Bioresource Technology 229 (2017) 222–230

Contents lists available at ScienceDirect

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

Review

Photo-fermentative hydrogen production from crop residue: A mini

review
Quanguo Zhang a, Yi Wang a, Zhiping Zhang a, Duu-Jong Lee a,c,⇑, Xuehua Zhou a, Yanyan Jing a, Xumeng Ge b,
Danping Jiang a, Jianjun Hu a, Chao He a
a
Collaborative Innovation Center of Biomass Energy, Henan Agricultural University, Zhengzhou 450002, PR China
b
Department of Food, Agricultural and Biological Engineering, The Ohio State University/Ohio Agricultural Research and Development Center, 1680 Madison Ave., Wooster, OH 44691-
4096, USA
c
Department of Chemical Engineering, National Taiwan University, Taipei 10607, Taiwan

h i g h l i g h t s

 Technology of bio-hydrogen production from crop residues were reviewed.

 Pretreatment methods and substrate structure were discussed.
 Hydrogen from pure bacteria, consortia and mutants were discussed.
 Geometry, light source and mass transfer properties of bioreactor were reviewed.

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

Article history: Photofermentative hydrogen production from crop residues, if feasible, can lead to complete conversion
Received 29 November 2016 of organic substances to hydrogen (and carbon dioxide). This mini review lists the studies on photofer-
Received in revised form 3 January 2017 mentative hydrogen production using crop residues as feedstock. Pretreatment methods, substrate struc-
Accepted 6 January 2017
ture, mechanism of photosynthetic bacteria growth and metabolism were discussed. Photofermentative
Available online 10 January 2017
hydrogen production from pure culture, consortia and mutants, and the geometry, light sources, mass
transfer resistances and the operational strategies of the photo-bioreactor were herein reviewed.
Keywords:
Future studies of regulation mechanism of photosynthetic bacteria, such as highly-efficient strain breed-
Bio-hydrogen
Photofermentation
ing and gene reconstruction, and development of new-generation photo-bioreactor were suggested.
Crop residues Ó 2017 Elsevier Ltd. All rights reserved.
Pretreatment
Photosynthetic bacteria

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 223
2. Crop residues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 223
2.1. Status of the crop residue resources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 223
2.2. Bio-hydrogen production from the crop residues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 223
2.3. Pretreatment of the crop residues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 224
3. Anoxygenic photosynthetic bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 225
3.1. Pure culture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 225
3.2. Photo-synthetic mutants. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 225
3.3. Consortia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 225
4. Photobioreactor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 226
4.1. Design and operation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 226
4.2. Light sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 227

⇑ Corresponding author at: Department of Chemical Engineering, National

Taiwan University, Taipei 10617, Taiwan. Fax: +886 223623040.
E-mail address: [email protected] (D.-J. Lee).

http://dx.doi.org/10.1016/j.biortech.2017.01.008
0960-8524/Ó 2017 Elsevier Ltd. All rights reserved.
 Q. Zhang et al. / Bioresource Technology 229 (2017) 222–230 223

4.3. Mass transfer characteristics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 228

5. Use of photofermentation to produce biohydrogen from crop residues. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 228
6. Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 228
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 229
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 229

