricultural uses (Hazell and Wood, Roesijadi et al., 2010; Yun et al., 2015). This approach for the
offshore biomass production was recently coined seagriculture
⇑ Corresponding author. (http://seagriculture.eu/).
E-mail address: [email protected] (A. Golberg).

http://dx.doi.org/10.1016/j.biortech.2017.06.061
0960-8524/Ó 2017 Elsevier Ltd. All rights reserved.
 A. Chemodanov et al. / Bioresource Technology 241 (2017) 1084–1093 1085

Seagriculture could play a significant role in the development of performance for cultivation and maintenance of several local to
bioeconomy, which would lead to the reduction in the use of fossil Eastern Mediterranean species of green macroalgae, which can
fuels (Zilberman, 2013). In addition, the expansion of biomass pro- be potentially used as feedstock for biorefinery. This system pro-
duction offshore would slow the rate of land use conversion for vides an example of research infrastructure, required to perform
agriculture (Lehahn et al., 2016). The basic unit of the seagriculture continuous macroalgae research and small scale biomass produc-
based bioeconomy is a marine biorefinery. Biorefinery is a system, tion for in the closed urban environments.
which includes feedstock cultivation, harvesting, and conversion
into products used in different branches of economy (Golberg 2. Materials and methods
et al., 2014). The potential of macroalgae feedstock for biorefinery
is under intensive investigation on the laboratory and pilot scale 2.1. Marine macroalgae biomass
(Bikker et al., 2016; van der Wal et al., 2013). However, macroalgae
feedstock development has been hindered in comparison with Green macroalgae species, Cladophora sp., Ulva compressa and
advances in terrestrial crops and microalgae (Wichard et al., 2015). Ulva rigida were collected, from Tel Aviv (Reading), Haifa, Mikh-
Unavailability of technologies and research tools to grow and moret, and Rosh HaNikra areas during spring 2016. These species
maintain macroalgae in the laboratory conditions slow develop- were chosen to test the developed MPBR as they are known for
ment of macroalgae feedstock research (Loureiro et al., 2015; Van the fast growth rates (Bruhn et al., 2011) and, thus, could provide
Hal et al., 2014; Wichard et al., 2015). In comparison, a major sci- rapid feedback on the MPBR. In addition, these species are consid-
entific tool that advanced multiple applications of microalgae in ered as potential feedstock for biorefinery (Bikker et al., 2016;
research and industry is a photobioreactor (PBR) (Singh and Ek et al., 1998; Polikovsky et al., 2016).
Sharma, 2012). Although intensively used in the microalgae Collected biomass was transported in the plastic bags filled
research and commercialization (Wang et al., 2012), reports on with the seawater to the laboratory and sorted manually to get
PBRs for adult macroalgae growth, propagation and research are clean monocultures. Monocultures were cultivated/maintained in
very rare (Holdt et al., 2014; Mullikin and Rorrer, 1998; Rorrer separate MPBRs. Nutrients were supplied by adding ammonium
and Mullikin, 1999). In most studies on macroalgae as a biorefinery nitrate (NH4NO3, Haifa Chemicals Ltd, IS) and phosphoric acid
feedstock, macroalgae are either harvested from natural stocks, or (H3PO4, Haifa Chemicals Ltd, IS) to maintain 6.4 g m3 of nitrogen
cultivated in the large outdoor tanks, in the sea or in the small lab and 0.97 g m3 of phosphorus in the seawater. The sole CO2 supply
tubes. was bubbled air. Fresh weight (FW) of the biomass was monitored
However, natural stocks harvesting could lead to the inconsis- weekly with analytical scale (Mettler Toledo, PB-S model,
tency in genetics and phenotypes between studies and even in Switzerland). Before weighing, all surface water was carefully
the same study. Although cultivation in outdoor tanks and in the removed with a hand powered kitchen centrifuge until the
open sea (both near shore and offshore) is effective in the concepts removed water weight was less than 1 g.
of integrated multitrophic aquaculture (Korzen et al., 2015), it pro- The daily growth rates, P, expressed in %d1, were calculated as
hibits the use of genetically modified macroalgae, required for fun- described in Eq. (1) (Schmidt et al., 2010):
damental studies and biotechnology applications. This limitation is
due to the high probabilities of genetically modified biomass runoff P ¼ 100%  ðFW f  FW i Þ=ðFW i  tÞ ð1Þ
to the fragile marine environment. In addition, these outdoor sys-
where FWf (g) is the final fresh weight of all the biomass in the reac-
tems are under continuous threat of contamination. Small lab
tor, FWi (g) is the initial fresh weigh in the same reactor, t (d) is the
flasks and tubes, which allow for maintenance of clean cultures,
number of days between the measurements.
can support the work with mutants and allow for precise con-
trolled experiments. However, these systems are usually of a very
small scale, and cannot provide optimal cultivation conditions in 2.2. Indoor macroalgae photobioreactor (MPBR) to develop
terms of natural illumination, water and gas exchange, required macroalgae feedstock for the future offshore marine biorefinery
by macroalgae physiology. Therefore, the results from these con-
trolled studies in tubes can be biased by non-optimal environmen- The major motivation for the development of indoor MPBR was
tal conditions. In a parallel vein, an emerging concept in the recent the need to create a research infrastructure develop macroalgae
years is the integration of algae PBRs into buildings (Lakenbrink, feedstock for the future offshore biorefinery. Development of such
2013; Pagliolico et al., 2017; Pruvost et al., 2016). Although these a feedstock requires macroalgae cultivation in the relevant physio-
systems, based on microalgae cultivation, have been proposed for logical conditions in the laboratory where some of the environ-
improving the energy balance of buildings by biogas production mental conditions can be controlled and the runoff of species to
(Lakenbrink, 2013) and shading (Pagliolico et al., 2017), to the best the marine environment is excluded. To achieve these aims we
of our knowledge they never been used for macroalgae and nor developed a closed loop, indoor cultivation system with 29 reac-
was the chemical composition of the cultivated algae reported. tors (40.4 L each, with continuously exchanging water) with total
To goal of this work is to address the current limitations of operation volume of 1,171.6 L of seawater and with an air bubble
macroalgae research infrastructure by providing a design of a mixing. The water was continuously recirculated and filtered.
new PBR developed for macroalgae studies in the laboratory condi- The system allowed for macroalgae biomass acclimation, cultiva-
tions and for the small scale biomass production in buildings. The tion and species maintenance under natural sun illumination, with
closed macroalgae photobioreactor system (MPBR) allows for spe- controlled nutrients and mixing intensities levels.
cies maintenance, research and propagation. The MPBR was incor-
porated into the Leadership in Energy and Environmental Design 2.3. Vertical polyethylene photobioreactor for macroalgae cultivation
(LEED) certified building, with existing solar-thermal absorption
chiller air condition (AC) system. The developed MPBR is different A basic unit of the developed system is a reactor for macroalgae
from the proposed until now microalgae PBR incorporated into cultivation. In MPBR, the cultivation reactor (Fig. 1a) was welded
buildings (Lakenbrink, 2013; Pagliolico et al., 2017; Pruvost et al., from 200 mm polyethylene sleeve (Polytiv, Israel, Length 100 m,
2016), as it uses seawater, it is integrated with a thermos-solar thickness 200 mm, width 0.4 m) with embedded anti-UV protec-
powered AC system and it is focused to grow and maintain tion. The total volume of each cultivation reactor was 40.4 L. Air
macroalgae. This work describes the system design and bubble mixing was provided from the bottom and water exchange
1086 A. Chemodanov et al. / Bioresource Technology 241 (2017) 1084–1093

