Bioresource Technology 135 (2013) 182–190

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

Potentials of macroalgae as feedstocks for biorefinery

Kyung A Jung a, Seong-Rin Lim b,⇑, Yoori Kim a, Jong Moon Park a,c,⇑
a
Advanced Environmental Biotechnology Research Center, School of Environmental Science and Engineering, POSTECH, 77 Cheongam-ro, Nam-gu, Pohang 790-784, South Korea
b
Department of Environmental Engineering, Kangwon National University, 1 Kangwondaehak-gil, Chuncheon 200-701, South Korea
c
Department of Chemical Engineering, Division of Advanced Nuclear Engineering, POSTECH, 77 Cheongam-ro, Nam-gu, Pohang 790-784, South Korea

h i g h l i g h t s

" This review focuses on the potential of macroalgae as a biorefinery feedstock.

" Their basic information and background knowledge are summarized.
" Their production status and carbohydrate compositions are investigated.
" Up-to-date macroalgae-based biorefinery technology and research are examined.
" Macroalgae could be utilized as a new promising biomass for low-carbon economy.

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

Article history: Macroalgae, so-called seaweeds, have recently attracted attention as a possible feedstock for biorefinery.
Available online 17 October 2012 Since macroalgae contain various carbohydrates (which are distinctively different from those of terres-
trial biomasses), thorough assessments of macroalgae-based refinery are essential to determine whether
Keywords: applying terrestrial-based technologies to macroalgae or developing completely new technologies is fea-
Bioenergy sible. This comprehensive review was performed to show the potentials of macroalgae as biorefinery
Biorefinery feedstocks. Their basic background information was introduced: taxonomical classification, habitat envi-
Biomaterials
ronment, and carbon reserve capacity. Their global production status showed that macroalgae can be
Macroalgae
Seaweed
mass-cultivated with currently available farming technology. Their various carbohydrate compositions
implied that new microorganisms are needed to effectively saccharify macroalgal biomass. Up-to-date
macroalgae conversion technologies for biochemicals and biofuels showed that molecular bioengineering
would contribute to the success of macroalgae-based biorefinery. It was concluded that more research is
required for the utilization of macroalgae as a new promising biomass for low-carbon economy.
Ó 2012 Elsevier Ltd. All rights reserved.

1. Introduction
Over the last decades, the world has been facing crucial eco-
nomic and environmental issues such as fossil fuels depletion
and climate change. These issues have led to the expansion of Re-
search and Developments (R&D) on alternative energy with high
renewability and sustainability. As a direction of the R&D, biorefin-
ery has been spotlighted as a potential solution to escape from the
fossil-based economy (Ragauskas et al., 2006). Biorefinery is de-
fined as sustainable processing that can convert biomass into var-
ious marketable products and energy (IEA, 2009). Thus, biorefinery
⇑ Corresponding authors. Address: Department of Environmental Engineering,
Kangwon National University, 1 Kangwondaehak-gil, Chuncheon 200-701, South
Korea. Tel.: +82 33 250 6358; fax: +82 33 254 6357 (S.-R. Lim), tel.: +82 54 279
2275; fax: +82 54 279 2699 (J.M. Park).
E-mail addresses: srlim@kangwon.ac.kr (S.-R. Lim), jmpark@postech.ac.kr (J.M.
Park).
should take into account the sustainability of final products. This
implies that biorefinery products should be produced without
impacting our economy and ecosystems from the life cycle per-
spective (Fargione et al., 2008; IEA, 2009; Ragauskas et al., 2006).
Since biorefinery has utilized mainly crop biomass to produce
liquid biofuels (e.g. bioethanol and biodiesel), that biorefinery
has significantly affected the world economy due to the competi-
tion for energy and food. World production of bioethanol reached
over 51000 million liters in 2007 (RFA, 2008), and 70% of ethanol
was produced mainly from corn and sugarcane in the United States
and Brazil, respectively (Sánchez and Cardona, 2008). Although
bioethanol can be produced from lignocellulosic biomass as well,
at present crops are regarded as the best energy resources due to
their high ethanol yield and well-established fermentation tech-
nology. Consequently, this has induced the competition for energy
and food resources in the global market (Sánchez and Cardona,
2008). This situation also has occurred with biodiesel because it
is produced from food resources such as soybean, palm oil,