1. Introduction the following formula (CH3COOH + 2H2O ? 2CO2 + 4H2) using

acetate as the model feed substrate. Chandrasekhar et al. (2015)
The global industrial development in the past century heavily commented on the advantages and disadvantages for photofer-
depended on consumption of fossil fuels, not only causing concerns mentative hydrogen production. Uyar (2016) summarized the con-
on depletion of the nonrenewable energy source, but also leading cerns for designing the photofermentative bioreactor. This mini-
to the global warming issue due to greenhouse gases (GHG) emis- review focused on the research progress in photofermentative
sion. A large portion of current fossil fuel reserves (1/3 of oil, 1/2 of hydrogen production using crop residues as feedstocks, consider-
natural gas, and more than 4/5 of coal) should remain unused up to ing the aspects of feedstock types, pretreatment methods, photo-
2050 to meet the 2 °C target for GHG control over the 21st century synthetic bacteria, reactors, and operational strategies on
(Mcglade and Ekins, 2015). Meantime, global energy demand is hydrogen productivity. Perspectives for future studies in photo-
still increasing to nearly doubled by year 2050 (IRENA, 2015). To fermentative hydrogen production from crop residues are
reduce the GHG emission with meeting energy demand, renewable highlighted.
energy supplies, such as biofuels from biomass, are desired (Balan,
2014). It is estimated that biofuel in total transportation fuel would 2. Crop residues
grow up to 27% in 2050 (https://www.iea.org/newsroomande-
vents/pressreleases/2011/April/biofuels-can-provide-up-to-27-of- 2.1. Status of the crop residue resources
world-transportation-fuel-by-2050-iea-report-.html)
Crop residues are produced from corn, wheat, and rice process- Agriculture and forestry are the two sources of renewable car-
ing, with those from China contributing about 23% of corn, 18% of bon sources that can be used for energy production (Chandra
wheat, and 28% of rice over the globe in 2012 (FAOSTAT, 2012). et al., 2012). Compared to forestry residues, agricultural waste usu-
About 0.5 billion dry ton of crop residues were available in China ally has higher cellulose and hemicellulose contents and lower lig-
(Jiang et al., 2012). Liquid and gas fuels, such as bioethanol, biobu- nin contents, making them more favorable for bio-energy
tanol, biomethane and biohydrogen can be produced from this production. Annually, a large quantity of crop residue is produced
abundant and renewable feedstock (Karimi and Taherzadeh, in the world (Lal, 1995). The primary crop residues can be catego-
2016). Among these fuels, hydrogen has the highest energy density rized into cereal crop residue, leguminous crop residue, root crop
per mass (142 kJ/g) and produces no GHG while burning residue, and oil seeds residue. In terms of the total residue produc-
(Ghanavati et al., 2015; Hay et al., 2013). tion quantity, cereals are the most important residue stream than
Global hydrogen market was estimated to grow annually at a the other three.
rate of 6.2% from 2011 ($87.5 billions) to 2016 ($118 billions), with The main worldwide production of cereal crop residue is com-
88% of hydrogen being produced from nonrenewable energy posed of rice straw, wheat straw, corn stover, and sugarcane
sources, such as natural gas, heavy oil, naphtha, and coal (Hay bagasse (Bakker et al., 2013). Due to the different demands of the
et al., 2013). There are efforts for bio-hydrogen production from crops on climate and availability of water, the four major straws
biomass and wastewater with microorganisms. Bio-hydrogen can can be collected from different locations: rice straw and wheat
be produced by: (1) bio-photolysis with cyanobacteria or green straw are mostly produced in Asia, America is the major producer
algae, (2) dark fermentation with anaerobic bacteria, (3) photofer- of corn stover and sugarcane bagasse (Sarkar et al., 2012). The com-
mentation with photosynthetic bacteria, and (4) microbial electrol- position of various constituents in crop residue varies from one
ysis. During bio-photolysis process, light energy is converted to plant species to another. Table 1 presents the chemical composi-
free energy of hydrogen at a low efficiency (theoretical efficiency tions of the four major crop residues and illustrates the annual pro-
no more than 4.6%), which limits its application to a practical sys- ductions in China. Among the major 4 crop residues, corn stover is
tem (Hallenbeck, 2012). Dark fermentation also has a drawback of the largest crop residue stream in China (327.4 million ton/year).
low H2 yields due to accumulation of volatile fatty acids. In con- Conversely, production of sugarcane bagasse is much lower in
trast, photo-fermentation can use organic compounds, usually quantity than other three crop residues.
organic acids, as the substrates (Hallenbeck and Ghosh, 2009;
Keskin and Hallenbeck, 2012). 2.2. Bio-hydrogen production from the crop residues
Extensive reviews on dark fermentation are available; con-
versely, only few information on photofermentative hydrogen pro- Cellulose, hemicellulose, and lignin are main components of
duction from crop residues is available (Hay et al., 2013). crop residues. Cellulose is a polysaccharide with b-1,4-glycosidic
Photofermentation bio-hydrogen production can be described by bonds. Crystalline cellulose is resistant to digest while amorphous

Table 1
Chemical compositions of four major crop residues and H2 production potential in China.

Crop residue Cellulose Hemicellulose Lignin Production in China References

(%) (%) (%) (million tones/yr)
Rice straw 32–47 19–27 5–24 195.1 Saratale et al. (2008) and Jiang et al. (2012)
Wheat straw 33–38 26–32 17–19 126.6 Saratale et al. (2008) and Jiang et al. (2012)
Corn stover 33,37.5 28,30 8.4 327.4 Zhang et al. (2014a), Jiang et al. (2012) and Li et al. (2009a)
Sugarcane bagasse 40–45 30–35 20–30 12.2 Rai et al. (2014) and Jiang et al. (2012)
224 Q. Zhang et al. / Bioresource Technology 229 (2017) 222–230