Fig. 1. Schematic representation of a. A single macroalgae photobioreactor (MPBR). b. Recirculated seawater filtration system. Dashed lines show the filter bags.

from the top (Fig. 1a). The rate of aeration and water exchange was several species simultaneously, complete filtration of the all con-
controlled manually for each reactor with mechanical valves. The taminants is very expensive and not practical. Therefore, the fol-
top part of the reactor contained a filtering net (0.5–3 mm, depend- lowing system of filtration meshes was developed. At the exit
ing on the biomass size) to prevent biomass washing out to the from the cultivation reactors to the drainage tank, the water passed
main circulation system. Biomass harvesting was done from the through a series of 0.5–5 mm filters to remove large pieces of deb-
bottom, by opening the cover and filtering the biomass through ris and thalli (Fig. 1a). At the entrance to the drainage tank, the
the aquarium net (Fig. 1a). During the cultivation, continuous water was further filtered up to 800 mm (Fig. 1b). At the entrance
water exchange removed the metabolites produced by the algae to the storage tanks, on the 4th floor, water was further filtered
and associated organisms. For maintenance, every 1–3 weeks, the up to 40 mm with membranes, installed at the end of the pipe,
biomass was removed to a different reactor and the reactor was (Fig. 1b) and wadding polyester Sintepon (Pentair Aquatic
cleaned mechanically. Eco-Systems, Inc., FL). In addition, PVC ribbon with high surface
for biofilter (Bio-Fill and BF 250, Pentair Aquatic Eco-Systems,
2.4. Closed loop seawater system for continuous water exchange Inc, FL) to prevent contamination was used.

The total operation volume of the system was 6400 L of seawa- 2.5. Solar flux measurements
ter (salinity 3.9%, pH 8.2). Initial water stock was provided from the
Tel Aviv Reading marine area and was partially (1/4–1/3) The variation of solar flux (Photosynthetically active radiation,
exchanged every 3 months. Evaporation was compensated by add- PAR) between cultivation reactors was measured exactly at noon
ing deionized water to the system to maintain the salinity at 3.9%. in August-September 2016 for each cultivation reactor with
The total circulating volume was 3400 L. Additional 3000 L were Li-Cor Spherical Quantum Sensor (LI 193SA, Li-Cor, NE). The
stored separately. 2000 L were stored in two 1000 L plastic storage measurements were taken at the same point, 15 cm from the top,
tanks at the basement. The rest of the water was pumped to the for each reactor during three cloudless day. The illumination
4th floor of the building using 32 mm pipe and Dm 30 N Pedrollo profiles during 24 h outside and inside the single reactor were
1.1 kW pump (Italy). On the 4th floor 1000 L was stored in the plas- measured by OnsetÒ HOBOÒ sensor UA-002-08 (Onset Inc. MA)
tic storage tank and 3682 L of water were used in the active vol- in August-September 2016.
ume distributed as follows: 1) 2 tanks, with capacity of 1000 L
each and 1 tank with a capacity of 500 L (connected) on the 4th 2.6. Temperature measurements
floor, 2) 1,171.6 L were in the 29 cultivation reactors with the bio-
mass on the 3th floor; 3) 1500 L of PVC drainage tank, located Minimum and maximum daily temperatures were measured in
under the system of reactors on the 3th floor (Fig. 2b). The addi- the system with thermometer (Maxi-mini-thermometer, model:
tional role of the drainage tank was to serve as a safety buffer to MMG-3, Shanghai QualityWell Industrial Co., Ltd, China) during
absorb all the water from MPBR system in the case of emergency. 6 months of operation. Temperature changes during 24 h inside
The water flowed by gravitation from tanks on the 4th floor to the and outside the reactors were measured by OnsetÒ HOBOÒ sensor
MPBRs (50 mm PVC major pipe and 20 mm distribution pipes UA-002-08 (Onset Inc, MA) in August-September 2016.
(Fig. 2b)), and from them to the drainage tank (25 mm PVC pipe).
Once the water in the drainage tank approached a predetermined 2.7. Air bubble mixing
level, a pump (PQAm70 0.55 kW, Pedrollo, Italy) recirculated the
water back to the 4th floor storage tanks. The gravitation driven Air bubble column was used for thalli mixing inside the cultiva-
flow was a key element to save electricity and prolong the pump tion reactors. The air system consisted of an air blower (SC201MF
life. 0.4KW Emmecom Srl.,Italy) located at the 4th floor (Fig. 2b) and
A critical part of the system was water filtration (Fig. 1b). Filtra- distribution pipes. The central pipe 50 mm branched to smaller
tion was needed to prevent plankton and epiphytes growth and to 16 mm, feeding the reactors (Fig. 1a) at 2–4 L min1. The air flow
prevent cross contamination when several species were grown at rate in each reactor was manually regulated with the incorporated
the same time. As fresh sea water was used for cultivation of in series flow meters (DFA-15, Darhor Technology Co.,Limited,
 A. Chemodanov et al. / Bioresource Technology 241 (2017) 1084–1093 1087