0960-8524/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.biortech.2012.10.025
 K.A Jung et al. / Bioresource Technology 135 (2013) 182–190
rapeseed, and sunflower (Atabani et al., 2012). Due to surging food
cost from the competition, global economies have become unsta-
ble; in 2006, global food stocks of major grains such as rice, wheat,
and corn were at their lowest for the past 20 years (Heady and Fan,
2008).
In environmental aspects, terrestrial biomass-based biorefinery
can rather exacerbate climate change when taking into account
the life cycle of its final products. Fargione et al. (2008) and
Dominguez-Faus et al. (2009) reported that direct and indirect land
use change for energy crop cultivation induces a significantly high car-
bon debt and high water consumption. Although many researchers
have been trying to utilize lignocellulosic biomass that is not used
for food, this biomass can still incur the same environmental con-
sequences associated with land use and water consumption
(Dominguez-Faus et al., 2009; Fargione et al., 2008). Thus, terres-
trial biomass-based biorefinery seems not to be sustainable at
present due to environmental as well as economic impacts.
Marine macroalgae, so-called seaweeds, have the high poten-
tials to fully and partly displace terrestrial biomass and produce
sustainable bioenergy and biomaterials. Macroalgae do not need
land and freshwater for their cultivation (Lobban et al., 1985). Mac-
roalgae can convert solar energy into chemical energy with higher
photosynthetic efficiency (6–8%) than terrestrial biomass (1.8–
2.2%) (FAO, 1997). Also, macroalgae have a lower risk for the com-
petition for food and energy than other energy crops like corn and
wheat as seaweed markets are mainly in a few East Asia countries
where seaweed is used for food, hydrocolloids, fertilizer, and ani-
mal feed (Bixler and Porse, 2011; McHugh, 2003). Despite the envi-
ronmental and economic merits of macroalgae, many challenges
exist as macroalgae have unique carbohydrates, which are distinc-
tively different from those of terrestrial biomass (Roesijadi et al.,
2010; Sze, 1993). Due to the carbohydrate difference, terrestrial
biomass-based technology cannot be directly applied to macroal-
gal biomass. Therefore, it is imperative to thoroughly review the
accumulated knowledge and information on macroalgae-based
biorefinery.
The objective of this review is to comprehensively provide up-
to-date knowledge and information on macroalgae-based biorefin-
ery to show the potentials of macroalgal biomass as a feedstock for
biorefinery. Although ongoing researches on macroalgal biofuels in
both academia and industry are at infancy, interests in macroal-
gae-based biorefinery continue to increase because of the necessity
to resolve environmental and economic drawbacks of terrestrial
biomass-based biorefinery. This recently leads to the publication
of many research papers on macroalgal biomass and biorefinery
applications. This review first deals with basic backgrounds on
macroalgae: taxonomical classification, habitat environment, and
carbon reserve capacity. To examine a feedstock supply potential
of macroalgae, their global mass-cultivation status and carbohy-
drate compositions are investigated. We also examine and discuss
the macroalgae-based technology and research developed to con-
vert various macroalgal carbohydrates to biomaterials and bioen-
ergy. This review can help terrestrial biomass-oriented
researchers understand macroalgae as a promising new biomass
for a low-carbon economy.
2. Macroalgae backgrounds
2.1. Taxonomical classification
Macroalgae are multicellular photosynthetic organisms and be-
long to the lower plants, consisting of a leaf-like thallus instead of
roots, stems, and leaves (Lobban et al., 1985). Macroalgae are clas-
sified as green, red, and brown algae, according to the thallus color
derived from natural pigments and chlorophylls (Sze, 1993).
183
Green algae belong to phylum Chlorophyta, which has the same
ratio of chlorophyll a to b as land plants (Lobban and Wynne,
1981). Lewis and McCourt (2004) have addressed that higher green
plants (particularly, herbaceous plant) had evolved from green al-
gae. Although this is still controversial, there is no doubt that bio-
chemical compositions of green algae are similar to land plants.
There are about 4500 species of green algae including 3050 species
of freshwater-favorable algae (class Trebouxiophyceae and Chloro-
phyceae) and 1500 species of seawater-favorable algae (class
Bryopsidophyceae, Dasycladophyceae, Siphoncladophyceae, and Ulvo-
phyceae) (Guiry, 2012).
Red algae are all included in a single class (i.e., Rhodophyceae)
consisting of two subclasses: Florideophycidae and Bangiophycidae.
The red color is derived from chlorophyll a, phycoerythrin and
phycocyanin (Lobban and Wynne, 1981; Sze, 1993). There are
4000–6000 species of red algae in over 600 genera, and most of
them exist in tropical marine environments (Yu et al., 2002).
Brown algae are classified as Phaeophyceae under phylum
Chrysophyta. Their principal photosynthetic pigments are chloro-
phyll a and c, b-carotene, and other xanthophylls (Sze, 1993). There
exist 1500–2000 species (Hoek et al., 1995).
2.2. Habitat environment
The pigment, growth, and chemical composition of macroalgae
are significantly affected by their habitat conditions such as light,
temperature, salinity, nutrient, pollution, and even water motion,
particularly depending on their taxonomical classes and species
like Porphyra, Gelidium, Laminaria, Sargassum, Ulva and Enteromor-
pha spp. (Lobban et al., 1985). Among the conditions, light is the
most principal contributor. Thus, the classes of macroalgae are ver-
tically distributed from the upper zone (close to the sea surface) to
the lower sublittoral zone (Lobban et al., 1985). This is because
macroalgae have their respective pigments, which absorb selec-
tively the light with specific wavelengths (Guiry, 2012). For in-
stance, while most macroalgae live in the littoral zone near
coastal line, some red algae like Gelidium sp. inhabit the deep sea
(over 25 m below the surface) where sunlight availability is limited
(Santelices, 1991). Gelidium sp. has phycoerythrin and phycocyanin
pigments, which can efficiently absorb light with wavelengths of
photosynthetically active radiation (PAR) that can penetrate sea-
water to the deep zone (Santelices, 1991). As such, the habitat
environment affects growth rates, size, weight, and chemical com-
position (Adams et al., 2011).
2.3. Carbon reserve capacity
Macroalgae are photoauxotrophic and thus produce and store
organic carbons (i.e., carbon sources for biorefinery) by utilizing
either CO2 or HCO3 (Gao and McKinley, 1994). Most macroalgae
directly uptake HCO3 rather than CO2 for their growth because
the diffusion rate of CO2 is extremely slow in seawater (Lobban
et al., 1985). However, a few macroalgae can utilize CO2 as a direct
substrate or accelerate the inter-conversion between CO2 and
HCO3 by using enzymes such as RuBP carboxylase and carbonic
anhydrase (Lobban et al., 1985).
Due to the high photosynthetic ability of macroalgae, they have
the potential to generate and store sufficient carbon resources
needed for biorefinery. Table 1 shows photosynthetic rates of mac-
roalgae. The photosynthetic rates highly vary depending on their
species (even in the same group). Note that Enteromorpha (green
alga) and Porphyra (red alga) have the highest photosynthetic rates,
which are 1–2 orders of magnitude higher than those of brown al-
gae. It should also be mentioned that macroalgae have higher pro-
ductivity rates than terrestrial biomass such as corn and
switchgrass (Chung et al., 2011). Chung et al. (2011) estimated that
184 K.A Jung et al. / Bioresource Technology 135 (2013) 182–190

