Bioresource Technology 349 (2022) 126858

Contents lists available at ScienceDirect

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

Review

Design and applications of photobioreactors- a review

Ranjna Sirohi a, b, 1, Ashutosh Kumar Pandey b, c, 1, Panneerselvam Ranganathan d, 1,
Shikhangi Singh e, Aswathy Udayan f, Mukesh Kumar Awasthi g, Anh Tuan Hoang h,
Chaitanya Reddy Chilakamarry i, Sang Hyoun Kim c, Sang Jun Sim a, *
a
Department of Chemical & Biological Engineering, Korea University, Seoul 136713, Republic of Korea
b
Centre for Energy and Environmental Sustainability, Lucknow 226 029, India
c
Department of Civil and Environmental Engineering, Yonsei University, Seoul, Republic of Korea
d
Department of Chemical Engineering, National Institute of Technology, Calicut, India
e
Department of Postharvest Processing and Food Engineering, GB Pant University of Agriculture and Technology, Pantnagar, India
f
Department of Chemical Engineering, Hanyang University, Seoul, Republic of Korea
g
College of Natural Resources and Environment, Northwest A&F University, Yangling, Shaanxi Province 712100,PR China
h
Institute of Engineering, HUTECH University, Ho Chi Minh City, Vietnam
i
Faculty of Chemical and Process Engineering Technology, Universiti Malaysia Pahang, 26300 Gambang, Malaysia

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 :

• Different types of PBRs for microalgae

and biohydrogen production reviewed.
• Closed PBRs offer effective control on
culture conditions and reduce pollution.
• Flat plate PBRs hold high biomass yield
comparison to other type of PBRs.

A R T I C L E I N F O A B S T R A C T

Keywords: There has been increasing attention in recent years on the use of photobioreactors for various biotechnological
Microalgae applications, especially for the cultivation of microalgae. Photobioreactors-based production of photosynthetic
Biohydrogen microorganisms furnish several advantages as minimising toxicity and providing improved conditions. However,
Design
the designing and scaling-up of photobioreactors (PBRs) remain a challenge. Due to huge capital investment and
Photobioreactors
operating cost, there is a deficiency of suitable PBRs for development of photosynthetic microorganisms on large-
scale. It is, therefore, highly desirable to understand the current state-of-the-art PBRs, their advantages and
limitations so as to classify different PBRs as per their most suited applications. This review provides a holistic
overview of the discreet features of diverse PBR designs and their purpose in microalgae growth and biohydrogen

* Corresponding author.
E-mail address: simsj@korea.ac.kr (S.J. Sim).
1
Contributed equally and share co-first authorship.

https://doi.org/10.1016/j.biortech.2022.126858
Received 10 January 2022; Received in revised form 10 February 2022; Accepted 12 February 2022
Available online 17 February 2022
0960-8524/© 2022 Elsevier Ltd. All rights reserved.
R. Sirohi et al.
production and also summarizes the recent development in use of hybrid PBRs to increase their working effi­
ciency and overall economics of their operation for the production of value-added products.
1. Introduction
The growing use of fossil fuels, their unfavourable consequences for
the environment, and the resulting “Food vs Fuels” war of words sparked
by primary biofuels has prompted scientists to work on renewable fuel
supplies that are both environmentally friendly, reliable and cost
competitive. Therefore, biofuel systems of second and third generation
were developed (for example, lignocellulosic and microalgal biofuel
frameworks) which have the possibility to address all of these challenges
and provide a new source of renewable energy. As an effect, third gen­
eration bio-fuels produced from microalgae are known to be a hypo­
thetically practical renewable energy option that is free of the main
pitfalls related with first and second generation biofuels, based on
existing information and technology predictions (Zhu et al., 2019).
Photosynthetic microorganisms, such as microalgae, produce high
quantity of lipids, carbohydrates, protein and that in shorter duration
and have unique growing conditions (Deprá et al., 2019). The use of
biohydrogen decreases greenhouse gas emissions because the conver­
sion of hydrogen to energy, whether by combustion or fuel cells, pro­
duces only pure water. Biohydrogen would be the ideal outcome of the
microbial process if suitable technology were used (Saratale et al.,
2019). These materials can be used to produce biofuels and other
valuable byproduct.
As a result, recent developments in photobioreactor engineering
have increased bioprocess engineering’s emphasis on decreasing pro­
duction costs and recognising algae’s ability. A photobioreactor is a
sealed, illuminated culture vessel that is used to generate managed
biomass. A photobioreactor is a closed structure that is locked off from
the outside environment and has no possible exchange of gases or pol­
lutants with it. Photobioreactors (PBRs) have the advantage of mini­
mising toxicity and providing improved environment for example, pH,
temperature, light, and CO2 concentration. They also allow for higher
cell concentrations and complex biopharmaceutical processing (Singh
and Sharma, 2012). Generally, PBRs have been considered as most
suitable systems for the cultivation of microalgae. Initially, the mass
cultivation of photoautotrophs has been studied in open raceways
because of their low cost but these systems have many drawbacks such
as control of temperature and water level, high chances of contamina­
tion etc. To remove these drawbacks closed systems came in existence,
these systems have many advantages, including reduced risk of
contamination and microalgae can be grow at optimum conditions
without environmental influences (Masojídek and Torzillo, 2014). Now,
PBRs are considered as the representative for the new type of algae
culture device and become an important key to solve the efficient pro­
duction of photoautotrophs and ensure the quality of the value added
products derived from them. The main characteristics of several PBR
designs, their utilization in microalgae growth and biohydrogen pro­
duction were examined in this study. This review also summarizes the
recent development of computational model development for
photobioreactors.
2. Advances in design of photobioreactors and applications in
microalgae cultivation and biohydrogen production
A series of decisions, ranging from light source to bioreactor struc­
ture, go into the collection and design of PBRs for microalgae processing.
The subsequent considerations should be made when developing the
PBR: reactor should be able to cultivate a wide range of microalgal or­
ganisms; reactor configuration must allow for even lightening of the
culture surface as well as rapid CO2 and O2 mass transfer. Microalgae
cells are extremely sticky, resulting in accelerated fouling of reactor
2
Bioresource Technology 349 (2022) 126858
light transmission surfaces (Yen et al., 2019). This requires repeated
reactor shutdowns for mechanical washing and sterilisation. The reactor
configuration should in such way that it will minimize fouling of the
reactor, especially the light-transmitting surfaces. PBRs should have as
minimal non-illuminated space as possible and must function in the
presence of excessive foaming, which is common in reactors having high
mass transfer rates (Zhou et al., 2020).
Despite their high cost, PBRs have many significant advantages over
open systems such as reduced pollution and enable monocultures of
axenic algae to be grown. They allow for more precise monitoring of
variables such as pH, temperature, light, and CO2 concentration. Also,
water does not evaporate in PBRs. Higher cell concentrations are also
possible in PBRs. For the development of algae and biohydrogen, a va­
riety of PBRs have been prepared and fabricated (Udayan et al, 2022;
Sirohi et al 2022). Artificial radiation, solar light, or both may be used to
illuminate algal culture structures. Natural sources of algal culture
structures with substantial illumination surface areas include open
ponds, flat-plate, horizontal/serpentine tubular airlift, and inclined
tubular PBRs (Dange et al. 2022). To artificially illuminate laboratory-
scale PBRs, fluorescent lamps or other light sources are typically
employed (either internally or externally). Example of these PBRs
include bubble columns, airlift columns, stirred tanks, helical tube,
conical, torus, and seaweed-type PBRs (Chang et al., 2017). Low capital
expenditures, a higher surface area -volume ratio, an absence of moving
components, appropriate heat and mass transfer, and effective release of
O2 and residual gas mixture are just a few of the advantages of the
bubble column bioreactor. Under oversaturating light conditions, the
flat panel bioreactor’s modification resulted higher productiveness, with
a volumetric mass productivity 1.7-fold higher than the bubble column
bioreactor’s. In outdoor culture, the horizontal tubular bioreactor’s form
is beneficial because of its orientation toward light, resulting in higher
light conversion efficiency. In addition, the photosynthetic performance
and production volume of the flat panel bioreactor were higher. Helical
type PBRs have an advantage over other bioreactors in terms of low land
requirements and improved CO2 transition from gas to liquid phases.
However, fouling within the reactor and the energy needed by the
centrifugal pump in recirculating culture, as well as associated shear
stress, limit their commercial usage (Huang et al., 2017).
A regulated experimental helical-tubular PBR was designed for
continuous development of Nanochloropsis sp. Its key benefits include a
high ratio of volume (culture) to surface area, combined with efficient
light penetration depth, efficient temperature and contaminant moni­
toring, excellent visual flow of fresh air and CO2, better CO2 transfer
through a broad surface interface between fresh air and the culture-
liquid medium, as well as an unique automated flow-through sensor
that monitors cell concentrations in real time (Briassoulis et al., 2010).
The BioCO2 project (2008–2011), a research collaboration between
Norway’s Norwegian Institute for Agricultural and Environmental
Research, Sweden’s Uppsala University, and India’s IIT Kharagpur,
planned, built, and tested a flat screen, rocking photobioreactor for
algae cultivation (non-rocking mode) and hydrogen processing (rocking
mode).
Regardless of the way that microalgae research has expanded as of
late, with the quantity of papers on microalgae multiplying and the
quantity of distributions on PBRs trebling, more laboratory research on
the selection and efficiency of PBRs for diverse uses on a lab scale is still
required (Bosma et al., 2014; Skjånes et al., 2016). The production of
hydrogen is one goal that presents some challenges. Many PBR struc­
tures have been used to grow microalgae, and many more have been
studied for use in hydrogen production research. Because agitation of
the culture is an essential parameter in PBRs for hydrogen production,
R. Sirohi et al. Bioresource Technology 349 (2022) 126858