Fig. 2. Closed macroalgae photobioreactor (MPBR) integrated into the LEED building of PSES at Tel Aviv University a. System location inside the eco-wall of the PSES building.
b. Detailed plan of the MPBR integrated within solar tubes of the building. Red arrow shows the position of sleeve reactors in the gap between solar tube arrays. Blue lines
show water flow; green lines show air flow. c. Digital photography view of the MPBR system. Red arrow indicates the cultivation area, where maximum solar light is available
to the reactors. Yellow star indicates the species maintenance reactors where intensive growth is not expected because of the limited by solar tubes illumination.(For
interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

China). The flow rates was adjusted for complete circulation of all ICS-5000 platform (Dionex, Thermo Fischer Scientific, MA, USA)
thalli in the cultivation reactor. The usual flow rates were with an analytical column (Aminopack 10) and its corresponding
2–4 L min1. guard column. Electrochemical detector with AgCl as reference
electrode was used for detection. The analysis was performed
2.8. Protein analysis using an isocratic flow of 4.8 mM KOH generated by the automatic
Eluent Generator (Dionex, Thermo Fischer Scientific, MA, USA) dur-
Harvested with an aquarium net biomass was dried at 40 °C for ing 20 min. The column was washed with 100 mM KOH between
12 h. Five gram of each sample were analyzed according to AOAC each run and re-equilibrated with 4.8 mM KOH prior to injection.
981.10 with an automatic Kjeldahl system for total protein quan- The column temperature was kept at 30 °C, and the flow rate
tification. Protein calculation factor of 6.25 was used. Analysis was set to 0.25 mL min1. Calibration curves were produced for
was done by a certified food chemistry company (AminoLab, Reho- each monosaccharide with internal standards.
vot Israel). Glucuronic acid content was quantified with a program that
involved three handmade eluents: NaOH, ultrapure water and
2.9. Carbohydrate and sugar acid analysis sodium acetate. Two additional small peaks were observed but
not analyzed in the area of glucuronic acid peak in all samples.
The biomass was dried in an oven at 40 °C until constant These were hypothetically identified as aldobiouronic acid and
weight. The dried biomass was made brittle by liquid nitrogen iduronic acid as stated in (Quemener et al., 1997). Total yield
and then it was grinded into powder manually by mortar & pestle. was calculate using the following Eq. (2):
All chemicals and standards were purchased from Sigma-Aldrich P
10 6i¼1 mi
(Israel) if not otherwise mentioned. Thermochemical deconstruc- %Yield ¼ ð2Þ
1000  %Solid
tion (2% sulfuric acid, 1:20 solid to solvent ratio, 30 min, 121 °C)
was conducted in 10 mL centrifuge tubes (NalgeneTM Oak Ridge where mi (mg) is the mass of carbohydrate i in the sample, %Solid is
High-Speed PPCO Centrifuge Tubes (Thermo-Fisher Scientific, the solid load of the dried at 105 °C for 24 h biomass for the hydrol-
CA)) in autoclave (Tuttnauer 2540MLV, Netherlands). For each ysis from the total weight. The summed carbohydrates were rham-
batch, dried samples of biomass (50 mg) were weighed on analyt- nose, xylose, arabinose, glucose, galactose and glucuronic acid. The
ical balance (Mettler Toledo, Switzerland) Sulfuric acid was added concentrations of the rest of the released monosaccharides were
into the tube and the mix was vortexed to make the powder well negligible. Each biomass sample was hydrolyzed in duplicate for
distributed in acid. The hydrolysates were stored at 20 °C after the analysis. All hydrolysates were analyzed in duplicates for carbo-
centrifugation (5 min, 12,000 rpm using a benchtop centrifuge hydrates content.
(Epindorf, Germany).
For carbohydrate analysis, the hydrolysates were thawed, an 2.10. Ash content quantification
aliquot was taken and diluted 50 times in ultrapure water before
being filtered through a 0.22 mm syringe-filter (Millipore, USA) into About 0.5 g (±0.01) of harvested biomass were weighted and
High Pressure Ion Chromatography (HPIC) vials (Dionex, Thermo then dried at 105 °C using conventional oven for 24 h in pre-
Fischer Scientific, MA, USA). Monosaccharide contents in the weighted clean ceramic crucibles. The crucibles were then cooled
hydrolyzates were monitored by HPAEC-PAD using a Dionex down in desiccator, weighted, and ignited at 550 °C for 3 h in a
1088 A. Chemodanov et al. / Bioresource Technology 241 (2017) 1084–1093