Table 1 to 15.8 million wet tons, which were harvested from wild habitats
Photosynthetic rates of macroalgaea. and aquaculture farms in 2010 (note that most of them were mass-
Species Photosynthetic rateb (lmol CO2/h) cultivated in farms) (FAO, 2012a). As shown in Table 2, the amount
Green algae of the mass-cultivated macroalgae is four and six orders of magni-
Acrosiphonia centralis 468 g dry 1 tude greater than for the microalgae and lignocellulosic biomass,
Cladophora rupestris 30.5 g dry 1 respectively, even though the macroalgae is two orders of magni-
Codium fragile 68.3 g dry 1 tude less than the energy crops. This implies that with current
Enteromorpha sp. 1786 g wet 1
Monostroma grevillei 1466 g dry 1
farming technology, macroalgae can be more mass-cultivated to
Ulva sp. 48.7 g dry 1 sufficiently supply feedstocks for biorefinery.
Red algae
At present the most promising macroalgae species for biorefin-
Asparagopsis taxiformis 174 g dry 1 ery feedstock are Laminaria japonica, Eucheuma spp., Kappaphycus
Chondrus crispus 21.2 g dry 1 alvarezii, Undaria pinnatifida, and Gracilaria verrucosa (Table 2).
Delesseria sanguinea 37.9 g dry 1 For brown algae, only two species, L. japonica and U. pinnatifida, ac-
Gracilaria sp. 85 g wet 1
count for over 40% of the total. For red algae, Eucheuma, Kappaphy-
Iridaea cordata 29.4 g dry 1
Porphyra sp. 1808.7 g dry 1 cus and Gracilaria spp. account for about 40%. In contrast, the
production amount of green algae is negligible. Considering cur-
Brown algae
Alaria marginata 109.3 g dry 1 rent mass-cultivation technology and market demand, macroal-
Cymathere triplicata 58.5 g dry 1 gae-based refinery technology needs to be focused on utilizing
Dictyopteris sp. 221 g dry 1 brown and red algae rather than green algae.
Fucus sp. 561 g dry 1 To increase the amount of macroalgal biomass for biorefinery
Laminaria sp. 124 g dry 1
Macrocystis sp. 171.8 g dry 1
globally, international cooperation would be necessary to dissem-
Sargassum sp. 415 g dry 1 inate and improve the farming technology and experience of the
a
East Asian countries (i.e., China, Korea, Japan, Indonesia, and the
Adjusted from Gao and McKinley (1994), Lobban and Wynne (1981).
b Philippines), which are the principal macroalgae producers (FAO,
Estimated in lmol CO2/h on the basis of dry weight (g dry 1) or wet weight
(g wet 1). 2012a). These countries accounted for 95% of the world’s supply
in 2010. Major species cultivated in the countries are different
due to habitat conditions such as climate. For L. japonica and U. pin-
macroalgae cultivation along coastlines could sequestrate about 1 natifida, China and Korea cultivated 85% and 30% of the total world
billion tons of carbon annually. Muraoka (2004) reported that in Ja- production, respectively (FAO, 2012a). While Porphyra sp. was pro-
pan about 32000 tons of carbon can be annually absorbed by mass- duced primarily in Japan, other red algae were cultivated mainly in
cultivated seaweeds such as Laminaria, Undaria, Hizikia, Gelidium, Indonesia and the Philippines (Chung et al., 2011; FAO, 2012a). Due
and Porphyra spp. to their farming technology and experience built up over decades,
the East Asian countries would have an important role in increas-
ing the amount of globally produced macroalgae for biorefinery
3. Mass-cultivation of macroalgae
feedstock.
Macroalgae are mass-cultivated based on current farming tech-
nology. Although only a dozen of algae are commercially cultivated 4. Chemical compositions of macroalgae
among over 20000 species reported worldwide (Critchley et al.,
1998), the amount of macroalgae mass-cultivated in the world Since the biorefinery process and performance are affected by
has continuously increased over the last 10 years at an average of chemical compositions of feedstocks, researchers need to under-
10% (Fig. 1) (FAO, 2012a). Brown and red algae were cultivated stand what types and contents of chemical resources are available
more than green algae. It is noted that the red algae production in macroalgal biomass. For instance, information on the content of
dramatically increased and the brown algae production attained six- and five-carbon sugars is a prerequisite to determine an

Fig. 1. World production of farmed macroalgae from 2001 to 2010. Adjusted from FAO (2012a).
 K.A Jung et al. / Bioresource Technology 135 (2013) 182–190 185