cellulose is more readily to be digested. Hemicellulose is polysac- (grinding, steam-explosion, extrusion, imposing irradiation,
charides of mono-sugars and uronic acids with randomly branched hydrothermolysis), chemical pretreatment (acids, bases, ionic liq-
heterogenetic structures (Lin et al., 2015). Hemicellulose itself is uids), and/or biological pretreatment (enzymes, fungus) (Yang
usually amorphous in structure, thus is easy to digest. However, et al., 2015a,b). Pretreatment for hydrogen production from crop
hemicellulose can interact with cellulose and lignin to form a net- residues, such as corn stalk, sugarcane bagasse, and wheat straw,
work structure which increases the recalcitrance of biomass. Lignin has been studied (Reginatto and Antônio, 2015).
is a class of complex heteropolymers of aromatic alcohols, and is A few studies were reported on pretreatment of crop residues
the most recalcitrant component of lignocellulose. The rigid for photo-fermentative hydrogen production (Mirza et al., 2013),
three-dimensional cross-linked matrix, composed of cellulose, particularly on pretreatment for dark and photo-fermentative
hemicellulose and lignin, resists hydrolysis of lignocellulosic hydrogen production from crop residues (Table 2). Water hyacinth,
biomass. rich straw, barley straw, corn stalk, and corn cob have been studied
Photofermentation enables the conversion of organic substrate to for bio-hydrogen production via pretreatment, enzymatic hydroly-
hydrogen by anoxygenic photosynthetic bacteria to carbon dioxide sis, and dark- and photofermentation. The maximum hydrogen
and biomass (Ghimire et al., 2015). In this process, both the reducing yield through combined dark fermentation and photofermentation
power from oxidation reaction of organic compounds and the energy from treated crop residues ranged 463–752 mL/g total volatile
deriving from light reduce H+ to H2 gas (Adessi and de Philippis, solids. Grinding pretreatment of crop residues decreased particle
2012). Photofermentative hydrogen was yielded by nitrogenase of size and lowered structure crystallinity, which makes cellulose
photosynthetic bacteria coupled with photosynthetic phosphoryla- raw materials exposed to enzyme action for enhanced, follow-up
tion. Since these bacteria exhibit a photosystem not powerful hydrogen production. Steam-explosion pretreatment destroyed
enough to directly split water molecules, the electrons from oxida- the cellulose internal hydrogen bond network and freed out new
tion reaction of organic substances are transported through electron free hydroxyl for improved reducing sugar production (Jin and
carriers to pump protons through cell membrane to produce ATP. Chen, 2006). Acid made almost all hemicellulose but lignin in bio-
Then part of the used electrons is sent to ferredoxin, which drives mass to dissolve so can be used to spin off lignin from the feed
electrons to nitrogenase with the formed ATP to produce hydrogen stock (Kim et al., 2001). Alkaline pretreatment caused crop resi-
under nitrogen (NH+4) starving conditions. dues materials swelling, leading to increase in internal surface area
The crop residues are incorporated proteins and amino acid- and reduce polymerization and the crystallinity of biomass. Acid
containing substances, whose hydrolysis generate high contents pretreatment was found to be more efficient than alkaline pre-
of ammonium ions under anaerobic and neutral and alkaline con- treatment for water hyacinth which has high contents of hemicel-
dition. Pre-oxidization step may be needed to convert ammonium lulose (up to 55% of dry weight). Su et al. (2010) pretreated water
to nitrate for prevent severe inhibition on anoxygenic photosyn- hyacinth using steam heating + microwave-assisted alkaline, and
thetic bacteria in photofermentative hydrogen production. followed by enzymatically hydrolysis, to reach less than 60% of
theoretical hydrogen yields in the follow-up combined dark fer-
2.3. Pretreatment of the crop residues mentation and photofermentation steps. In another study, the fer-
mentative hydrogen yield from water hyacinth was increased to
The substrates containing starch and cellulose need pretreat- 75.2% by microwave-assisted dilute H2SO4 pretreatment (Cheng
ment to be depolymerized into simple organic matters (Keskin et al., 2013). Alkaline pretreatment is efficient in lignin removal,
et al., 2011). Hence, photofermentative hydrogen production from and thus is more suitable for reducing biomass recalcitrance of
crop residues with photosynthetic bacteria is basically the utiliza- crop straws that have high lignin content (about 22–29%). Cheng
tion of simple monomers which are the products of saccharifica- et al. (2010) used microwave-assisted alkali to pretreat rice straw,
tion rather than of the recalcitrant biomass directly. and obtained a maximum hydrogen yield of 463 mL/g TVS via com-
Pretreatments can be achieved through physical pretreatment bined dark- and photofermentation. Yang et al. (2015a,b) studied

Table 2
Hydrogen yield for photo-fermentative or combined hydrogen production from crop residues.

Feedstock Pretreatment Fermentation Max H2 yield Percent References

yield
Photo-fermentation
Wheat straw 4% H2SO4 at 121 °C for 30 min – 254 mL/L – Mirza et al.
(2013)
Detoxification with Ca(OH)2 – 372 mL/L – Mirza et al.
(2013)
30% (v/v) ammonia at 50 °C for 24 h Cellulase 80 FPU/g, b-glucosidase 220 CbU/mol, 712 mL/L – Mirza et al.
50 °C for 24 h (2013)
Wheat straw 6% Ca(OH)2 at 120 °C for 2 h Cellulase 0.1 g/g-substrate, 50 °C for 84 h 2.1 mol/mol – Jiang et al.,
glucose 2015
Corn stover 6% Ca(OH)2 at 120 °C for 2 h Cellulase 0.1 g/g-substrate, 50 °C for 84 h 1.9 mol/mol – Jiang et al.
glucose (2015)
Dark- and photo-fermentation
Water hyacinth (microwave-assisted) Cellulase 500 U/g-substrate + 1.67 g/L of CaCl2, 751.5 mL/g TVS 75.2% Cheng et al.
40 °C for 72 h (2013)
microwave (420 W) for 1.0 min Cellulase 500 U/g-substrate + 1.67 g/L of CaCl2, 596.1 mL/g TVS 59.6% Su et al., 2010
45 °C for 48 h
Rice straw 0.5% NaOH at 140 °C for 15 min Cellulase 500 U/g-substrate + 1.67 g/L of CaCl2, 463 mL/g TVS 43.2% Cheng et al.,
(microwave-assisted) 40 °C for 96 h 2010
Corn stalk 0.75% NaOH at 108 °C for 0.5 h Cellulase 12 IU/g-CS, hemicellulase 2400 IU/g-CS, 594.4 mL/g TVS – Yang et al.
50 °C for 10 h (2015a,b)
Corn cob 1.5% HCl at 100 °C for 0.5 h Cellulase 6.5 U/g, 50 °C 738.1 mL/g TVS – Yang et al.
(2010a)
 Q. Zhang et al. / Bioresource Technology 229 (2017) 222–230 225