muffle furnace (Thermolyne muffle furnace, Thermo scientific) and The MPBR system was divided into two sub-system: cultivation
then kept at 105 °C. The crucibles were finally cooled down in des- MPBRs and maintenance MPBRs. To further increase the use of
iccator and weighted. The dry weight content (DW) was calculated solar energy within the building, we decided to locate the system
with Eq. (3): cultivation MPBRs between the gaps between the tubes
m3  m2 (Fig. 2b and c red star area). However, it is important to note, that
DW ¼ ð3Þ the cultivation MPBRs were not exposed to the maximum solar
m1  m2
irradiation, which is attenuated by the solar-thermal tubes. There-
where m1 (g) is the weight of the biomass samples (dried at 40 °C) fore, we did not expect to maximize the biomass yields in this sys-
and the weight of the crucible combined, m2 (g) is the weight of the tem in comparison to open sun systems, where reactors are
ceramic crucible and m3 is the weight of the biomass samples and exposed to the open light. The maintenance MPBRs were located
the weight of the crucible after drying at 105 °C. The ash content behind the solar tubes (Fig. 2c, yellow star area), their goal was
(Ash) was calculated with Eq. (4): to maintain the clean monoculture species stocks alive without
intensive growth for all experiments.
m4  m2
Ash% ¼  100% ð4Þ
m3  m2
3.2. Environmental parameters of the system: light intensity and
where m4 (g) is the weight of the biomass samples and the weight temperature
of the crucible the after combustion at 550 °C for 3 h.
As the system was located indoors but in the open air (inside
2.11. Specific energy quantification the eco-wall), we did not control the light and temperature during
the cultivation time. Depending on specific reactor location, PAR
Twenty gram (DW) of biomass were analyzed for energy con- varied between reactors in 238–348 mmole photons m2 s1
tent (specific energy e [MJ kg1] according to ASTM D5865 – 13 (52.12–76.21 W m2, Fig. 3a). The open sun measurement (outside
(Standard Test Method for Gross Calorific Value of Coal and Coke) the solar tubes) at the same location and time showed PAR in
by a certified laboratory of Israel Electric company. 2,035–2065 mmole photons m2 s1 (445.66–452.23 W m2)
range. This order of magnitude intensity lost was caused by shad-
ing from the integrated in building thermal-solar tubes. The illumi-
2.12. Energy balance analysis
nation profile during 24 h outside and inside a single reactor are
shown on Fig. 3b. The measurements inside the reactor were taken
Solar irradiation for the cultivation period was extracted from
in a reactor filled only with water and in a reactor with 1.5 grww L1
the Israel Meteorological Services (http://www.ims.gov.il/IMS/CLI-
of U. rigida biomass. Biomass at this density led to reduction of the
MATE/LongTermRadiation/) for Beit Dagan Israel measurement
illumination inside the reactors two times (Fig. 3b).
station. The daily global solar irradiance (kWh m2) was calculated
The minimum and maximum temperature distribution in the
as the irradiance from 5am to 7pm on each day of the cultivation
system is shown in Fig. 3c. Day/night temperature differences of
experiment. The IMS data base provides information of the accu-
0.5–13 °C in April-first 2 weeks of June and 1–3.5 °C in second half
mulated global irradiance with 1 h resolution. The total solar
of June-August were observed. The 24 h distribution of tempera-
(Esolar) input to the MPBR was calculated for the total illuminated
ture inside and outside the single cultivation reactor is shown on
area of the eco-wall (4.48 m2).
Fig. 3d.
The maximum PAR to chemical energy conversion efficiency of
macroalgal biomass in the MPBR was calculated using Eq. (5)
3.3. Green macroalgae biorefinery with indoor MPBR
DðFW f  FW i Þmax  FW=DW  e  N
%gmax ¼  100% ð5Þ
Esolar  Dt For system validation, we cultivated three green macroalgae
species, isolated from different locations in the costs of Israel.
where DðFW f  FW i Þmax (gww) is the maximum biomass accumula- The macroalgae were cultivated in the system during spring and
tion for each species per reactor; FW/DW is wet: dry weight ratio, summer 2016 at least at 3 repeats per experiment (three cultiva-
measured by biomass drying at 105 °C for 24 h; e (MJ kg1) is the tion reactors per species) (Fig. 4). On Fig. 4, the minimum (Pmin),
specific energy determined as described in Section 2.10; N is the the maximum (Pmax) and the average (Pav) growth rates for each
number of the cultivation reactors (14), and Dt (d) is the number species is reported as measured during the whole cultivation per-
of days with Pmax, calculated in Eq. (1). iod. On Table 1, the chemical composition and growth rate at the
day of chemical composition measurement (Ph) for a representa-
3. Results and discussion tive sample is reported.
Cladophora sp., isolated from Rosh HaNikra sampling site was
3.1. Design of MPBR incorporated into the LEED building cultivated for 122 days from 5 May to 26 July 26, 2016. The growth
rates changed from Pmin 3.66% day1 to Pmax 9.78% day1, with a
The MPBR system was constructed within the south/east corner Pav of 3.47% day1. The Pmax was measured for 12 continuous days
of the eco-wall of the LEED Platinum certified building of the Porter from 5 May to 17 May 2016. Cladophora sp. isolated from
School of Environmental Studies (PSES) at Tel Aviv University Mikhmoret sampling site was cultivated for 122 days from 5 May
(Fig. 2a). Eco-wall incorporates a series of solar-thermal tubes that to 26 July 26, 2016. The growth rates changed from Pmin 9.32%
provide thermal energy for the building AC system. However, the day1 to Pmax 95.5% day1, with a Pav 36.63% day1. The Pmax was
tubes do not cover completely the south wall (Fig. 2b, red star for 12 continuous days from 5 May to 17 May 2016. Cladophora
area); therefore there is still available solar flux that comes to sp. isolated from Reading sampling site was cultivated for 38 days
the building and is not used for heating the solar tubes. This loca- from May 30 to July 7. The growth rate was stable at
tion of MPBR behind the solar tubes increased the total energy har- P 95.47% day1 during the entire period of 38 cultivation days from
vesting of the eco-wall structure. Recent theoretical work analyzed May 30 to July 7, 2016 (Fig. 4a). This is in comparison to P 8–15%
a microalgae PBR incorporated into the building façade for biomass day1 reported for Cladophora sp. in (de Paula Silva et al., 2013)
production, energy consumption reduction and thermal regulation at optimum pH with enhanced CO2 or to P of 0.68–0.74 d1 for
of the building (Pruvost et al., 2016). Cladophora sp. at optimum N:P ratio (Liu and Vyverman, 2015).
 A. Chemodanov et al. / Bioresource Technology 241 (2017) 1084–1093 1089