Table 2 ification of lignin-originated inhibiting compounds (Meinita et al.,

World production of macroalgae, microalgae, energy crops, and lignocellulosic 2012a). Compared to the terrestrial biomass, macroalgae have the
biomass.
high contents of water (70–90% fresh wt.) and minerals such as ali-
Species Group (or phylum) Production % of total kali metals (10–50% dry wt.) (Ross et al., 2008). In contrast, they
Macroalgaea had the low contents of protein (7–15% dry wt.) and lipids (1–5%
Laminaria japonica Brown algae 5,146,883 32.61 dry wt.) (Jensen, 1993), whereas most microalgae have the high
Eucheuma spp. Red algae 3,489,388 22.11 content of protein (40–60% dry wt.) and intermediate lipids (10–
Kappaphycus alvarezii Red algae 1,875,277 11.88
Undaria pinnatifida Brown algae 1,537,339 9.74
20% dry wt.) (Becker, 1994).
Gracilaria verrucosab Red algae 1,152,108 7.30
Porphyra spp. Red algae 1,072,350 6.79 4.2. Carbohydrate composition of macroalgae
Gracilaria spp.b Red algae 565,366 3.58
Porphyra tenera Red algae 564,234 3.57
Carbohydrate compounds are abundant in macroalgae. The car-
Eucheuma denticulatum Red algae 258,612 1.64
Sargassum fusiforme Brown algae 78,210 0.50 bohydrate contents of green, red, and brown algae are 25–50%, 30–
Phaeophyceae Brown algae 21,747 0.14 60%, and 30–50% dry wt., respectively (Becker, 1994; Jensen, 1993;
Enteromorpha clathrata Green algae 11,150 0.07 Ross et al., 2008). Since macroalgae have a variety of carbohydrates
Monostroma nitidum Green algae 4,531 0.03 depending on their species, information on their carbohydrate
Caulerpa spp. Green algae 4,309 0.03
compositions is necessary to effectively utilize them as carbon
Codium fragile Green algae 1,394 0.01
Gelidium amansii Red algae 1,200 0.01 sources for bioenergy and as chemical sources for biomaterial
Total 15,784,098 100.00 and bioproducts.
Microalgaec
Arthrospira sp. Cyanophyta 3000 4.2.1. Green algae
Chlorella sp. Chlorophyta 2000 Green algae have polysaccharides in the form of starch (i.e., a-1,
Dunaliella salina Chlorophyta 1200
4-glucan) and lipids but their proportions are small (1–4% for
Haematococcus pluvialis Chlorophyta 3000
starch; and 0–6% for lipids) (Bruton et al., 2009). Ulva and Entero-
Energy cropsd
morpha sp. have water-soluble ulvan and insoluble cellulose (38–
Corn 844,405,181
Palm oil 45,097,422 52% dry wt.) in their cell walls (Lahaye and Robic, 2007). Ulvan, a
Rapeseed 59,071,197 distintive feature of green algae, is composed mainly of D-glucu-
Sugar cane 1,685,444,531 ronic acid, D-xylose, L-rhamnose, and sulfate (Lobban and Wynne,
Soybean 261,578,498 1981).
Lignocellulosic biomasse
Corn stover 12.6 4.2.2. Red algae
Switchgrass 9.0
Red algae are different from green and brown algae in the syn-
a
Estimated in wet metric ton and adjusted from FAO (2012a). thesis and metabolism machinery of carbohydrates. The unique
b
Including macroalgae cultured in brackish water. carbohydrates for red algae are floridean starch and floridoside,
c
Estimated in dry metric ton and adjusted from Hejazi and Wijffels (2004),
which are similar to general starch, but green and brown algae
Lorenz and Cysewski (2000), Pulz and Gross (2004), Ratledge (2004).
d
Estimated in ton and adjusted from FAO (2012b). do not have those carbohydrates (Sze, 1993; Yu et al., 2002). Flor-
e
Estimated in dry metric ton a hectare and adjusted from Lemus et al. (2002), idean starch is an a-1,4-glucosidic linked glucose homopolymer
Shinners and Binversie (2007). and accounts for up to 80% of the cell volume (Yu et al., 2002). Be-
cause floridean starch has the property to weaken gel strength, it is
removed as an impurity in the production of agar and carrageenan
appropriate fermentation microorganism and a process for bioeth- by using thermophilic a-amylase treatment (Yu et al., 2002).
anol production. Also, that kind of information would be helpful to The major polysaccharide constituents of red algae are galac-
understand what biomaterials can be readily and economically tans such as carrageenan (up to 75% dry wt.) and agar (up to
obtained or converted through biorefinery. 52%), which are the most commercially important polysaccharides
for red algae (Lobban and Wynne, 1981; McHugh, 2003). Carra-
4.1. Difference between terrestrial- and marine-biomass geenan consists of repeating D-galactose unit and anhydrogalac-
tose, which may or may not be sulfated (Lobban and Wynne,
Macroalgae are significantly different from terrestrial plants in 1981). Carrageenans can be readily obtained by extracting red sea-
terms of their chemical composition, as well as physiological and weeds or dissolving them into an aqueous solution (McHugh,
morphological features. Table 3 shows the type of principal carbo- 2003). Purified carrageenans are generally used for forming thick
hydrates included in marine macroalgae, microalgae, and lignocel- solution or gel (Lobban and Wynne, 1981). Commercial carrageen-
lulosic biomass. Macroalgae have manan, ulvan, carrageenan, agar, ans have been originated from Chondrus, Gigartina, and Eucheuma
laminarin, mannitoal, alginate, and fucoidin (Lobban and Wynne, sp. (Vera et al., 2011). As another major constituent, agar is made
1981), which are not included in microalgae and lignocellulosic up of alternating b-D-galactose and a-L-galactose with scarce sulf-
biomass. Thus, the monosaccharides hydrolyzed from these carbo- ations (Lobban and Wynne, 1981). If these galactose compounds
hydrates and/or whole polysaccharides should be targeted to de- are highly sulfated, that agar cannot make a gel structure (Lobban
velop macroalgae-based biorefinery technology. Like terrestrial and Wynne, 1981). Agars are utilized as algal hydrocolloids in food,
biomass, macroalgae except green algae do not have the high con- pharmaceutical, and biological industries (Bixler and Porse, 2011).
tent of starch and oil (Roesijadi et al., 2010), which is differentiated Agar is produced from Gracilaria, Gelidium, and Pterocladia sp. by
from microalgae (Brown, 1991). It should be noted that macroalgae treating them with acid/heat or alkali (McHugh, 2003).
almost do not include lignin because macroalgae do not need to
stand rigidly in the water (Wegeberg and Felby, 2010): lignin is a 4.2.3. Brown algae
constituent needed for the rigidity of terrestrial plants. Thus, the A major polysaccharide of brown algae is alginic acid (i.e., algi-
cell wall of macroalgae is structurally flexible. Due to their low lig- nate), which accounts for up to 40% dry wt. as a principal material
nin content, macroalgae can provide many benefits for biorefinery: of the cell wall (Draget et al., 2005). Alginate is composed of three
no need for complex processes such as lignin removals and detox- different uronic acids: mannuronic acid blocks, guluronic acid
186 K.A Jung et al. / Bioresource Technology 135 (2013) 182–190