agitation methods have received special attention. Sulfur deprivation as are made up of translucent tubes with a diameter of 0.1 m.The specific
a tool for producing hydrogen from green microalgae has recently been design of tubular reactor is divided into two major sections: (1) photo­
reviewed, with up-scaling attempts. Phototrophic species light conver­ stage loop and, (2) mixing (retention) tank. The prior is the reactor’s
sion and hydrogen synthesis efficiencies, as well as the relationship main portion (where photosynthesis and biomass development take
between the two has also been reviewed (Dasgupta et al., 2010). place), while the mixing tank is mostly used to extract oxygen and
The unique design approaches and process optimization strategies regulate culture variables. The tube diameter is the first variable to be
for PBRs will be discussed in this part. Table 1 shows design parameters calculated in the photostage. In order to avoid inhibiting dissolved ox­
and hardware design considered for design of different PBRs. Tubular, ygen concentrations evolved as a function of photosynthesis (RO2), and
flat plate, column, and soft-frame PBRs, as well as certain modified liquid velocity (v) the overall length of the loop (L) is determined after
hybrid systems, are the most common. Different types of PBRs are shown the tube diameter is chosen. The liquid velocity varies from 0.1 to 0.8
in Fig. 1. The efficiency of microalgae development and biohydrogen ms− 1 to reduce power consumption and prevent cell injury, with total
production, which were carried out by these novel designs and optimi­ tube lengths ranging from 20 to 400 m (Acién et al., 2017). To circulate
zation, was likewise analyzed. the liquid along the tubing, mechanical or airlift devices may be used.
The needed power is primarily required to overcome head loss due to
friction in the tubes. In tubular PBRs, power requirements vary from 10
2.1. Tubular type PBRs to 100 W m2 (Ugwu et al., 2008). The retention tank’s primary purpose
is to meet the system’s mass transfer requirements, particularly in terms
Tubular photo bioreactors are perhaps the most appropriate form for of desorption of dissolved oxygen. The culture must circulate again into
outdoor mass cultures among the PBRs suggested. The majority of out­ the mixing tank to release the oxygen collected in the photostage.
door tubular PBRs are made of glass or plastic tubes, and their cultures The tubular PBR, on the other hand, has one of the most significant
are re-circulated using a pump or, preferably, an airlift device. So far, disadvantages: slow mass conversion. It’s important to note that when
PBR designs were reported that are horizontal/serpentine, vertical, near tubular PBRs scale up, mass transfer (oxygen build-up) becomes a
horizontal, conical, and inclined (Vasumathi et al., 2012). The culture is problem. As the diameter of tubes in a tubular PBR is increased, the
pumped either by pumps or through air streams in these devices which illumination surface to volume ratio decreases (Torzillo and Zittelli,
are normally made of glass or plastic tubing (airlift). 2015). Although a tubular PBR is scaled up by the width of the tubing,
whereas, the length of the tube should be held as short as possible. If
2.1.1. Configuration and operation mixing device is strong, the cells in the lower part of the tube will not
Tubular PBRs have surface-volume ratio (S/V) of up to 80 m− 1, attain an adequate amount of light for cell growth (due to light shading
allowing them to deal with high concentration of biomass cultures, and effect). In addition, most tubular PBRs make it difficult to regulate
culture temperatures, whereas they can be built-in with a thermostat to
Table 1 maintain the optimal culture temperature, this can be costly and time-
Design parameters considered for design of different PBRs. consuming to incorporate.
Photobioreactor Hardwares Design Enhancement
types design parameters methods 2.1.2. Microalgae growth in tubular PBRs
Tubular reactor • sparger • mixing- • incorporating
The basic feature of a properly built tubular PBR is to have a regu­
design- residence time static mixers lated atmosphere in which the microalgal strain used can achieve op­
orifice, ring, distribution (half-moon- timum growth and product development. Species of algae, area, tube
foam types (RTD), shaped blades) diameter, biomass fixation, distance among tubes, and the quantity of
• method of circulation time • static kenics
tubes per stack in upward stacked frameworks, all these affect the
mixing ; mixer
design • gas hold up • helical mixer microalgae efficiency in tubular photobioreactors (Fernández et al.,
• pumping • kLa, bubble • swirl flow 1999). A relatively small tube diameter, generally 0.1 m or less, is
diameter, –tangential inlet, required for an optimal light regime and therefore high biomass output.
interfacial area twisted
Unless there is hydrodynamic tension due to circulation, the greater the
• light and dark
cycles- intensity
diameter of a photo-limited structure, the higher the volumetric pro­
and frequency ductivity. Another benefit of increasing the diameter is that the culture’s
Flat-plate • sparger • mixing- RTD, • incorporation of biomass concentration increases. This is crucial for culture harvesting,
photobioreactor design circulation deflector especially when working with small organisms. Comparisons between
• baffles design time, shear • vertical,
various tube diameters are difficult, as they are influenced by many
rate; horizontal,
• gas hold up inclined and considerations, including the mixing rate (Reynolds number), the O2
• kLa, bubble wave types and CO2 concentrations, the number of passages of the culture through
diameter, baffles the circulation system, and the temperature profile, which can shade the
interfacial area • swirl flow- jet effect of a stronger light to dark cycle attainable under a shorter light
• L/D cycle inlet
efficiency- • double paddle
path.
Light intensity wheel The length of the tubes, on the other hand, has the most impact on
• illuminated the culture’s residence time and mixing time within the reactor (Torzillo
surface to and Zittelli, 2015). The O2 emitted by photosynthesis repeatedly exceed
volume ratio
that produced by air saturation in PBRs with too long tubes, which can
Air-lift reactor • sparger • mixing- RTD, • incorporation of
design- shear effect; serial lantern- hinder photosynthesis. Arthrospira cultures and other microalgae are
orifice, ring, • gas hold up shaped draft tube harmed by oxygen concentrations greater than 35 mg L-1 (Torzillo et al.,
foam types • kLa, bubble • cyclinder draft 1986; Carvalho et al., 2006). Several experiment explain that on
• ratio of riser diameter, tube increasing the tube length while maintaining a constant diameter,
to downcome interfacial area • Tesla Valve
diameter • L/D cycle baffles
changes the pH of the culture at the tube exit, as well as the oxygen
efficiency- • H and X-shapes content in the culture and CO2 losses. The length of the tubular PBR is
Light intensity • vertical multi directly proportional to the rise in mixing time, a consideration that
column airlift must be considered during scale-up to ensure adequate homogenous
reactor
distribution of nutrient within the community (Torzillo and Zittelli,