Fig. 3. a. Light distribution between cultivation reactors at noon during August–September 2016 in Israel. Three measurements were done at 12 pm in August–September
2016. b. Illumination profile during 24 h outside the reactor (black line), inside the reactor with sea water (blue line) and inside the reactor with 1.5 gr L1 of Ulva biomass
(green line) in August-September 2016 are shown. c. Temperature distribution in the system during March-August 2016. d. 24 h distribution of temperature inside and
outside the cultivation reactors. Data from 7 consequent measurements in August-September 2016 are shown.(For interpretation of the references to colour in this figure
legend, the reader is referred to the web version of this article.)

Fig. 4. MPBR system validation for the cultivation of a. Cladophora sp. b. Ulva compressa; c. Ulva rigida. Thalli morphology is shown on the left panel. Biomass growth rates are
shown on in the right.

Carbohydrate profiling was done for Cladophora sp. harvested at was 4.37 ± 0.85 mg mg1 1
DW, arabinose 34.27 ± 3.47 mg mgDW, galac-
1 1
Mikhmoret site and cultivated in the system (Table 1, Fig. 5). The tose 29.91 ± 3.16 mg mgDW, glucose 69.44 ± 6.71 mg mgDW, xylose
growth rate at the day of harvest (Ph) was 63.9%. Rhamnose content 20.02 ± 2.66 mg mg1 1
DW and glucuronic acid 1.10 ± 0.09 mg mgDW.
1090 A. Chemodanov et al. / Bioresource Technology 241 (2017) 1084–1093

Table 1
Macroalgae species grown in the MPBR system approximate composition and energy density content based on DW at 105 °C.

Species (Origin, Ph% (day1) at Rh* Arb* Gal* Gluc* Xyl* Gluc* Ash Protein Specific
date of collection harvest from mg mg1
DW mg mg1
DW mg mg1
DW mg mg1
DW mg mg1
DW acid mg mg1
DW mg mg1
DW energyMJ kg1
in origin) system mg mg1
DW

Cladophora sp. 63.9% 4.37 ± 0.85 34.27 ± 3.47 29.91 ± 3.16 69.44 ± 6.71 20.02 ± 2.66 1.10 ± 0.09 267 ± 10 120 15.042
(Mikhmoret, (30.5.2016)
16.05.2016)
Ulva compressa 3.5% 55.57 ± 4.72 0.33 ± 0.17 10.34 ± 1.52 85.94 ± 5.93 27.26 ± 2.69 20.73 ± 1.87 276 ± 10 290 14.310
(Rosh HaNikra, (14.6.2016)
1.03.2016)
Ulva rigida (Haifa, 1.4% 42.11 ± 1.62 0.52 ± 0.18 4.07 ± 0.54 61.93 ± 2.59 10.29 ± 0.35 18.77 ± 4.98 473 ± 20 330 9.879
1.03.2016) (20.6.2016)
*
Rh (rhamnose), Arb (arabinose), Gal (galactose), Gluc (glucose), Xyl (xylose), Gluc acid (glucuronic acid).

Fig. 5. a. Approximate cultivated macroalgae composition. b. Cultivated in MPBR macroalgae Cladophora sp., Ulva compressa and Ulva rigida major carbohydrates profile. Error
bar show ± Standard deviation (n = 4).