the effects of NaOH delignification/enzymatic hydrolysis with cel- (Chromatiaceae), green nonsulfur bacteria (Choloroflexus), and
lulase and hemicellulase on dark- and photofermentative hydro- green sulfur bacteria (Chlorobiaceae) (Chen et al., 2011). Among
gen from corn stalk, obtaining a maximum hydrogen yield of these organisms, PNS bacteria which contain photosynthetic pig-
594.4 mL/g total volatile solids. NaOH concentration was found ments and are able to perform anoxygenic photosynthesis under
to be the most significant parameter followed by cellulase dosage anoxic conditions are used for photo-hydrogen production (Adessi
quantity, temperature of hydrolysis reaction, hemicellulose activ- and de Philippis, 2012, 2014). Most studies for photofermentative
ity, and hydrolysis time on hydrogen yields (Yang et al., 2015a,b). hydrogen production is realized directly using simple sugar mono-
Mirza et al. (2013) investigated effect of dilute H2SO4 pretreatment mers (such as glucose) or organic acids (such as acetate and buty-
and ammonia pretreatment on photo-biohydrogen production rate) rather than crop residues since single culture normally lack
from wheat straw with Rhodobacter capsulatus-PK. Wheat straw of capacity in using mixed substrates. Also, the substrate for single
was pretreated using 30% ammonia and then hydrolyzed with cel- cultures needs thorough sterilization and has high risk for secondary
lulase and b-glucosidase to obtain 712 mL/L of hydrogen which pollution on the culture. However, as Table 3 lists, several reports
was higher than those obtained by using dilute H2SO4 pretreat- have employed pure cultures for photofermentative hydrogen pro-
ment (Mirza et al., 2013). Jiang et al. (2016) applied enzymatic pre- duction and dark-photo fermentative hydrogen production.
treatment using cellulase at 50 °C on corn stalk pith and then
produced hydrogen using photosynthetic bacteria. The hydrogen 3.2. Photo-synthetic mutants
yield reached 2.6 mol/mol sugar consumed.
Fermentation inhibitors, such as acetic acid, 5- Numerous metabolic pathways exist in photofermentative
hydroxymethylfurfural (HMF), and furfural, may form during pre- hydrogen production, which are regulated by enzymes such as
treatment processes, especially those use high temperature and/ hydrogenase and nitrogenase. Use of mutagenesis and genetic
or acids for a long time. Mirza et al. (2013) applied dilute H2SO4 engineering techniques to revise hydrogenase and nitrogenase to
on wheat straw biomass to produce hydrolysate, and then detoxify build uptake hydrogenase deletion or multiple nitrogenase expres-
the hydrolysate with added Ca(OH)2. After filtration, more than sion of Rs. rubrum can significantly improve hydrogen yield from
half of HMF and all of the furfural were removed, while mono- lactate + glutamate wastewater (Kern et al., 1994). A
sugars and acetic acid were retained in the hydrolysate (Mirza hydrogenase-deficient mutant by be inserted with the interfering
et al., 2013). The hydrogen production was increased from hupl gene produces three times more hydrogen than the wild
254 mL/L to 372 mL/L due to the implementation of detoxification strain (Yoshino et al., 2006). Masukawa et al. (2002) found that
step, which revealed that yielded acetic acid can also be beneficial the hydrogen production efficiency of cyanobacterium Anabaena
to the subsequent bio-hydrogen production step. dehydrogenase deletion (hoxL-) mutant had 4–7 times higher the
Selecting proper pretreatment methods based on the composi- hydrogen production rate than wild strain under the optimum con-
tions of targeted lignocellulosic biomass is critical for the success ditions. The efficiency of hydrogen production was greatly
of subsequent fermentation process. improved by modified electron transfer chains of Rhodobacter cap-
sulatus (Ozturk et al., 2006). In addition, using genetic technology
3. Anoxygenic photosynthetic bacteria to build oxygen-resistant hydrogenase to improve its tolerance to
oxygen and other adverse environmental factors.
The selection of highly efficient hydrogen-producing strains and The hydrogen-producing mutants with low light dependence
efficient engineered bacteria were the research focus of photo- are of research interests. Kim et al. (2006) concluded that the
fermentative hydrogen production fields. Through the breeding B875 complex is necessary for photosynthetic hydrogen produc-
and modification of high-yield hydrogen production strains the tion by photosynthetic bacteria and the mutants without B850–
photofermentative hydrogen production can gain advantages in 800 complex had enhanced hydrogen production rates. The
market competition in transportation fuels. mutants that can absorb less light at wavelength 350–1000 nm
than the wild strain would yield less pigments but generate more
hydrogen (Kondo et al., 2002a,b).
3.1. Pure culture