3
R. Sirohi et al. Bioresource Technology 349 (2022) 126858

Fig. 1. Different type of PBRs (A) Helical tubular type PBR, (B) Flat pannel PBR, (C) Column type PBR, (D) Flat PBR, (E) Tubular helical PBR.

2015). bends or connected by manifolds; horizontal or inclined tubes. Hori­

2.1.3. Biohydrogen production in tubular PBRs
Long transparent tubes having diameters 3–6 cm and lengths from 10
− 100 m were utilized in tubular PBRs. Either mechanical or air-lift
pumps are used in pumping the culture liquid through these tubes.
The tubes can be positioned in a variety of ways: horizontally as straight
tubes with a small or large number of U-bends; vertically, coiled as a
cylinder or cone; vertically, positioned in a fence-like structure using U-
zontal tubes can be fixed at certain distances in between the tubes with
varied relative surface. Despite the fact that tubular reactor designs vary
widely, the deviation in photon flux density impinge on the reactor
surface is the most important influence of the various designs on the
light regime. In most designs, the light gradient in the tubes has a similar
form. For outdoor photo-fermentative hydrogen production by purple
non sulphur bacteria, a glass stacked tubular bioreactor with uniform
velocity and light distribution, low pressure drops, low gas permeability,

Table 2
Microalgal strains and their H2 production efficiency by photosynthesis.
Configuration of Algae species Cultivation Light source and Hydrogen productivity References
Photobioreactor irradiance (µmol
m-2s¡1)

Helical tubular and flat panel(5 C. reinhardtii(CC124) Batch photo cool white 1.3 ± 0.05 mL H2 L-1h− 1 with flat (Oncel and
L) mixotrophic fluorescent light panel 1.05 ± 0.05 mL H2 L-1h− 1 with Kose, 2014)
(~75 µE m− 2 s− 1 × tubular
2)
Erlenmeyer flask Aphanothecehalophytica Batch 30 µmol photons Up to 13.8 mmol mg Chla-1h− 1 with (Taikhao et al.,
photomixotrophic m− 2 s− 1 cool white N-free medium containing 0.4 mM 2013)
light Fe3+
Glass tubes (20 mL) Chlorella protothecoides Batch 30–35µmol m− 2 s− 1 Up to ~ 140 mL L-1 (with (Zhang et al.,
photoheterotrophic simultaneous nitrogen and sulphur 2014)
limitation)
2 − 1
Glass air lift reactors (1 L), with S. obliquus semi-continuous 150 μE m− s 113:1 mL g− 1 VS C. butyricum (Batista et al.,
bubbling air 2014)
2 − 1
Cylindrical, conical ended Chlorella vulgaris (NIER-10003) Batchphoto ~120 µmol m− s Maximum volume of 1315 mL L-1 (Rashid et al.,
photobioreactor (1 L) mixotrophic- with pH = 8, sucrose = 5 mg L-1 2013)
immobilized Maximum rate of 24 mL L-1h− 1 was
with fructose
Plastic bags photobioreactors cyanobacterium Anabaena sp. Batch reactor 290 and 340 µmol 33.2 mL L-1 with productivity rate (Shastik et al.,
PCC 7120 photons m− 2 s− 1 20.6 mL day− 1 L-1 2020)
Electrochemical sequential Spirulina Batch reactor optimum intensity 27.49 and 13.37 mol of H2 d-1 m− 3& (Hasnaoui
batch reactor, two cylindrical 2.92 W m2 0.3 V voltage and ~ 2.5 mA current et al., 2020)
chambers Pyrex glass production rate 2.65 m3 m− 3 d-1pH
9.5
2
Flat-platephoto-bioreactor Cyanothecesp. ATCC51142 Batch reactor 45 W m− – (Zhang et al.,
2015)
Glass tubes photobioreactor Desertifilum sp. IPPAS B-1220 Batch reactor 45 µmol photons 0.229 μmol mg-1Chl h− 1
(Kossalbayev
m− 2 s− 1 et al., 2020)
1
One side glass tube (cultivation Synechocystis sp. PCC 6803 Batch reactor 60 µmol photons 5.73 ± 0.69 mL H2 mg cells− (Touloupakis
columns) (400 mL) m− 2 s− 1 et al., 2016)