The total carbohydrate yield was 15.91 ± 0.86%. To the best of our from April 14 till 23 August 2016. The growth rates were mostly
knowledge, this is a first report for acid hydrolysis of whole marine negative, with the biomass loss at Pmin 82.34% day1, Pmax of only
Cladophora sp with quantitative information on the individual 0.83% day1 was observed 38 continuous days from 14 April to 24
monosaccharides release. Previous studies reported on water sol- May 2016 (Fig. 4b). Previous studies reported on 10 to 35% day1
uble cladophoran reported on 4:3:1 M ration of arabinose: galac- at various environmental conditions (Martins et al., 1999; Potter
tose: xylose (O’Donnell and Percival, 1959). Glucose source is et al., 2016).
most probably cellulose, which is a major target for Cladophora Carbohydrate and protein profiling was done for U. compressa
derived products (Ek et al., 1998; Mihranyan, 2011, 2008, 2007). harvested at Rosh HaNikra site and cultivated in the system
The protein content in the biomass was 12% (DW105°C), in compar- (Table 1, Fig. 5). The Ph was 3.5%. Rhamnose content was
ison to 15–21% reported in (Trung et al., 2013). The ash content 55.57 ± 4.72 mg mg1 1
DW, arabinose 0.33 ± 0.17 mg mgDW, galactose
was 26.76 ± 0.01%. 10.34 ± 1.52 mg mgDW, glucose 85.94 ± 5.93 mg mg1
1
DW, xylose
U. compressa isolated from Rosh HaNikra sampling site was cul- 27.26 ± 2.69 mg mg1
DW and glucuronic acid 20.73 ± 1.87 mg mgDW.
1

tivated for 175 days from 1 March to 23 August 2016. The growth The total carbohydrate yield was 20.17 ± 8.40%. These results are
rates changed from Pmin 2.47% day1 to Pmax 16.79% day1, with a lower than the results reported in (Feng et al., 2011), where the
Pav 2.89% day1. The Pmax was observed for 18 continuous days optimization of U. compressa (previously classified as
from 18 May to 5 June 2016. U. compressa isolated from Mikhmoret Enteromorpha) was reported. In that study biomass was collected
sampling site was cultivated for 172 days from 1 March to 20 from the shore and extracted monosaccharides content was
August 2016. The growth rates changed from Pmin 1.46% day1 to 175.2, 55.3, 183.4, and 88.5 mg g1 for glucose, xylose, rhamnose
Pmax 5.51% day1, with a Pav 3.65% day1. The Pmax was observed and glucuronic acid at the best hydrolysis conditions for each of
for 27 continuous days from 3 May to 30 May 2016. U. compressa the monosaccharides (Feng et al., 2011). The parameter that could
isolated from Reading sampling site was cultivated for 143 days explain the difference between these results is the nitrogen
 A. Chemodanov et al. / Bioresource Technology 241 (2017) 1084–1093 1091