Table 3
Carbohydrate composition of macroalgae, microalgae, and lignocellulosic biomass.
Macroalgaea
Green algae Red algae
Polysaccharide Polysaccharide
Mannan Carrageenan
Ulvan Agar
Starch Cellulose
Cellulose Lignin
Monosaccharide Monosaccharide
Glucose Glucose
Mannose Galactose
Rhamnose Agarose
Xylose
Uronic acid
Glucuronic acid
a
Adjusted from Jang et al. (2012), Roesijadi et al. (2010), Turvey and Christison (1967), Wegeberg and Felby (2010).
b
Adjusted from Brown (1991).
blocks, and alternative blocks of mannuronic and guluronic units
(Lobban and Wynne, 1981). Alginate tends to become gel due to
its high affinity for divalent cations such as calcium, strontium,
barium, and magnesium (Draget et al., 2005). Various brown algae
tend to have their respective alginate structure and proportions of
mannuronic and guluronic acids in alginate (Lobban and Wynne,
1981). Alginates have been used mostly in the textile (50%) and
food (30%) industries (McHugh, 2003).
As a unique polysaccharide for brown algae, they have lami-
narin (i.e., b-1, 3-glucans) (Adams et al., 2011). This polysaccharide
accounts for up to 35% dry wt. of brown algae (Mautner, 1954).
Their laminarin contents vary depending on seasons and water
depth, which affect nutrient conditions for growth of macroalgae
(Adams et al., 2011; Mautner, 1954). Brown algae also have fucoi-
dan, which is a sulphated complex polysaccharide consisting of fu-
cose and a linear backbone of sulfate monosaccharides (Holtkamp
et al., 2009). Fucus vesiculosus is used to produce relatively pure
fucoidan (Duarte et al., 2001). Fucoidan has been extensively stud-
ied due to its potential in pharmaceutical applications (Li et al.,
2008). In addition, brown algae have glucose and glyoxylic acid
in small amounts (Mautner, 1954).
5. Biomaterials and bioproducts from macroalgae
At present, macroalgae are utilized for human food, algal hydro-
colloids, therapeutic materials, fertilizer, and animal feed. Among
macroalgae-related industries, the food industry is the largest,
accounting for $5 billion worldwide on an annual basis, which is
83–90% of the total seaweed industry (Roesijadi et al., 2010). Sea-
weed food markets are mainly in the East Asian countries
(McHugh, 2003). Macroalgae themselves are uptaken as food
ingredients and converted to other products. For instance, agar is
used as food ingredients, and carrageenan as food additives for
dairy, meat, water-based, and pet foods (McHugh, 2003).
Besides food uses, macroalgae are utilized to produce diverse
biomaterials and bioproducts in various industries. One of the prin-
cipal materials is algal hydrocolloids, which accounts for $132–240
million worldwide on an annual basis, and their key components
are agar, alginate, and carrageenan (Roesijadi et al., 2010). Annual
world sales amount of seaweed hydrocolloids has increased by 6%
from 1999 to 2009, and its sales amounts have almost doubled in
that period (Bixler and Porse, 2011). Since macroalgae have respec-
tive characteristics for gel-forming and water-dissolving, various
macroalgae are used for industrial uses (McHugh, 2003). Agar is
Microalgaeb Lignocellulosic biomass
Brown algae
Polysaccharide Starch Cellulose
Laminarin Total carbohydrate Hemicellulose
Mannitol Arabinose Lignin
Alginate Fucose
Fucoidin Galactose
Cellulose Glucose
Monosaccharide Mannose
Glucose Rhamnose
Galactose Ribose
Fucose Xylose
Xylose
Uronic acid
Mannuronic acid
Guluronic acid
Glucuronic acid
used as a laxative in the pharmaceutical industry and as a chemical
to test the presence of bacteria (McHugh, 2003). Carrageenan is
utilized as an essential ingredient in toothpaste (McHugh, 2003),
even though this market is not large. Alginate is used in only
non-food industries such as textile printing, immobilized biocata-
lyst, pharmaceutical tablet disintegrant, medical fiber, welding
rod, and paper industries (Bixler and Porse, 2011; Kraan, 2010;
Roesijadi et al., 2010).
Several polysaccharides and oligosaccharides derived from
macroalgae are used for therapeutic applications due to their bio-
activity (Jiao et al., 2011; Li et al., 2008; Vera et al., 2011). For in-
stance, the saccharides are fucodidan and fucan from brown
algae; sulfated galactan and ulvan-like sulfated polysaccharide
from green algae; and sulfated polysaccharides such as carra-
geenan and galactan from red algae. These substances were recog-
nized to have antithrombotic, antiviral, immuno-inflammatory,
antilipidemic, and antioxidant activities (Jiao et al., 2011). Vera
et al. (2011) reported that ulvan, alginate, fucan, laminarin, and
carrageenan and their derived oligosaccharides could increase
the immune ability of terrestrial plants against pathogens by acti-
vating signal pathways in the plants.
In addition to the aforementioned biomaterials, many efforts
are being taken to develop the precursors of biomaterial building
blocks and fermentation products from macroalgae. The precursors
are derived as main products and byproducts from biorefinery pro-
cesses using physiochemical treatment and microbial fermentation
(Chang et al., 2010). Kraan (2010) and Chang et al. (2010) have re-
ported some possible fermentation products and high-value
byproducts from macroalgae. The yield and the selectivity of
fermentation products depend largely on reaction conditions
(Gunaseelan, 1997; Veeken et al., 2000), which are determined
by taking into account economic viability of building block prod-
ucts. Volatile fatty acids (VFAs) such as acetic, propionic, lactic,
and butyric acids can be produced from macroalgae by using
anaerobic digestion. Chang et al. (2010) have suggested a novel
platform using these VFAs to produce chemicals and fuels. In
previous studies, anaerobic digestion has been applied to generate
lactic acid as well as methane from macroalgal biomass (Gupta
et al., 2011). Due to the low lignin content of macroalgae, valuable
VFAs could be efficiently produced by anaerobic digestion.
Other bioproducts derived from macroalgae are amino acids.
Lammens et al. (2012) have evaluated the availability of protein-
derived amino acids from byproducts of macroalgal biorefinery
because glutamic acid can be a source of valuable bio-based
chemicals, i.e., as N-methylpyrrolidone, N-vinylpyrrolidone, and
 K.A Jung et al. / Bioresource Technology 135 (2013) 182–190
acrylonitrile. Although macroalgae have a wide range of protein
contents depending on their species, the average protein propor-
tion (20%) of macroalgae is higher than for other crop residues such
as corn stover, wheat straw, and sugarcane leafs (Lammens et al.,
2012).
6. Bioenergy from macroalgae
6.1. Biogas
Anaerobic digestion can be applied to produce biogas, particu-
larly methane, from various macroalgae (Gupta et al., 2011).
Gunaseelan (1997) has compared digestion characteristics of sev-