4
R. Sirohi et al.
and efficient gas–liquid separation has been built (Kayahan et al., 2016).
Four stacked U-tubes (tube diameter 3 cm) and two vertical manifolds
make up the design. The glass stacked tubular reactor design has a lower
capacity and a long life. Under outdoor conditions, this design was built
and run with Rhodobacter capsulatusYO3 hup with molasses as the car­
bon source.
The situations in most designs are also similar when it comes to
liquid mixing. Because of the deposition of gas, the length of the tubes is
restricted; however this may not be as critical for nitrogenase-based
activities, which are less hindered by hydrogen. Boran et al., (2012)
studied a pilot solar tube PBR for photofermentative hydrogen genera­
tion using a mutant of R. capsulatus (Hup) in fed batch operation under
outdoor conditions. In this, a novel feeding approach was adopted by
varying the feed acetate content to keep the acetic acid concentration in
the PBR between 20 and 30 mM. The highest molar productivity was
0.40 mol H2/(m3 h), with a production of 0.35 mol H2 per mole of acetic
acid supplied. By volume, evolved gas included 95–99% hydrogen and
the remainder were carbon dioxide. Generally, tubular bioreactors
should show higher efficiency because they use short dark or average
light cycles.
Table 2 shows some examples of PBRs used for biohydrogen
production.
2.2. Flat panel PBRs
Flat panel PBRs are well-known through their high surface-to-
volume ratio, vertical or slanted slope of the channels from horizontal,
and lack of automatic mechanisms for cell suspension. The cuboidal
design of the flat panel reactor allows for a short light path. Transparent
materials such as glass, plexiglass, and polycarbonate can be used to
create it (Agbebi 2019). Besides, the culture development, gas
exchanged, and degassing is finished by bubbling air from the lower part
of each channel. Air is bubbled from one side through a perforated tube,
or it is manually rotated by a motor to produce agitation.
2.2.1. Configuration and operation
PBRs with flat panels have a basic design that considerably reduces
the depth of light penetration through the culture surface. It consists of a
frame with a transparent plate on both sides. Yang et al. (2011) designed
a flat panel PBRs, made from standard 16 mm thick plexi-glass alveolar
plates, which have a high surface-to-volume ratio. Due to the enormous
lighting surface area, it has been observed that flat-plate PBRs can reach
significant photosynthetic efficiencies. In comparison to horizontal
tubular PBRs, the deposition of dissolved O2 concentrations in flat-plate
PBRs is comparatively minimal. However, as compared to tubular PBRs,
these systems often have lower areal yields. In terms of configuration
changes, Jung et al., (2014) proposed ultra-compact PBRs to address
uneven light distribution by stacking slab waveguide layers with light
scatterers. The development proficiency of 10-layer level plate PBRs was
improved by eight times, and biomass effectiveness was also expanded.
The performance of level plate PBRs was likewise affected by the sur­
rounding atmosphere. In flat plate PBRs, there are matrices of opera­
tional conditions (e.g., light pathway, panel inclination, panel spacing,
microorganism type, temperature), and the optimization process is used
to maximise biomass output while reducing energy consumption. Sleg­
ers et al. (2011) demonstrated that the presence of shadow between
panels has a detrimental influence on light penetration. A spacing of 0.2
to 0.4 m between panels was optimum. In addition, north–south panel
orientations yielded 50% more biomass than east–west panel orienta­
tions, especially in high-latitude locations. Sierra et al., (2008) investi­
gated the relationship between dissolved gas, heat transfer, mass
transfer, and mixing and aeration rates in flat plate PBRs under various
operating circumstances. DO apparatus had a power output of 53 W/m3,
similar to bubble column PBRs but less than the tubular unit, which had
a power output of 2000–3000 W/m3. In airlift loop PBRs, the effect of
superficial gas velocity, gas holdup liquid circulation speed, mixing time
5
Bioresource Technology 349 (2022) 126858
and mass transfer efficiency was shown to save 16.3 % energy (Guo
et al., 2015). Furthermore, (de Mooij et al., 2016) advised that light
absorption be minimised because over-illumination was not required for
biological energy generation. As a result, varied light spectrum in the
range of different light colours should be used. White (warm) and yellow
light, for example, were seen to have the utmost production, appeared to
be double that of blue light. For the analysis of productivity certain
relevant software was also used. Massart et al. (2014) used a computa­
tional fluid dynamics (CFD) model to predict optimal flow rate and
optimise biomass output in flat panel airlift PBRs. PBRs were generated
using Gambit® software, and then the flow regime was simulated using
Fluent® software. 1.5 L/min and 312 sec of mixing time was the opti­
mal air flow rate.
2.2.2. Microalgae growth in flat panel PBRs
Flat panel bioreactors may also be useful in terms of capture angle,
and depending on the agitation mechanism employed, a high mixing
rate and low shear stress may be achieved. In different study, Sun et al.
(2016) designed hollow polymethyl methacrylate tubes in flat plate
PBRs. The aluminum-coated polyethylene terephthalate was used to
cover the inside of tubes, with the goal of increasing light transmission
to the reactor’s dead zone. This increased illumination in the interior
zone by 2–6.5 times and increased biomass production by 23.42%.
Tredici and Zittelli(1998) developed a near horizontal flat screen with
five channels separated lengthwise and two plexiglass funnels at the top
and bottom. The surface area to volume ratio was 40 m− 1, and the gas
hold up capacity was 10.3%. Through the bottom tubular plexiglass
manifolds, a mixture of carbon dioxide gas was pumped axially. Flat
panel reactors were further modified by adding more technical charac­
teristics for example, V shape reactor produces a high shear rate,
removing escape corners to lessen shear stress and cell adherence to the
reactor walls, and introducing baffles to increase agitation (Zhang et al.,
2001; Iqbal et al., 1993).
Koller et al. (2017) used a variety of microalgae and found that
Scenedesmus ovalternus growth at 30 ◦ C, pH 8.0, and a light flux of 1300
mol photons/m2s in flat plate gas-lift PBRs. The maximal biomass and
growth rates, respectively, were 7.5 0.1 g L-1 and 0.11 h− 1. As previously
mentioned, illumination pattern had an influence on biomass yield;
yellow light produced the maximum biomass output (54 g m− 2 d-1),
whereas blue and red light produced almost half (29 g m− 2 d-1) (de
Mooij et al., 2016).
2.2.3. Biohydrogen production in flat panel PBRs
In terms of hydrogen production, the drawbacks are associated to
agitation techniques. When it comes to algae cultivation, the most
popular agitation method is sparging. Magnetic stirring, impeller stir­
ring, baffles, and rocking motion are some of the other ways. Agitation
via sparging includes hydrogen gas dilution and its recirculation, both of
which might increase the danger of leakage.
Agitation, whether by magnetic stirring or impeller stirring, needs a
large amount of energy. The flat panel reactor was appropriate in terms
of hydrogen production, owing to its ability to prevent the backpressure
of stored hydrogen. Research focused on horizontal flat panel photo­
bioreactors with magnetic stirring identified the impact of hydrogen
headspace concentration on hydrogen generation efficiency (Kosourov
et al., 2012). In addition, Hydrogen has been produced using flat plate
bioreactors agitated by sparging with recirculated gas. (Tamburic et al.,
2011; Davis et al. 1953; Soeder et al. 1981) addressed the idea of
employing a flat panel design in a horizontal position with a rocking
motion for agitation, and this option may be converted to a hydrogen
production unit (Gilbert et al., 2011).When the reactor is utilised for
hydrogen production, however, adding gas is an inefficient agitation
technique since the generated gas is diluted, which is a significant
drawback. The increased possibility of leakage makes gas circulation
problematic. Gas exchange is likewise vital during the hydrogen pro­
duction stage, which requires mixing at a reasonable speed and angle. As