Pure cultures of photosynthetic bacteria were applied to pro- 3.3. Consortia

duce hydrogen from various substrates. These anoxygenic photo-
synthetic bacteria can be classified into four phyla: purple The crop residues usually contain a mixture of monosaccharides
nonsulfur (PNS) bacteria (Rhodospirillaceae), purple sulfur bacteria and complex, polysaccharides, which makes its conversion to

Table 3
Photosynthetic bacteria isolated from different medium.

Stains Carbon source Yield References

(mol H2/mol substrate)
Photo-fermentation
Rhodopseudomonas palustris Rice straw 328 mL H2/TVS Cheng et al. (2010)
Rohobatersphaetoide RV Ground wheat 1.23 mol H2/mol glucose Kapdan et al. (2009)
Rohobatersphaetoide (NRLL B-1727) Ground wheat 0.81 mol H2/mol glucose Kapdan et al. (2009)
Rohobatersphaetoide (DSZM-158) Ground wheat 0.97 mol H2/mol glucose Kapdan et al. (2009)
Rhodobactercapsulatus JP91 Beet molasses 10.05 mol H2/mol sucrose Keskin and Hallenbeck (2012)
Dark-photo fermentation
Clostridium butyricum-Rhodopseudomonas palustris Rice straw 463 mL H2/TVS Cheng et al. (2010)
Enterobacter aerogenes(MTCC 2822) and Rhodopseudomonas (BHU 01) Sugarcane 1755 mL H2/l culture Rai et al. (2014)
bagasse
Caldicellulosiruptor saccharolyticus and hup-mutant of Rhodobacter capsulatus Sugar beet 6.85 mol H2/mol glucose Ozgur et al. (2010)
(YO3) molasses
Clostridium butyrium and Rhodobacter sphaeroides Starch 4.9 mol H2/mol hexose Laurinavichene and Tsygankov
(2015)
226 Q. Zhang et al. / Bioresource Technology 229 (2017) 222–230

Table 4
Hydrogen production performance using different consortia.

Strains Substrate Total H2 yield References

Photo-fermentation
Mixture of three different Rhodobacter sp- Wheat powder 3.85 mol H2/mol glucose Argun et al.
solution (2008)
Consortium Corn stalk pith 2.61 mol H2/mol glucose Jiang et al.
(2016)
Consortium Corncob 228.94 mmol H2/ Zhang et al.
L culture (2014a)
Consortium Sorghum stover 149.93 mmol H2/ Zhang et al.
L culture (2014a)
Consortium Corn stover 145.67 mmol H2/ Zhang et al.
L culture (2014a)
Consortium Rice straw 140.45 mmol H2/ Zhang et al.
L culture (2014a)
Consortium Soybean stalk 131.12 mmol H2/ Zhang et al.
L culture (2014a)
Consortium Cotton stalk 118.46 mmol H2/ Zhang et al.
l culture (2014a)
Consortium Apple waste 11.85 mL H2/g TS Lu et al. (2016)
Consortium Sucrose 2.36 mol H2/mol glucose Lee et al.
(2002)
Consortium Sucrose 3.47 mol H2/mol glucose Zhang et al.
(2008)
Dark-photo fermentation
Dairy manure and R. sphaeroides Corncob 713.6 mL H2/g COD Yang et al.
(2010b)
Anaerobic sludge and Rhodobacter sphaeroides (NRRL-B 1727) Ground waste 3.4 mol H2/mol glucose Sagnak and
wheat Kargi (2011)
Anaerobic sludge and Rhodobacter sphaeroides (NRRL-B 1727) Ground wheat 1.32 mol H2/mol glucose Ozmihci and
starch Kargi (2010)
Anaerobic sludge and mixture of Rhodobacter Sphaeroides (NRRL-B 1727), Rohobatersphaetoide (DSZM- Ground waste 1.16 mol H2/mol glucose Argun et al.
158),Rhodopseudomonas palustris (DSMZ-127), Rhodobacter sphaeroide RV wheat (2009)
Mixed culture of Clostridium butyricum; Enterobacter and Rhodobacter Sphaeroides (M-19) Sweet potato 7.2 mol H2/mol glucose Yokoi et al.
starch waste (2002)
Activated sludge and Rhodopseudomonas palustris Water hyacinth 751.5 mL H2/g TVS Cheng et al.
(2013)
Activated sludge and Rhodopseudomonas palustris Cassava starch 2.86 mol H2/mol glucose Su et al. (2009)