eral land- and water-based biomass. According to this work, the
macroalgae (0.31–0.48 m3 CH4 kg 1 volatile solid) exhibited higher
methane production rates than the land-based biomass (0.34–
0.42 m3 CH4 kg 1 for grass, and 0.32–0.42 m3 CH4 kg 1 for wood),
and kelp was only biomass that did not need pretreatment, be-
cause of no existence of lignin. It should be mentioned that the
anaerobic digestion performance is affected by the species and
the composition of macroalgae, depending on seasons, geography,
and so on (Costa et al., 2012). Methane production rate can be im-
proved by co-digesting macroalgae (Ulva sp.) with manure and
waste activated sludge (Costa et al., 2012). While biogas produc-
tion from macroalgae is more technically-viable than for other
fuels, that biogas production is not yet economically-feasible due
to the high cost of macroalgae feedstocks, which needs to be re-
duced by 75% of the present level (Roesijadi et al., 2010).
6.2. Bioethanol
Bioethanol can be fermented from all kinds of macroalgae by
converting their polysaccharides to simple sugars and by employ-
ing appropriate microorganisms. Since macroalgae have various
carbohydrates such as starch, cellulose, laminarin, mannitol, and
agar, carbohydrate conversion to sugars and the choice of appro-
priate microorganisms are pivotal for successful bioethanol fer-
mentation; however, those researches are now at the early stage.
Brown algae are a principal feedstock for bioethanol production
because they have high carbohydrate contents and can be readily
mass-cultivated with current farming technology. Among their
carbohydrates, mannitol and laminaran (for Laminaria sp., 25%
and 30% dry wt., respectively (Horn et al., 2000a)) are the most
readily utilized by certain microorganisms (Horn et al., 2000a,b).
Horn et al. (2000a,b) have shown that mannitol and laminaran ex-
tracts from L. hyperborea can be fermented to produce bioethanol.
They have also examined the ethanol fermentation performance
for brown algae extracts by applying various bacteria and yeasts.
Bacterium Zymobacter palmae converted only mannitol to ethanol
due to its lack of laminarase activity, whereas two yeast strains
Kluyveromyces marxianus and Pacchysolen tannophilus fermented
laminaran but not manitol. Only yeast Pichia angophorae has simul-
taneously utilized both mannitol and laminaran to produce etha-
nol. This yeast achieved the highest yield of 0.43 g ethanol
g substrate 1.
Many attempts have been taken to utilize various carbohy-
drates in macroalgal biomass by using physicochemical hydrolysis,
as in the saccharification of lignocellulosic biomass. Dilute-acid
hydrolysis is a typical physicochemical method to treat raw macro-
algal biomass with 0.3–0.9 N H2SO4 at 100–140 °C (Meinita et al.,
2012b; Park et al., 2012). In the acid hydrolysis, reaction parame-
ters such as acid concentration and hydrolysis time affect the total
yields of reducing sugars and ethanol production: optimum condi-
tions need to be determined to maximize concentrations of mono-
sugars and ethanol (Meinita et al., 2012b).
187
Besides chemical hydrolysis, enzymatic hydrolysis is another
general and mild approach to saccharify macroalgal biomass. How-
ever, its procedures for high ethanol productivity have been under-
developed because the enzyme activity is specific to the type of
polysaccharides while even a single species of macroalgae consists
of more than one type of polysaccharide complexes (Choi et al.,
2009). Many studies have carried out macroalgae hydrolyses by
using cellulase and cellobiase as for lignocellulosic biomass (Ge
et al., 2011; Yanagisawa et al., 2011) as well as commercial enzyme
complexes (Choi et al., 2009). A few studies have applied macroal-
gae-specific enzymes such as laminarinase and agarase to sacchar-
ify macroalgae; however, these enzymes showed low hydrolysis
efficiency. Thus, their treatment needs additional pretreatment or
multi-enzyme complexes (Adams et al., 2011).
Chemical and enzymatic hydrolyses have been combined to
more effectively obtain mono-sugars from macroalgae (Adams
et al., 2011; Ge et al., 2011; Jang et al., 2012). A thermal acid hydro-
lysis and an enzyme treatment were applied to Saccharina sp. and
Laminaria sp. (brown algae) to recover potentially fermentable
reducing sugars such as D-mannuronate, L-guluronate, D-glucose,
L-fucose, D-galactose, D-xylose, and L-glucuronate (Ge et al., 2011;
Jang et al., 2012). Gelidium amansii and Kappaphycus alvarezii (red
algae) were more readily fermented than brown algae by using
chemical and enzymatic hydrolyses (Park et al., 2012).
More elaborate research has been performed to investigate the
optimal pretreatment with respect to the carbohydrate character-
istics of macroalgae species. Yanagisawa et al. (2011) have sug-
gested tailor-made saccharification methods to increase
bioethanol yields for green, red, and brown algae. For G. elegans
(red alga), a combined saccharification process consisting of acid
and enzyme hydrolyses was used to convert the original polysac-
charides (i.e., galactan and glucan) to galactose and glucose
(Lobban and Wynne, 1981). This red algae-specific saccharification
led to an increase in the ethanol concentration (5.5% vol., or 0.44 g
ethanol g glucose 1), which is higher than the economically feasi-
ble concentration (4–5%) for distillation. For Ulva pertusa and Alaria
crassifolia (green and brown algae, respectively), an enzymatic
hydrolysis was enough to saccharify because glucan, a single
polysaccharide in the two seaweeds, can be hydrolyzed to glucose
by the enzyme (Yanagisawa et al., 2011).
Pretreatment for saccharification can inhibit microbial fermen-
tation, and thus detoxicification research is required to effectively
utilize macroalgal biomass. Heat and pH pretreatments have been
found to rather lower bioethanol yields for a brown alga (Saccha-
rina latissima) (Adams et al., 2009). Although heat treatment is
used to solubilize laminaran, that heat can generate inhibitory
compounds. Also, acid treatment has caused the ethanol yield for
S. latissima to decrease by 40–47%, probably due to cell disruption
and salt inhibition (Adams et al., 2009). Representative inhibitory
compounds generated in the acid hydrolysis condition (even in di-
lute acid solutions) are furfural, 5-hydroxymethylfurfural (HMF),
levulinic acid, and caffeic acid (Meinita et al., 2012a). These com-
pounds are derived primarily from xylose and galactose in macro-
algal biomass. The inhibitors can be detoxified by applying lime
and activated charcoal treatments (Meinita et al., 2012a). Another
inhibition on microbial fermentation could be derived from the
metals in macroalgae, which could be released to the broth during
pretreatment. This is because the metal contents (0.5–11% wt.) of
macroalgae are higher than for terrestrial biomass (1–1.5% wt.)