R. Sirohi et al.
a result, preventing all hydrogen leakage as much as feasible is an
important requirement for a successful design and use of a PBR for
hydrogen production. This implies that any substance in interface either
with hydrogen gas or a media producing hydrogen should have char­
acteristics that prevent hydrogen gas from penetrating too deeply.
Furthermore, all connections should have seals that have been proven to
be hydrogen leakage free, both in terms of material qualities and seal
location. The design ought to take into account simple extractions from
culture, collected gas, and the culture compartment’s headspace without
compromising hydrogen porousness.
2.3. Column types PBRs
Section or vertical cylindrical photobioreactors are option of stirred
reactor in which the most part of agitation is finished via air sparging.
They are likewise delegated airlift reactors, and bubble column, on the
basis of liquid flow. The culture is aerated with air or CO2 for mixing to
initiate the suspending process. The advantages of such a system include
excellent gas–liquid mass transfer and biomass production, low shear
stress, high mixing rates, low energy utilization, and light/dark cycle
control characteristics. Bubble column reactors are widely used in in­
dustry for the manufacture of baker’s yeast, beer, vinegar, and waste­
water treatment.
2.3.1. Configuration and operation
Column PBRs are not difficult to set up since they are built by
interfacing modules as well as coordinating with different process, for
example the membrane separation process. Column reactors are cylin­
drical vessels that are higher than its diameter. There are no additional
internal structures other than the sparger. Different designs of photo­
bioreactors were designed to improve the mass transfer coefficient of
hydrodynamic fluid and gas, including the X-shape, H-shape, and serial
column and among them; only the X-shape exhibits superior conditions
in terms of mass transfer coefficient of gas liquid and mixing time (Pham
et al., 2017). In column PBRs, the lighting patterns and position are
likewise thought of desirable alternates. Light was preferred when it was
provided from the interior zone, not just because of the known effects of
lighting intensity. Since liquid at inner dark zone flows to the external
photic zone at a more noteworthy gas stream rate, photosynthetic pro­
ficiency is profoundly affected by gas stream rate, light and dark cycle.
Therefore, on increasing the gas flow rate, the photosynthetic efficiency
increases leading to shorter light and dark cycle. Hu and Sato (2017)
improved interior illumination by arranging blue and red LED lights in
the right places. The distance between LED sources was measured and
the biomass yield estimated, according to the experimental data and
modelling results the distance between LED sources ranged from 30 to
50 mm, with illumination irradiances of 250, 420, and 1000 mol m− 2
s− 1.
In bubble column, the behaviour of bubbles emitted from the sparger
determines the column hydrodynamics and mass transfer characteristics
completely. At the point when bubbles are distributed over the cross-
segment of column and there is almost no back agitation of the gas,
then homogeneous flow happens at low gas flow rates. For bubbles
breakup and their dispersed coalescences in a tall bubble column during
scale up, perforated plates were used widely. In airlift column reactors,
there are two interconnecting zone. The one of the tube in reactor is
known as riser (gas mixture sparged) and other one is called a down­
comer (gas mixture not sparged). Without any physical agitation, the gas
is mixed by bubbling it via a sparger in the riser tube. Riser is similar to
bubble column where sparged gas moves upward randomly and
haphazardly (Koller, 2015). It has been designed into variety of forms
including the incorporation of a sparger into annular tube. Rectangular
airlift photobioreactors are also recommended because they have
excellent mixing properties and a high photosynthetic efficiency, but
their complexity and difficulties in scaling up are disadvantages (Naidoo
et al., 2021). Also, operating conditions such as temperature
6
Bioresource Technology 349 (2022) 126858
and mixing are important in column PBRs. Temperatures between 18
and 25 ◦ C had no effect on specific growth rate, while temperatures over
25 ◦ C affected the growth rate (Serra-Maia et al., 2016). This approach
might be useful for the production of chlorophyll pigments.
2.3.2. Microalgae growth in column type PBRs
Lipid is desirable result of the growing process in microalgae. As a
result, a number of related studies have been conducted in order to
maximise lipid production. The Taguchi technique was used to enhance
the growth conditions in bubble column photobioreactors so that the
marine microalgae Chlorella minutissima could produce more biomass
and fatty acids (Pereira et al., 2018). The highest production of palmitic
and stearic acid was found in the findings. For microalgae culture and
CO2 capture, a modified gas feeding bubble column PBRs was used
(Barahoei et al., 2020). Li et al., (2018) studied the microalgal growth
and CO2 fixation rate in a column photobioreactor with an internal light
column in which the mass transfer coefficient was 24.3 %. The tem­
perature, pH, light intensity, aeration rate, light–dark cycle, and time
optimal values were 25 ◦ C, 8.0, 2700 lx, 0.5 LPM, and 168 h, respec­
tively. By changing the light/dark ratio, the addition of an internal light-
column increased the light intensity of microalgal development. The
colour of light has a different influence on microalgae development. In
C. vulgaris and Gloeothece membranacea, red colour illumination
increased the biomass yield, but green colour favoured the chlorophyll
content in C. vulgaris and G. membranacea and was not as much of
dependent on light source and culture density (Mohsenpour and Wil­
loughby, 2013). Ozkan and Rorrer (2017) investigated the effect of
intake CO2 on phototrophic biomass, lipid, and chitin yields in Cyclotella
sp. As a result, until 3000 ppm, lipid production increased proportion­
ately with partial CO2 pressure input. In terms of nutritional re­
quirements also, photosynthetic activity was found lower in the N-
starving condition than in the N-redundant condition.
2.3.3. Biohydrogen productionin column type PBRs
Column type PBRs designs are challenging for hydrogen production
since mixing of the culture is dependent relative on either gas addition
or gas circulation, both of which result in dilution of the generated
hydrogen and a higher chance of leakage. In agitation system, bubbling
of an inert gas dilutes the stream of hydrogen, resulting problematic for
vertical tube reactors in production of hydrogen (Dasgupta et al., 2010).
Airlift photobioreactors (APBRs) possess a lower and more uniform
shear stress than related devices such as stirred tanks and bubble col­
umns, resulting in their widespread use in biological activities.
Furthermore, the aeration rate, or surface gas velocity, has a substantial
impact on cyanobacteria development. Anabaena sp. produced bio­
hydrogen in an airlift photobioreactor at various superficial gas veloc­
ities to determine the effect of bioreactor hydrodynamics on H2
generation (Zarei et al., 2021). At a surface gas velocity of 0.185 cm s− 1,
photosynthesis produced no hydrogen, demonstrating the possibility of
H2 production. The largest amount of hydrogen (371 mL h− 1 PBR-1) was
measured at 0.524 cm s− 1. Overall, 82.8 % of the initial substrate supply
was used in cylindrical bottles, which had the lowest substrate conver­
sion efficiency (SCE). The trend in substrate conversion to biomass was
the polar opposite of the trend in substrate conversion to hydrogen. As a
result, the culture system with the lowest SCE was the most efficient in
producing biomass (Palamae et al., 2018). Besides, another measure for
evaluating hydrogen generation efficiency is light conversion efficiency
(LCE). LCE is the ratio of the total amount of hydrogen generated free
energy content to the energy content of the light received by the culture
throughout the hydrogen production time (Palamae et al., 2018).
2.4. Soft frame PBRs
Soft-frame PBRs, unlike typical PBRs that use hard materials and are
immobile, may be split into small modules and are therefore more
transportable. However, because it must withstand a significant
R. Sirohi et al.