hydrogen a challenging task (Keskin et al., 2011). Most researchers obic conditions with light, which means that the reactor should
concerning this aspect claimed that the use of consortia can lead to have a high surface/volume ratio in order to have better distribu-
higher hydrogen yield when dealing with the complex waste tion of light over the reactor volume (Boran et al., 2012).
(Adessi and de Philippis, 2014). Utilization of consortia for fermen- Several aspects, such as penetration of light in grown culture,
tative hydrogen production is more practically feasible than those area by volume (A/V) ratio, agitation speed, temperature and the
by pure cultures since the former are easier to operate and control, gas exchange, should be considered in bio-hydrogen production
and may have a broader feedstock sources (Wang and Wan, 2009). with photosynthetic bacteria (Gilbert et al., 2011). Mixing method
Studies using consortia integrated dark-fermentation and and light distribution and utilization are key issues which influ-
photofermentation for conversion of the waste to hydrogen ence the performance of continuous operation and optimization
(Argun and Kargi, 2011; Argun et al., 2009; Keskin et al., 2011; of H2 production of the bio-hydrogen production systems (Adessi
Ozgur et al., 2010; Su et al., 2009). As listed in Table 4, consortia and De Philippis, 2014; Basak and Das, 2009; Eroglu et al., 2008;
have been used for photofermentative hydrogen production from Zhang et al., 2015). However, due to the electricity consumption,
crop residues. Although the units used in different studies are especially for illumination and mixing of the cultures resulting in
not consistent, the hydrogen yields with consortia are confirmed energy input for the processed lager than energy output (Adessi
to be higher than pure culture. The maximum of hydrogen yield et al., 2012). Design of simple, high-efficient, and low-cost photo-
(7.2 mol H2/mol glucose) from the combination of dark-photo fer- bioreactor is desired.
mentation with consortia is also higher than that with pure culture
(6.85 mol H2/mol glucose), indicating the consortia is efficient in
fermentative hydrogen production. However, loss of consortia 4.1. Design and operation
microbial community stability still challenges the success of fer-
mentative hydrogen production processes. Although works have been done for photobioreactor design and
operations and they have been widely used in the photo-
biohydrogen production, these studies mostly focus on microalgal
4. Photobioreactor cultivation (Degen et al., 2001). Studies on reactor design and oper-
ational strategy for photofermentative hydrogen production, espe-
Photobioreactor plays an important role in bio-hydrogen pro- cially with agricultural residues as feedstock, is largely limited.
duction with PNS bacterium, which must be closed system, owing However, the common constraints for the microalgal photobiore-
to the need to maintain anaerobic conditions and prevent H2 gas actors and the photofermentative bioreactor are mostly identical.
dispersion (Adessi and De Philippis, 2014; Basak and Das, 2009). Large light receiving surface area is required for light collection
Moreover, photosynthetic bacteria produce hydrogen under anaer- for satisfactory reactor performance (Lee et al., 2015). The viscosity
 Q. Zhang et al. / Bioresource Technology 229 (2017) 222–230 227

Table 5
Types of photo bioreactors with the corresponding hydrogen production rate (HPR), light conversion efficiencies (LCE), and H2 yield.

Type of Organism Form of Carbon source Light source Working HPR (mL/L/ LCE H2 yield References
PBR organism volume h) (%) (mol H2/mol
(L) substrate)
Tubular R. capsulatus YO3 Suspension Acetate Solar light 90 8.96 0.2 0.35 Boran et al.
(Hup ) (2012)
Colum R. palustris WP 3–5 in Suspension Wastewater Tungsten Lamps 7.5 8.54 – – Lee et al.
(2011)
Colum Consortium Hau-M1 Immobilization Swine manure Solar light + tungsten 31 36.6 – – Zhou (2007)
wastewater Lamps
Flat panel R. sphaeroides O.U. Suspension Malate Tungsten lamps 1 11 3.3 2.71 Gilbert et al.
001 (2011)
Flat panel R. sphaeroides O. Suspension Malate Solar light 8.0 10 – 4.6 Eroglu et al.
U.001 (2008)
Fiber Rhodopseudomonas Suspension Acetate Side-light optical fiber 0.5 14.56 1.8 1.19 Chen et al.
palustris WP3–5 (2006)
Fiber Rhodopseudomonas Immobilization Acetate Side-light optical 1.0 43.8 2.3 3.63 Chen and
palustris WP3–5 fiber + tungsten Chang (2006)
lamps
Baffle Consortium Hau-M1 Suspension Hydrolysate of LED lamps 2 7.37 mmol/ – 598.21 mmol/ Zhang et al.
corncob residue l/h h (2015)
Annular Rhodobacter Suspension Malate Tubular lamps 1.0 6.5 3.7 4.5 Basak and
triple sphaeroides O.U.001 Das (2009)
jacketed
Biofilm Rhodopseudomonas Immobilization Glucose solution LED lamps 1.2 38.9 56 0.2 Tian et al.
palustris CQK 01 (2010)