(Lee and Lee, 2012; Ross et al., 2008).
6.3. Biobutanol
Biobutanol can be produced from macroalgae through the ace-
tone-butanol (AB) fermentation using solventogenic anaerobic
bacteria such as Clostridium sp. (Huesemann et al., 2012).
188 K.A Jung et al. / Bioresource Technology 135 (2013) 182–190
Table 4
Microorganisms and enzymes that can degrade macroalgal polysaccharides.
Species
Green algae
Ulvan
Gram-negative marine bacterium (ulvan lyase, endo-)
Red algae
Agar
Alteromonas sp. C-1(b-agarases, extra-)
Bacillus sp. MK03 (b-agarases, extra-)
Pseudomonas atlantica (b-agarases I, II, endo-)
Thalassomonas sp. JAMB-A33 (a-agarases, intra-)
Vibrio sp. JT0107 (b-agarases, extra-)
Carrageenan
Alteromonas fortis
Delesseria sanguinea
Pseudoalteromonas carrageenovora
Zobellia galactanivorans
Brown algae
Alginate
Alginovibrio aquatilis (alginate lyases, endo-)
Alteromonas sp. strain H-4 (alginate lyase, exo-)
Asteromyces cruciatus (alginate lyases, endo-)
Dendryphiella arenaria (alginate lyase)
Marine bacterium ATCC 433367 (alginate lyases, exo-/endo-)
Pseudoalteromonas elyakovii IAM 14594 (alginate lyase, exo-)
Sphingomonas Strain A1 (alginate lyase, exo-)
Vibrio sp. (alginate lyase)
Fucoidan
Pecten maximus (intra-/extra- cellular)
Pseudomonas atlantica (fucoidanase)
Pseudoalteromonas atrea KMM3296 (fucoidanase)
Pseudoalteromonas citrea (fucoidanase)
Vibrio sp. (fucoidanase)
Laminarin
Aplysia juliana
Chaetomium indicum (laminarinase)
Pseudoaltermonas issachenkonii KMM 3549 (laminarinase; fucoidan
hydrolase; alginase)
Vibrio sp. 3 strains (laminarinase)
Adjusted from Alderkamp et al. (2007), Holtkamp et al. (2009), Reddy et al. (2008).
Clostridium sp. is capable of producing butanol, acetone, ethanol,
and organic acids from various carbon substrates. However, this
bacterium did not effectively utilize some glucose-based polysac-
charides (such as mannitol from brown algae), which caused
slow reaction rate and low productivity of organic acids and total
solvents (Huesemann et al., 2012).
6.4. Advanced technology for macroalgal biofuels
To commercialize macroalgae-based fuels, a priority needs to be
put on identifying microorganism that can metabolize major but
unique macroalgal carbohydrates. Some macroalgae-specific car-
bohydrates such as alginate and ulvan are not readily metabolized
by commercially applied fermenting microorganisms such as Sac-
charomyces cerevisiae (Wegeberg and Felby, 2010). To overcome
this drawback, some researchers have developed macroalgae-
specific enzymes to hydrolyze macroalgal carbohydrates (Jang
et al., 2012). Table 4 shows microorganisms and enzymes that
can degrade various macroalgal carbohydrates. Most of the micro-
organisms were originated from marine flora and fauna. Their
enzymatic functions on macroalgae have been well reviewed in
many studies (Erasmus et al., 1997).
Once those kinds of microorganisms and enzymes have been
identified and developed, they can be applied to the Simultaneous
Saccharification and Fermentation (SSF) system (Jang et al., 2012).
This SSF system has many advantages: low contamination, low ini-
tial osmotic stress of fermenting microorganisms, and high energy-
efficiency. It should be noted however, that applying various
microorganisms to a fermentation condition as in the SSF system
could inhibit enzyme activity and extracellular enzyme secretion
(Alderkamp et al., 2007; Holtkamp et al., 2009; Reddy et al.,
2008). Also, various and complex carbohydrates of macroalgae
can lead to low yield of biofuels in the SSF system (Jang et al.,
2012).
Recently, advanced biotechnology has been applied to resolve
aforementioned challenges in macroalgae-based biorefinery: so-
called Consolidated BioProcessing (CBP) (Kim et al., 2012; Sánchez
and Cardona, 2008; Wargacki et al., 2012). This CBP consists of a
diverse range of genetic transformation and metabolic engineering,
which are expected to provide a breakthrough in the development
of biomass-based bioenergy technology in the next 10 years. Kim
et al. (2012) have reported that S. cerevisiae was engineered to ex-
press heterologous sugar transporters and thereby remove glucose
repression under the mixed sugars condition. Also, secondary
sugar transporters and some metabolic genes were expressed to
bypass the regulatory mechanisms of the S. cerevisiae and thus
co-ferment mixed mono-sugars simultaneously. Wargacki et al.
(2012) have shown that biofuel was produced directly from algi-
nate by engineering secretable alginate lyases from Vibrio splendi-
dus and functional alginate transport and metabolic systems into
Escherichia coli. This approach has achieved 4.7% vol. (or
0.281% wt.) of ethanol yield, which surpasses the ideal ethanol
yield (0.254% wt.) for macroalgae.
Besides improving microbial abilities molecular bioengineering
is required to modify the physicochemical properties of macroal-
gae and make them readily utilized for biofuel production (Renn,
1997). For instance, metabolic engineering could be applied to sea-
weeds in order to alter their biosynthetic pathways and thereby
improve their polysaccharide composition and productivity (Renn,
1997). This approach could significantly improve seaweed produc-
tivity and contribute to the success of marine biorefinery. Although
meaningful outcomes have yet been reported due to difficulties in
the genetic manipulation of macroalgae, many efforts have been
taken to develop molecular biotechnology on macroalgae; for in-
stance, gene mapping, introduction of foreign genes into seaweed
cells, and promoter selection (John et al., 2011; Qin et al., 2004;
Renn, 1997).
7. Conclusions
Macroalgae have the high potential as feedstocks for biorefinery
to produce biomaterials and bioenergy. Macroalgae-based biore-
finery is expected to dramatically develop in the near future, due
to many environmental and economic benefits. For biorefinery
feedstock supply, macroalgae can be mass-cultivated with cur-
rently available farming technology. However, due to various mac-
roalgal carbohydrates, more efforts should be taken to effectively
and efficiently utilize macroalgae: identification of new microor-
ganisms, technology development for genetic transformation and
metabolic engineering, and process development and optimization
for yield enhancement. Once these technologies are established,
macroalgae could significantly contribute to low-carbon economy
as a most promising biomass.
Acknowledgements
This research was supported by Basic Science Research Program
through the National Research Foundation of Korea (NRF) funded
by the Ministry of Education, Science and Technology (Grant num-
bers 2011-0001108 and 2011-0008373), the Advanced Biomass
R&D Center (ABC) of Korea Grant funded by the Ministry of Educa-
tion, Science and Technology (ABC-2011-0028387), Marine
 K.A Jung et al. / Bioresource Technology 135 (2013) 182–190 189