pressure, the material employed in its construction should be prone to
damage. Soft frames are composed of ethylene vinyl acetate, poly­
ethylene, and polytetrafluoroethylene, all of which are flexible and
require less space for installation. Moreover, there are many dead zones,
resulting in lower biomass yield, and the agitation cost, due to its design,
is prohibitive for industrial use. As a result, the PBRs are smaller, have a
larger working volume, and can be rotated in direction of light sources.
Soft-frame PBRs, on the other hand, are currently the subject of minimal
research. PBRs with a soft frame have ability to integrate with tradi­
tional PBRs.
2.4.1. Configuration and operation
A number of materials are used in the soft-frame construction of
PBRs. However, there are no scaling-up guidelines in place for this
brand-new technology at the moment. At the pilot and industrial sizes,
the current state of soft-frame PBR research is inconclusive. The method
was first developed using a vertical flat panel PBR through a poly­
ethylene bag placed between two iron frames (Rodolfi et al., 2009).
Hamano et al. (2017) cultured algae on cellulosic/PTFE membrane
sheets, which they then attached to PBRs’ soft frames. There was no
need to mix the PBRs once the nourishment was supplied via capillary
mechanism, therefore energy consumption was decreased. Unfortu­
nately, the increasing cost of PTFE precludes this method from becoming
economically feasible. To decrease the production cost, a low-cost
plastic bag (PVC) was used in an algae culture system to drive the
movement of a rocking platform for accomplish mixing in a horizontal
PBR (Zhu et al., 2017). Without CO2 gas bubbling, the PBR promoted the
development of alkali halophilic microalgae Euhalothece sp. ZM001.
PBRs made of plastic bags can even be constructed to create cells in the
water; effective use of ocean waves improves mixing and mass transfer
while also lowering costs. A new construction material such as hollow
glass microspheres (HGM) were used basically to control the irradiance
the microalgae broth temperature. This can be done by in combination
of polymers to change thermal insulation and mechanical properties
(Pereira et al., 2014). HGM caused a 37% rise in growth rate and a 9◦
reduction in broth temperature. The composites examined had similar
mechanical resistance to the polymer matrix. The effect of PBR
composition [clear polyurethane (PolyU) vs. clear linear low-density
polyethylene (LLDPE) (top) and black opaque high-density poly­
ethylene (bottom) on biofouling on algal productivity was studied
(Harris et al., 2013). Chemodanov et al. (2017) utilized PE PBRs into the
design of a building. A polyethylene sleeve of 100 m, 200 m, and 0.4 m
length, thickness, and breadth has been developed. Per bag, there is a
total capacity of 40.4 L. The overall volume of the system is 3400 L,
which is distributed over four levels of the building. The water was
swapped from the top and the mixing was done via the bottom of the
bags. Garca-Galán et al. (2018) built full-scale soft-frame PE PBRs for
toilet wastewater treatment and agricultural run-off treatment. Those
PBRs were formerly known as horizontal multi-tubular PBRs.
2.4.2. Microalgae growth in soft frame PBRs
In the plastic bags or soft frame PBRs, a circulation pump maintains
liquid flow as well as air and media supply. This PBR design features a
high surface area to volume ratio. Scenedesmus obliquus was effectively
grown for biofuel production in plastic bag PBRs, with a biomass pro­
ductivity rate of 140 mg (Ld)–1(Abomohara et al., 2014). Also, Por­
phyridium was effectively grown in this configuration as well, giving a
biomass concentration three times higher than that produced in culti­
vation ponds (Cohen and Arad, 1989). Microalgae were cultured and
hanged in three different types of commercial PBs (Schreiber et al.,
2017). The biomass output ranged from 0.3 to 1.5 kg m− 3 at an irradi­
ation intensity of 150 mol photons/m2d, accounting for 2/3 of the
maximum growth rate (Schreiber et al., 2017).Plastic bag PBR with a
volume of 5 L was hung to cultivate C. sorokiniana microalgae on a large
scale (Chen et al., 2013). Growing microalgae as biofilms reduces the
challenges and costs of collecting and processing suspended microalgal
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Bioresource Technology 349 (2022) 126858
biomass. The rotating flat plate photobioreactor (RFPPBR) is a novel
photoautotrophic biofilm PBR that was created with the goal of culti­
vating Chlorella vulgaris at a low cost. Higher adhesion and biofilm
growth were encouraged by polyvinyl chloride, as well as poly­
propylene, polyethylene, and stainless steel (Melo et al., 2018). Ac­
cording to the findings, the photobioreactor is robust, encourages
biofilm development, is simple to run, has a compact footprint, and
enables for easy biomass collection. Areal productivity obtained was
2.99 g m2 day− 1, while biomass output (dry weight) was 3.35 g m− 2. The
total lipid content (dw) was 10.3%, with a high PUFA content.
2.4.3. Biohydrogen production in soft frame PBRs
The use of transparent plastic bags with a gas barrier layer as cheap
photobioreactors for H2 generation by cyanobacterium Anabaena sp.
PCC 7120 Hup mutant cells was investigated (Shastik et al., 2020). The
maximum H2 generation rate was 20.6 mL day -1 L-1 of culture with a
final H2 concentration of 1.1 % (v/v) and a 5 day accumulation of 33.2
mL L-1. Rhodopseudomonas sp. S16-VOGS3 generated poly-3-
hydroxybutyrate and molecular H2 when cultured on acetate or buty­
rate under nitrogen sufficiency (glutamate) or nitrogen deficit. Lactate,
on the other hand, did not produce any results (Carlozzi et al., 2019).
The material used in its construction, however, is prone to damage since
it must withstand a great quantity of pressure. Furthermore, there are
many dead zones, resulting in lower biomass yield, and the cost of
agitation is too expensive for industrial use due to its design (Vo et al.,
2019).
2.5. Hybrid photobioreactors
2.5.1. Configurations and operations
Hybrid photobioreactors (PBRs) are emerging systems that are the
integration of at least two compatible conventional designs such as the
flat- plate and bubble column or other technologies such as membrane
systems which helps to overpower the drawbacks of individual designs
(Show et al., 2017; Vo et al., 2019). One of the significant advantages of
the two-stage approach is the acquisition of benefits from each system to
derive a more efficient design (Soman and Shastri, 2015). For example,
low-cost open ponds combined with closed systems with better condi­
tions might result in a novel hybrid with superior properties. Closed
PBRs provide better control over contamination and biomass growth,
whereas open ponds or raceways are suitable to create nutritional stress
in exposed cells, thus triggering the synthesis of desired metabolites
(Płaczek et al., 2017). Hence, combining two systems in hybrid PBRs
seems promising both economy and technical efficiency, providing good
future perspectives. The two systems are adjusted based on suitable
height/diameter ratio, allowing the higher surface area to volume ratio
and resulting in higher load feasibility and productivity with low cost
and energy use (Singh and Sharma, 2012). The economic feasibility of
hybrid PBRs was revealed in the study by (Huntley et al., 2015),where
inoculum was provided continuously and consistently for a short period,
inhibiting the disruption of the biological system and ensuring sustained
production. The closed PBR required high initial expenditures, but
continuous production could overcome the economic barrier (Fig. 2).
Many novel hybrid PBR designs have been suggested in the litera­
ture; for example, in 2012, a cost-efficient and durable hybrid PBR was
designed and patented (Mottahedeh and Tredici, 2012). The system
consisted of a fibreglass enclosed C- shaped chamber with an open top
and an external removal fibreglass cover to create a close chamber. Both
the components were designed to achieve light irradiation in all di­
rections. Also, the closed chamber could incorporate a solar reflector to
achieve a cost-effective temperature check. Velea et al., (2014) inves­
tigated the biomass productivity of Chlorella homosphaera in a newly
designed hybrid PBR. The design comprised an open tank connected to a
flat plate PBR assembled in parallel and two vertical bubble columns in