of hydrolyzed crop residue is commonly higher than the substrates requirement for large footprints, high energy input due to high
for microalgal cultivation, which would increase the pumping costs flow resistance in the tube, difficulty in temperature control, high
and mixing costs, and the flow patterns inside the photobioreac- material cost, and low light conversion efficiency.
tors would be different. Ooms et al. (2016) commented on the Column reactor is a modified version from tubular reactor. Col-
sunlight-to-biomass conversion efficiency and strategies, suggest- umn reactors can have multiple reactors which are connected in
ing that the sunlight energy that can be adsorbed and the subse- series or in parallel. A lab-scale serial photo-bioreactor was used
quent losses in the process, including the waste by exceeding in a study on hydrogen production with Rhodopseudomonas palus-
saturation limits of photosynthetic systems, energy transduction, tris WP 3-5 with hydrogen fermentation effluent (Table 5) (Lee
cell maintenance and others. The optical engineering strategies et al., 2011).
proposed by these authors, originally aiming at increasing microal- Flat panel reactors were firstly reported in early 1950s (Fern
gae cultivation efficiency, can be also applied for enhancing the et al., 2008). The maximum permissible thickness for flat plate
photofermentative bioreactor performances. For instance, Sun photo bioreactors is proposed to be 5 cm since hydrogen produc-
et al. (2016) doped light scattering nanoparticles to planar waveg- tion rate was first increased as thickness of reactor increases from
uides for improving light distributions in their microalgae cultiva- 1 to 5 cm, but was then decreased beyond 5 cm thickness (Gilbert
tion reactor. This design modification increased the illumination et al., 2011; El-Shishtawy et al., 1998). Compared with tubular
surface area/volume ratio by more than 10 times and the microal- reactor, flat panel reactors seem to have an identical configuration
gae biomass production rate by 2.2 times. Light management, from potential and were reported to be more economically feasible (Lehr
collection, distribution to adsorption is the key for successful pho- and Posten, 2009). Zhang et al. (2015) compared the performances
tobioreactor design for photofermentative biohydrogen of three different photobioreactors with hydrolyzed corncob, find-
production. ing that the baffle reactors which are designed based on flat panel
By design geometry of the reactor, the common photobioreac- reactor harvested the highest hydrogen yield (589.21 mmol/L) and
tors can be categorized into flat panel and tubular reactors, which exhibited higher substrate conversion efficiency (40.48%) than
can be further classified into with exterior lighting and interior bath reactor or tubular reactor.
lighting based on the location of light source (Boran et al., 2010).
As shown in Table 5, types of photobioreactors have been utilized 4.2. Light sources
in photo-biohydrogen production. The use of exterior lighting is
higher than that of interior lighting. Photofermentation can be performed with light as energy
Tubular reactors may be the first and simplest type of reactor means that light is a critical parameter during the evolution pro-
developed for photo- hydrogen production. Tubular reactor gener- cess of bio-hydrogen. Indeed, light quality and source, light inten-
ally consists of one or multiple transparent tubes with same/differ- sity, and light distribution into the photo bioreactors are the key
ent sizes. The structure can be single cylinder, parallel cylinders, or issues to be considered in designing a photo bioreactor and opti-
sinusoidal tubes. Compared with flat panel reactor, the tubular mizing the bio-hydrogen production (Adessi and De Philippis,
reactor has higher surface to volume ratio to allow the cells to be 2014). The light sources frequently utilized for photo bioreactors
illuminated uniformly (Adessi and De Philippis, 2014; Boran are natural solar light, tungsten lamps, and Light Emitting Diodes
et al., 2010). Moreover, the tubular reactor has enhanced hydrogen (LEDs). As shown in Table 6, researches were conducted the exper-
production rate and solid-liquid separation rate since the associ- iments by using the three major light sources. Light conversion
ated mass transfer rate between the liquid and the gas phase is efficiency during biohydrogen production processes is relatively
high (Boran et al., 2010; Zabut et al., 2006). The main drawback low (average of 1–5%, highest of 7.9%) (Yigit et al., 1999) (Table 6).
is the limited diameter of tube for confined working volume, For scale-up system, in order to achieve a stable and cost-effective
228 Q. Zhang et al. / Bioresource Technology 229 (2017) 222–230

Table 6
Comparison of performances using different light sources.

Light Category Advantages Disadvantages References

sources
Solar light – 1. The energy input is the lowest 1. Affected by the weather and season Miyake et al. (1999b) and Adessi and De
2. Is necessary for permanent 2. In day time, the solar altitude, light Philippis (2014)
utilization intensity, and solar spectrum vary
3. Possesses a wide solar spectrum significantly
4. Is suitable for scale-up system
Artificial Tungsten 1. Possess a variety of light 1. Life time is short Kawagoshi et al. (2010)
light lamps wavelength 2. The energy input is higher than LEDs and
2. Is more stable than solar light solar light
LEDs 1. Life time is longer than tungsten 1. The energy input is higher than solar light Adessi and De Philippis (2014)
lamps
2. The cost is lower than tungsten
lamps
3. Is more stable than solar light