concentration. In our system, the nitrogen content was higher than during the sun light there is active photosynthesis. At night the
in natural sea water and previous studies showed that macroalgae 30 s mixing pulse was provided every 30 min to avoid anoxic con-
accumulate high carbohydrates at nitrogen starvation in Ulva sp ditions building up.
(Gómez Pinchetti et al., 1998). The total protein content of this bio- The energy balance of the proposed biorefinery system is shown
mass was 29% (DW105°C) in comparison with 17.48% reported in in Fig. 6. The majority of the incoming solar energy is attenuated by
(Kandasamy et al., 2012) or 9.42–20.60 (depending on the location the solar-thermal system existing in the building. This absorbed
and harvesting season) (Haroon et al., 2000), 9–14% (Aguilera- energy is then used for powering air condition of the building
Morales et al., 2005) and 21% reported in (Mamatha et al., 2007). through the absorption chiller. The rest of the direct solar energy
The ash content was 27.69 ± 0.01%. (10% of the total flux) arrives to the MPBR (3.5–5.2 kWh d1,
U. rigida isolated from Rosh HaNikra sampling site was culti- PAR). Additional direct energy inputs for the biomass growth in
vated for 89 days from June 7 to September 4. The growth rates our system came from 1) the air blower (0.4 kW, operating for
changed from Pmin 3.13% day1 to Pmax 19.51% day1, with a Pav 12 h a day during photosynthesis) 4.8 kWh per day; 2) recirculat-
4.61% day1. The Pmax was for 16 continuous days from 20 June ing water pump (0.55 kW, when fully operational the pump
to 6 July 2016 (Fig. 4c). U. rigida isolated from Haifa sampling site worked for 30 min and 30 min rests, when partially operational
was cultivated for 175 days from March 1 to August 23. The growth the pump worked for 15 min and 45 min rests) 3.3–6.6 kWh day1;
rates changed from Pmin 0.88% day1 to Pmax 8.39% day1, with a 3) pump for bringing the new water arrived from the sea to the 4th
Pav 2.01% day1. The Pmax was for 64 continuous days from 31 floor of the building (1.5 kW ton1), 0.05 kWh day1 during the 6
May to 3 August 2016 (Fig. 4c). Previous studies reported on 17% operation months. Thus, the total direct energy consumption of
day1 of U. rigida grown on effluents from fish cages (Korzen the system was 11.65–12.65 kWh during the 24 h of operation.
et al., 2015) and 18.7% day1 in tanks (Bruhn et al., 2011) and Additional, indirect source of energy for the system was the energy
11.8% in spray cultures (Msuya and Neori, 2010). embedded in the nutrients (ammonium nitrate and phosphoric
Carbohydrate and protein profiling was done for U. rigida har- acid). Quantification of nutrients absorbed by the biomass in this
vested at Haifa site and cultivated in the system (Table 1, Fig. 5). system is currently under research and because of the high dynam-
The Ph was 1.4%. Rhamnose content was 42.11 ± 1.62 mg mg1 DW, ara- ics of their concentrations is not in the scope of this work.
binose 0.52 ± 0.18 mg mg1 1
DW, galactose 4.07 ± 0.54 mg mgDW, glu- The measured specific energy content for Cladophora sp was
cose 61.93 ± 2.59 mg mg1 DW, xylose 10.29 ± 0.35 mg mg1 DW and 15.042 MJ kg1, for U. compressa it was 14.310 MJ kg1 and for U.
glucuronic acid 18.77 ± 4.98 mg mg1 DW. The total carbohydrate yield rigida it was 9.879 MJ kg1. The maximum accumulated energy
was 13.70 ± 5.88%. The protein content from the biomass harvested was calculated for the Pmax of each species for all 14 cultivation
was 33% (DW105°C), to comparison to 12–25% (measured by the MPBR and was 0.018 kWh day1 (0.033 Wh L1 d1) for Cladophora
same method) as reported in (Shuuluka et al., 2012) for a 5 month sp (starting cultivation density 0.05 grww L1), 0.045 kWh day1
study in natural and nutrient enriched cultivation. An analytical (0.081 Wh L1 d1) for U. compressa (starting cultivation density
study for U. rigida deconstruction reported 18.3% protein, 2.5 grww L1) and 0.016 kWh day1 (0.029 Wh L1 d1) for U. rigida
0.7 mg mg1 1 1
DW arabinose, 0.1 mg mgDW fucose, 11.7 mg mgDW galac- (starting cultivation density 0.36 grww L1). This translates to
tose, 1.4 mg mg1 DW galacturonic acid, 183 mg mg 1
DW glucose, energy conversion efficiency from PAR to chemical energy of
62.3 mg mg1 1
DW glucoronic acid, 1.4 mg mgDW fructose, 0.9 mg mgDW
1
0.35–0.53% for Cladophora sp, 0.87–1.3% for U. compressa and
mannitol, 18 mg mg1 DW mannuronic and guluronic acids, 0.31–0.47% for U. rigida. The effect of the initial cultivation density
91.2 mg mg1 1
DW rhamnose, and mg mgDW 38.5 xylose (Pezoa-Conte on the biomass energy accumulation on Ulva was investigated in
et al., 2015). The ash content was 47.36 ± 0.02%.
It is important to emphasize, that the total protein content was
measured using Kjeldahl method in which the total protein content
was calculated from the measured organic nitrogen content using a
factor of 6.25, required by the standard for the food industry. Pre-
vious studies, however showed that this factor can be different for
macroalgae (Angell et al., 2016; Lourenço et al., 2002) and a speci-
fic corrections will be needed in the future for each species.
The growth rates measured in this study had wide ranges,
mostly due to the biomass sporulation. This problem can be
addressed by synchronizing the age of the population and by
decreasing the stress conditions, such as temperatures fluctua-
tions. The biomass yields were also limited by the maximum illu-
mination, which was limited by the solar systems. Additional
problems could appear because of the rapid water evaporation
during the summer. Although the salinity was controlled by adding
the deionized water, fluctuations at the local level at each cultiva-
tion reactor during the day could take place. In addition, automa-
tion of nutrients measurements and addition will significantly
improve the overall efficiency of the system.

3.4. System integration and energy balance

For maintenance and cultivation of various macroalgae species,

the mechanical parts of the system were synchronized with natu- Fig. 6. Energy balance on the MPBR system inside the solar-thermal system of the
ral solar irradiance and biomass growth rates as follows. Water PSES building. Solar energy was taken from global illumination data for August-
September 2016 from the Israel Meteorological Service Database (http://www.
exchange in all reactors was continuous and was set for two vol- ims.gov.il/). Solar energy input was calculated for the total area of 14 cultivation
umes (81 L) exchange in 1–2 h. Air mixing was set to operate con- MPBR (4.48 m2). Biomass energy accumulation was calculated assuming maximum
tinuously during the day time with automatic control because only growth rates of species in all 14 reactors with 0.15: dry: 1 wet weight ratio.
1092 A. Chemodanov et al. / Bioresource Technology 241 (2017) 1084–1093