series. The entire system was made of transparent material, and light
assembly was arranged over the PBR tank for proper distribution. All the
R. Sirohi et al.
Fig. 2. Influential parameter and outcomes of a photobioreactor for economic feasibility.
design components were connected through pipes to ensure algae
recirculation and gas transfer. Improved flow dynamics and gas transfer
resulted in biomass densities up to 3.6 g L-1 which were reportedly 3
times higher than conventional open tanks. Another hybrid PBR was
configured by (Deprá et al., 2019) to optimize and increase the working
volume and improve the carbon dioxide bioconversion capacity of Sce­
nedesmus obliquus CPCC05.The system consisted of a bubble column
reactor combined with an illumination unit. This assembly was con­
nected to a cylindrical column of polyvinyl chloride with an air diffuser
at the base. Rotameters were used to control the flow of carbon dioxide
enriched air into the reactor. The kinetics of carbon dioxide biocon­
version for S. obliquus CPCC05 showed a maximum specific growth rate
of 0.96 d-1 (Deprá et al., 2019). An indoor helical-tubular PBR was
designed by (Hashemi et al., 2020)to produce beta-carotene within
microalgae Dunaliella salina. The system consisted of an open pond on
the top of a helical tubular PBR connected to an airlift column. The
pump circulates the culture medium through the airlift column con­
nected with both tubular and open pond units. LED lamps set up around
the spiral tube and at the top of the open pond were used for
illumination.
A PBR assembly of airlift reactor driven with an external tubular loop
placed horizontally in a thermostatic water pond was set by Fernández
et al. (2001).The airlift system can help in degassing and integrating
desired probes to control other culture variables. At the same time, the
tubular loop provides a large surface area to volume ratio for efficient
light-harvesting and proper control of culture temperature. The system
provided advantages of better maintenance of culture parameters,
higher productivity and less energy use. (Richmond et al., 1993) set up a
similar PBR unit with loop like light harvesting system whereas, in the
PBR created by (Grima et al., 1994),the system had parallel sets of tubes
placed horizontally for light harvesting. Horizontally placed tubes pro­
vided relatively better photosynthetic capacity. Still, they were not
feasible due to the requirement of a large land area and the cost asso­
ciated with land and the bundles of tubes. Horizontal floating PBR was
developed by (Dogaris et al., 2015) with two plastic films at the top and
bottom of PBR, sealed to each other and attached with two vertical airlift
units. Another novel hybrid PBR design was proposed by (Lee et al.,
8
Bioresource Technology 349 (2022) 126858
1995). The assembly was an α- shaped reactor in which airlifted the
microalgae culture up to 5 m to reach a receiver tank from where the
culture drifted down a PVC tube with an inclination angle at 25◦ . The
culture then reached another bundle of air riser tubes and the process
repeated. Low rates of air flow ensure high liquid flow rate in one di­
rection and the large surface area to volume ratio provide high photo­
synthetic efficiency (Lee et al., 1995). Attached cultivation systems are
known to provide more efficient biomass harvesting than suspended
systems. Keeping this in view, a capillary driven PBR was developed by
(Xu et al., 2017) in which capillary action was utilized to feed nutrients
and water into a polyester microfibers media resulting in biomass with
higher concentration of carbohydrates than proteins; suitable for use in
biofuel production.
The development of PBRs integrated with membrane processes
called membrane PBRs has also been reported in the literature (Gao
et al., 2016, 2015; Praveen et al., 2016). The main drawback associated
with membrane PBRs is the high cost of membranes, (Chang et al.,
2016), in which ion exchange membrane PBR separated wastewater
sources from microalgae chamber. The membrane allowed the flow of
nutrients from wastewater towards the microalgae side without the
transfer of harmful contaminants. Other membrane PBR designs include
integrating flat plate PBR with hollow fibre ultrafiltration membrane at
a large scale (Viruela et al., 2018) and a sequencing batch membrane
PBR (Sheng et al., 2017). Fouling is another major drawback encoun­
tered while using membranes. (Sun et al., 2018) while integrating
microalgae and sludge bioreactor successfully reduced the fouling of
hollow fibre membrane since the oxygen released from algal photo­
synthesis supported bacterial viability, which subjugated fouling.
2.5.2. Microalgae growth
Two-stage hybrid PBR successfully used for oil and astaxanthin
production by Haematococcus pluvialis where an average production rate
of more than 10-ton ha− 1 was achieved (Huntley and Redalje, 2007).
The hybrid PBR (Deprá et al., 2019) showed high performance with
maximum cell biomass of 2.8 kg m− 3, average carbon dioxide conver­
sion rate of 45.32 kg CO2 m− 3 d-1 and average oxygen release rate of
33.98 kg O2 m− 3 d-1. The characteristics of microalgae species also need
R. Sirohi et al.
attention while designing a photobioreactor for high productivity. For
instance, the combination of a closed airlift and helical tubular PBR with
an open pond was suitable for D. salina as it is halophilic and can thrive
in saline conditions. It also has enduring possible contamination in
closed systems (Hashemi et al., 2020). The capillary driven PBR pro­
posed by Xu et al., (2017) provided biomass yield per footprint area of
more than 121.5 gm− 2, and the highest biomass productivity was about
10 gm-2d-1. Retention of about 50% biomass through a membrane
ensuring appropriate microalgae concentration was presented by Bilad
et al., (2014) in a membrane PBR wherein the system could produce
more biomass while also reducing the water footprint by 77%. Thin-film
solar PBR was found to provide biomass productivity as high as 7.07 kg
m-3d-1 (Pruvost et al., 2017), higher than reported by other authors.
Horizontal floating PBR developed by Dogaris et al., (2015) reportedly
provided biomass concentration of 4 gL-1 in indoor conditions and 4.3
gL-1 in outdoor environments.
2.5.3. Hydrogen production through photobioreactors
Microalgae have been recently explored as an alternative source of
renewable energy producing bio-diesel, bio-ethanol and biohydrogen
(Kosourov et al., 2007; Kovács et al., 2006). Microalgae synthesize
hydrogen in two stages: photosynthetic carbon dioxide fixation in the
presence of sunlight, followed by the fermentative breakdown of stored
organic molecules to produce hydrogen (Antal and Lindblad, 2005;
Mallick, 2002; Song et al., 2011). A two-stage system (Oncel and Kose,
2014) was used to study the hydrogen production of Chlamydomonas
reinhardtii strain CC124 in tubular and panel type PBR. The first stage
was aerobic, followed by a second anaerobic stage incorporated with
mixing time and light intensity at each stage. The aerobic phase in
tubular PBR showed 11% more biomass productivity at 31.8 ± 2.1 mg L-
1 − 1
h than panel PBR whereas, in terms of H2 productivity, panel PBR
showed higher H2 production at 1.3 ± 0.05 mL L-1h− 1. Conclusively, the
results suggested using tubular design for the aerobic phase and panel
PBR for anaerobic H2 production (Oncel and Kose, 2014) presented in
Table 1. Immobilization of cells has been used as an effective strategy
during the cultivation of microalgae cells. Immobilized cells do not
clump during growth (Song et al., 2011). They are also reported to
produce a higher amount of hydrogen than free algal cells (Guan et al.,
2004) and immobilized Synechocystis sp. PCC 6803 produced H2
attaining a maximum production rate of 5.73 ± 0.69 mL H2 mg cells− 1
(Touloupakis et al., 2016).
Light, nutrition and pH are the leading factors that influence
microalgae hydrogen production. High light intensity is known to sup­
press photosynthesis and oxygen release while simultaneously sup­
porting the hydrogenase and nitrogenase enzymes that produce
hydrogen (Mallick, 2002; Song et al., 2011). Efficient hydrogen pro­
duction is also assisted by sulphur deprivation as this causes hindrance
in protein synthesis, thus preventing oxygen release (Antal and Lind­
blad, 2005). Arresting oxygen is important since it is an inhibitor of
hydrogenase. Another crucial parameter to be maintained during