photo-hydrogen, several strategies have been proposed to enhance were use as complimentary light source, obtaining the highest
photofermentative hydrogen production. Rapid mixing has been hydrogen production rate of 36.6 mL/L/h by using swine manure
suggested based on the ‘‘flashing light effect” demonstrated by wastewater as substrate (Zhou, 2007). There is room for further
Patrick C (Hallenbeck and Benemann, 2002). improvement on light conversion efficiency with modified reactor
Ogbonna et al. (1999) reported an internally illuminated stirred resign; however, the related studies are largely lacking in litera-
tank photobioreactor, using solar light collected with a device and ture. The crop residues hydrolysates generally contain excess fine
distributed inside the reactor through optical fibers. This design particles than the feeds to other related photo studies such as those
makes it possible to use solar light for indoor photo-bioreactors. on microalgal cultivation. The excess fine particles would largely
The device was equipped with a light tracking sensor which guides affect the light distribution and utilization efficiency and lead to
the lenses rotating with the position of the sun (Ogbonna et al., severe fouling on the transparent surfaces of the photoreactors.
1999). Exposure to light–dark cycles can also improve hydrogen Anti-fouling surfaces may be a must for the revised photofermen-
production compared to continuous illumination (Miyake et al., tative biohydrogen reactors (Kim et al., 2015).
1999b). Chen et al. (2008) integrated the photo-hydrogen produc- The efficiency for photofermentative hydrogen production is
tion using artificial and solar light systems. Besides, hydrogen pro- about two orders of magnitude less than that for dark fermentation
duction with mix strains that contains different photosynthetic pathways since the growth rate for anoxygenic photosynthetic
bacteria with different photosynthetic features is also a promising bacteria is much lower than the fermentative bacteria. Therefore,
scenario (Kondo et al., 2002a,b). In addition, light conversion effi- the reactor size for the former should be much larger than the lat-
ciency for different types of bioreactors were evaluated, which ter for unit hydrogen production rate. However, the photofermen-
can be used as the benchmarks for bioreactor design to improve tation process can theoretically completely convert organic
light conversion efficiency and hydrogen production in individual substances into hydrogen, which cannot be achieved using dark
applications (Miyake et al., 1999a,b). fermentation processes. Proper pretreatment methods should be
selected for different crop residues according to their composition.
Further efforts are needed to optimize pretreatment methods,
4.3. Mass transfer characteristics
increase effectiveness of photo bioreactors, and commercialize
these technologies.
Reactor size and structure, flow rate and pattern determines the
The cost for photofermentative hydrogen production process
flow field in bioreactor (Zhang et al., 2014b). Relationship between
remains high to be competitive in the current market (US Depart-
the reactor volume, reflux ratio, temperature and hydrogen yield,
ment of Energy set up the goal of biohydrogen production cost of
and the energy balance in the dark-fermentation bio-hydrogen
2.6 USD/kg-H2). Taking a hydrogen production rate at 50 mL/L/h,
production was examined (Obazu et al., 2012). To enhance the
10 h time period with sufficient sunlight, the production of one
mass transfer by swing flow in plate bioreactor (Gilbert et al.,
kg of H2 with density 0.08 kg/m3 requires 25 m3 reactor volume.
2011) or by medium shaking (Li et al., 2009b) would increase the
Taking a planer reactor with thickness of 5 cm, the foot print of
maximum hydrogen yields. The photo-fermentation bio-
the reactor is 500 m2. Hence, to minimize the operational cost with
hydrogen production system from crop residues with a high con-
reactor performance enhancement is not a feasible option. Copro-
centration of solid phase, high viscosity and low light transmit-
duction of valuable products with the hydrogen may provide the
tance needs extensive mixing; a novel reactor design with
financial niche. The production of hydrogen and polybeta-
minimum mixing power input is desired.
hydroxybutyrate via photofermentation process demonstrated by
Corneli et al. (2016) is an example for the proposed niche. Hydro-
5. Use of photofermentation to produce biohydrogen from crop gen has wide applications. Techno-economic analysis could help in
residues reducing capital and operational cost for industrial application of
the photo bioreactors.
Chen and Chang (2006) combined the interior light (side-light
optical fiber) and exterior light (tungsten lamps) system for
photo-hydrogen production with an indigenous PNS photosyn- 6. Conclusions
thetic bacterium Rhodopseudomonas palustris WP3-5, resulting in
a maximum hydrogen production rate level of 43.8 mL/L/h. An Few attention is paid to photofermentation for biohydrogen
interior lighting reactor for photo-fermentative hydrogen produc- production since it has much slower productivity and needs excess
tion was developed by Henan Agricultural University, which had light source to drive the reactions compared with the dark fermen-
a light source inserted via optical fiber, and incandescent lamps tation. Complete conversion of organic substrates to hydrogen is
 Q. Zhang et al. / Bioresource Technology 229 (2017) 222–230 229

the main niche for photofermentation processes, however, the Degen, J., Uebele, A., Retze, A., Schmid-Sttaiger, U., Ttosch, W., 2001. A novel airlift
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