(Bruhn et al., 2011) and showed to have an optimum at 4 g L3, and Chen, H., Zhou, D., Luo, G., Zhang, S., Chen, J., 2015. Macroalgae for biofuels
production: progress and perspectives. Renewable Sustainable Energy Rev. 47,
is the subject of the future work for other species.
427–437.
To summarize, MPBR operation has been demonstrated for de Paula Silva, P.H., Paul, N.A., de Nys, R., Mata, L., de Nys, R., Kiyohara, M., 2013.
6 months on maintenance and cultivation of three green macroal- Enhanced production of green tide algal biomass through additional carbon
gae species Cladophora sp., U. compressa and U. rigida isolated from supply. PLoS One 8, e81164.
Ek, R., Gustafsson, C., Nutt, A., Iversen, T., Nyström.,, C., 1998. Cellulose powder from
3 sampling points in the costal areas of Israel. Although the Pmax for Cladophora sp. algae. J. Mol. Recognit. 11, 263–265.
Cladophora sp., was 95.5% day1, for U. compressa was 16.79% day1 Feng, D., Liu, H., Li, F., Jiang, P., Qin, S., 2011. Optimization of dilute acid hydrolysis of
and for U. rigida was 19.51% day1, very high fluctuations Enteromorpha. Chin. J. Oceanol. Limnol. 29, 1243–1248.
Golberg, A., Vitkin, E., Linshiz, G., Khan, S.A., Hillson, N.J., Yakhini, Z., Yarmush, M.L.,
in the growth rate led to Pav of 3.47–95.47% day1 for 2014. Proposed design of distributed macroalgal biorefineries:
Cladophora sp., -40.76–8.03% day1 for U. compressa and thermodynamics, bioconversion technology, and sustainability implications
2.01–4.61% day1 for U. rigida, depending on the origin site. These for developing economies. Biofuels Bioprod. Biorefin. 8, 67–82.
Gómez Pinchetti, J.L., del Campo Fernández, E., Moreno Díez, P., Reina, G.G., 1998.
large fluctuations cannot be explained by variations in illumina- Nitrogen availability influences the biochemical composition and
tion, mixing and nutrients supply and future studies are needed photosynthesis of tank-cultivated Ulva rigida (Chlorophyta). J. Appl. Phycol.
to understand the impact of the biological parameters, such as 10, 383–389.
Haberl, H., Erb, K.-H., Krausmann, F., Bondeau, A., Lauk, C., Müller, C., Plutzar, C.,
strains background, ploidy, age and sporulation on the growth rate Steinberger, J.K., 2011. Global bioenergy potentials from agricultural land in
fluctuations. Although the protein content for investigated biomass 2050: Sensitivity to climate change, diets and yields. Biomass Bioenergy 35,
was high in comparison with other plants, 12% for Cladophora sp., 4753–4769.
Haroon, A.M., Szaniawska, A., Normant, M., 2000. The biochemical composition of
29% for U. compressa, and 33% for U. rigida, further studies are
Enteromorpha spp. from the Gulf of Gdańsk coast on the southern Baltic Sea⁄.
needed for protein content factor determination. Further work is Oceanologia 42, 19–28.
needed for profiling of the residual, unhydrolysed polymers in Hazell, P., Wood, S., 2008. Drivers of change in global agriculture. Philos. Trans. R.
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Holdt, S.L., Christensen, L., Iversen, J.J.L., 2014. A novel closed system bubble column
photobioreactor for detailed characterisation of micro- and macroalgal growth.
4. Conclusions J. Appl. Phycol. 26, 825–835.
Höök, M., Tang, X., 2013. Depletion of fossil fuels and anthropogenic climate change
– a review. Energy Policy 52, 797–809.
In this work, we reported on the indoor, laboratory scale system Kandasamy, G., Karuppiah, S.K., Subba Rao, P.V., 2012. Salt- and pH-induced
that enables maintenance and cultivation of macroalgae in the functional changes in protein concentrate of edible green seaweed
Enteromorpha species. Fish Sci. 78, 169–176.
building environment. MPBR operation has been demonstrated Korzen, L., Abelson, A., Israel, A., 2015. Growth, protein and carbohydrate contents
for 6 months on maintenance and cultivation of three green in Ulva rigida and Gracilaria bursa-pastoris integrated with an offshore fish
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imum measured growth rates for Cladophora sp., was 95.5% day1, International Building Exhibition. Hamburg. pp. 1–22.
for U. compressa was 16.79% day1 and for U. rigida was 19.51% Lehahn, Y., Ingle, K.N., Golberg, A., 2016. Global potential of offshore and shallow
waters macroalgal biorefineries to provide for food, chemicals and energy:
day1. The system provides a convenient platform technology that
feasibility and sustainability. Algal Res. 17, 150–160.
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urban laboratory environment. filamentous algae Cladophora sp., Klebsormidium sp. and Pseudanabaena sp.
under varying N/P conditions. Bioresour. Technol. 179, 234–242.
Loureiro, R., Gachon, C.M.M., Rebours, C., 2015. Seaweed cultivation: potential and
Acknowledgement challenges of crop domestication at an unprecedented pace. New Phytol. 206,
489–492.
Lourenço, S.O., Barbarino, E., De-Paula, J.C., Pereira, L.O.D.S., Lanfer Marquez, U.M.,
The authors acknowledge TAU Institute for Innovation in Trans-
2002. Amino acid composition, protein content and calculation of
portation, Israel Ministry of Energy and Water resources, Israel nitrogen-to-protein conversion factors for 19 tropical seaweeds. Phycol. Res.
Ministry of Economy, and Israel Ministry of Science for the support 50, 233–241.
of this project. The authors thank the team of Israel Electric Com- Mamatha, B.S., Namitha, K.K., Senthil, A., Smitha, J., Ravishankar, G.A., 2007. Studies
on use of Enteromorpha in snack food. Food Chem. 101, 1707–1713.
pany at Orot Rabin power station (Ella Kotler and Sara Moscowich), Martins, I., Oliveira, J.M., Flindt, M.R., Marques, J.C., 1999. The effect of salinity on
Dr. Dror Itzhak and Dr. Gabriel Jinjikhashvily from the Engineering the growth rate of the macroalgae Enteromorpha intestinalis (Chlorophyta) in
Division for the help we caloric value measurements. the Mondego estuary (west Portugal). Acta Oecologica 20, 259–265.
Mihranyan, A., 2011. Cellulose from cladophorales green algae: from environmental
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Appendix A. Supplementary data Mihranyan, A., Edsman, K., Strømme, M., 2007. Rheological properties of cellulose
hydrogels prepared from Cladophora cellulose powder. Food Hydrocolloids 21,
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Supplementary data associated with this article can be found, in Mihranyan, A., Nyholm, L., Garcia Bennett, A.E., Strømme, M., 2008. A novel high
the online version, at http://dx.doi.org/10.1016/j.biortech.2017.06. specific surface area conducting paper material composed of polypyrrole and
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