hydrogen production by microalgae is pH. Algae generally grow in a pH
range of 4 to 10. Changes in the overall pH of the system are caused by
photosynthetic CO2 fixation, the creation of organic molecules, and the
fermentative production process, resulting in a fall in hydrogen pro­
ductivity. (Rashid et al., 2013) investigated the effects of light intensity,
pH and organic carbon (glucose, fructose, sucrose and malt extract) on
hydrogen production by Chlorella sp. Optical fibre was installed inside
the bioreactor instead of an external light source, which resulted in a
prolonged lag time of hydrogen production. pH 8 was observed as op­
timum for hydrogen production from the microalgae. Among the carbon
sources fed at an optimum concentration (5 g L-1), sucrose resulted in the
highest H2 volume of 1315 mL L-1 while fructose provided the highest H2
production rate of 24 mL L-1h− 1 (Rashid et al., 2013). The effect of
simultaneous sulphur deprivation and nitrogen limitation on hydrogen
production by Chlorella protothecoides was studied by Zhang et al.
(2014). It was observed that nitrogen limitation was relatively more
9
Bioresource Technology 349 (2022) 126858
significant in reducing oxygen release and maintaining anaerobic con­
ditions after 12 h of incubation, resulting in high H2 production. During
light incubation, nitrogen limitation significantly inhibited the relative
variable fluorescence and PS II (photosystem II) photochemical activity.
The inhibition was much higher than in the case of sulphur deprivation
(Zhang et al., 2014). Moreover, it was observed that in the presence of 3-
(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU), an inhibitor of photo­
synthetic electron transfer, the nitrogen-sulphur limited culture rather
than nitrogen-limited culture produced higher H2. This observation
suggested that some other electron source independent of PS II provided
more electrons to hydrogenase in nitrogen-limited sulphur culture
(Zhang et al., 2014). 10 mM DCMU has been reported to induce a 1.5-
fold increase in H2 production by Desertifilum sp. IPPAS B-1220;
increasing the H2 production from 0.229 mmol H2 mg-1Chl h− 1 to 0.348
mmol H2 mg-1Chl h− 1(Kossalbayev et al., 2020). Cyanobacteria have
also been reported to provide higher H2 production in nitrogen and
sulphur limitation (Antal and Lindblad, 2005; Weissman and Benemann,
1977) and various carbon sources (Baebprasert et al., 2010; Khetkorn
et al., 2012). In addition to light, nutrition, and temperature, nickel and
iron concentration alter hydrogenase in cyanobacteria, affecting H2
generation (Carrieri et al., 2008; Vignais et al., 2001). Taikhao et al.,
(2013) investigated the influence of nitrogen and sulphur limitation,
carbon source, light intensity and temperature on H2 production by
cyanobacterium Aphanothece halophytica. H2 production increased four
times in nitrogen limitation, which was not the case with sulphur
deprivation; glucose was the preferred carbon source but H2 production
reduced at high glucose concentration; the optimum temperature and
light intensity for H2 production was 35 ◦ C and 30 μmol photons m− 2s− 1
respectively. Nitrogen limitation favoured H2 production in
A. halophytica but also inhibited cell growth; hence, a two-stage system
was adapted where the first stage involved growth in normal medium for
biomass formation while the second stage included nitrogen depletion to
assist H2 production resulting in as high as 13.804 μmol H2 mg chl
a− 1h− 1 (Taikhao et al., 2013). In a first-ever attempt to explore the
possibility of H2 production in an outdoor environment, (Shastik et al.,
2020) used simple, transparent plastic bags with a gas barrier layer as
PBR to produce H2 by mutant cells of Anabaena sp. PCC 7120. Two
experiments were performed with the average daily temperature at
21.7 ◦ C and 20.6 ◦ C, light intensity at 290 and 340 μmol photon m− 2
s− 1, respectively, for experiment 1 and 2. The maximum H2 production
rate was 20.6 mL day− 1 L− 1 culture with a 5-days accumulation of 33.2
mL L− 1. The lower H2 production rate as compared to other PBRs re­
ported in literature could be seemingly due to the sub-optimal weather
conditions and the elementary design of reactor (Shastik et al., 2020).
Nevertheless, simple plastic bag designs were feasible as outdoor PBR
and could be optimized in future for higher H2 production. To overcome
the microalgae H2 yield limitation, (Hasnaoui et al., 2020) investigated
the impact of a small voltage applied during H2 production by Spirulina
using an electrochemical photobioreactor (EPBR). H2 formed in both
cathodic and anodic chamber by conversion of protons into molecular
hydrogen, and as a result, the EPBR was able to achieve a maximum H2
evolution rate of 44.86 mol H2 m− 3 d-1 at 0.3 V voltage; 4-fold higher
production rate when compared to production without voltage appli­
cation (Hasnaoui et al., 2020). Moreover, the operation of EPBR for
three successive batches, that is, the Electrochemical Sequential Batch
Reactor (ESRB), provided a more effective total H2 production rate at
2.65 m3 m− 3 d-1; batch mode gave 1.2 m3 m− 3 d-1. EPBR could prove to
be an economical alternative to microbial electrolysis cells (MECs) for
high H2 production at relatively lower voltage and current density (2.5
mA) (Hasnaoui et al., 2020).
3. Research needs and perspectives
H2 can be used as a clean energy source for energy generation with
great efficiency. Due to their ability to split water into H2 and O2 using
solar energy, algal strains can be exploited as a possible source of H2
R. Sirohi et al.
energy. There is no one-size-fits-all PBR, and the ideal design is still
determined by the microalgae species and the intended final metabolite.
There are various parameters which still need to be optimized for H2
production in photobioreactors such as changes in geometry and fluid
mixing pattern, improved gas exchange, light penetration, and building
material, all of which have benefits and drawbacks. Most of the studies
favour illumination patterns, fluid dynamics, cooling requirements,
mixing efficiency, and mass transfer when operating PBRs. This results
in increased H2 production, lower prices, and energy savings. In addi­
tion, the designs have been tweaked and coupled with other technolo­
gies, including membranes. A membrane bubble column PBRs, for
example, might minimize reactor size while lowering operating and
maintenance costs. Photobioreactor integration and upgrades will have
a bright future in terms of scalability, operating costs, and sophisticated
setups. Though CFD can be used as an indispensable tool for under­
standing the hydrodynamics, gas–liquid mass transfer in the photo­
bioreactor along with biokinetic and light intensity modelling, an
integrated multi-scale modelling of photobioreactor needs to be devel­
oped for further understanding the insight of photobioreactor which can
lead to better design and operations. The multi-scale model includes a
microscopic kinetic model derived based on photosynthetic units (PSUs)
and meso/macroscopic continuum model for reactor dynamics along
with the light transport model which can be used to simulate spatio-
temporal changes of microalgae growth in the photobioreactors.
4. Conclusions
PBRs are promising option with numerous advantages. In compari­
son to open or natural ecosystems, PBRs have control for processing
parameters and cultivation conditions for microalgal growth and bio­
hydrogen production. Closed PBRs offer effective control on culture
conditions and reduce pollution. Although flat-plate and pipeline-type
PBRs provide easy to control the conditions, large light areas and
higher maintenance costs are major bottlenecks. Internally illuminated
PBRs seem attractive due to separate light-harvesting and cultivation
process. Disposable PBRs are low-cost and potentially sustainable, but
much research needed for large-scale applications. For outdoor culti­
vation, solar-irradiation filtration technologies could be integrated into
PBRs for garnering multiple advantages.
Declaration of Competing Interest
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.
Acknowledgments
The corresponding author acknowledges the funds provided by
Korea Carbon to X, R&D Center (2020M3H7A1098295) and the Na­
tional Research Foundation (NRF-2019R1A2C3009821 / NRF-
2020R1A5A1018052) of the Ministry of Science and ICT of Korea.
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