Biotechnology Program funded by Ministry of Land, Transport and Hoek, C.V.D., Mann, D., Jahns, H.M., 1995. Algae: An Introduction to Phycology.
Cambridge University Press.
Maritime Affairs of Korean Government, Korea and the Manpower
Holtkamp, A., Kelly, S., Ulber, R., Lang, S., 2009. Fucoidans and fucoidanases—focus
Development Program for Marine Energy funded by Ministry of on techniques for molecular structure elucidation and modification of marine
Land, Transportation and Maritime Affairs (MLTM) of Korean gov- polysaccharides. Appl. Microbiol. Biotechnol. 82, 1–11.
ernment, by WCU (World Class University) program through the Horn, S.J., Aasen, I.M., Østgaard, K., 2000a. Ethanol production from seaweed extract.
J. Ind. Microbiol. Biotechnol. 25, 249–254.
National Research Foundation of Korea funded by the Ministry of Horn, S.J., Aasen, I.M., Østgaard, K., 2000b. Production of ethanol from mannitol by
Education, Science and Technology (R31-30005), and by 2011 Re- Zymobacter palmae. J. Ind. Microbiol. Biotechnol. 24, 51–57.
search Grant from Kangwon National University. Huesemann, M.H., Kuo, L.-J., Urquhart, L., Gill, G.A., Roesijadi, G., 2012. Acetone-
butanol fermentation of marine macroalgae. Bioresour. Technol. 108, 305–309.
IEA (International Energy Agency), 2009. IEA Bioenergy Task 42 Biorefinery.
References Available from: <http://www.iea-bioenergy.task42-biorefineries.com/>.
Jang, J.-S., Cho, Y., Jeong, G.-T., Kim, S.-K., 2012. Optimization of saccharification and
ethanol production by simultaneous saccharification and fermentation (SSF)
Adams, J., Gallagher, J., Donnison, I., 2009. Fermentation study on Saccharina
from seaweed, Saccharina japonica. Bioprocess Biosyst. Eng. 35, 11–18.
latissima for bioethanol production considering variable pre-treatments. J. Appl.
Jensen, A., 1993. Present and future needs for algae and algal products.
Phycol. 21, 569–574.
Hydrobiologia 260–261, 15–23.
Adams, J.M.M., Toop, T.A., Donnison, I.S., Gallagher, J.A., 2011. Seasonal variation in
Jiao, G., Yu, G., Zhang, J., Ewart, H., 2011. Chemical structures and bioactivities of
Laminaria digitata and its impact on biochemical conversion routes to biofuels.
sulfated polysaccharides from marine algae. Mar. Drugs 9, 196–223.
Bioresour. Technol. 102, 9976–9984.
John, R.P., Anisha, G.S., Nampoothiri, K.M., Pandey, A., 2011. Micro and macroalgal
Alderkamp, A.C., Van Rijssel, M., Bolhuis, H., 2007. Characterization of marine
biomass: a renewable source for bioethanol. Bioresour. Technol. 102, 186–193.
bacteria and the activity of their enzyme systems involved in degradation of the
Kim, S.R., Ha, S.-J., Wei, N., Oh, E.J., Jin, Y.-S., 2012. Simultaneous co-fermentation of
algal storage glucan laminarin. FEMS Microbiol. Ecol. 59, 108–117.
mixed sugars: a promising strategy for producing cellulosic ethanol. Trends
Atabani, A.E., Silitonga, A.S., Badruddin, I.A., Mahlia, T.M.I., Masjuki, H.H., Mekhilef,
Biotechnol. 30, 274–282.
S., 2012. A comprehensive review on biodiesel as an alternative energy resource
Kraan, S., 2010. Mass-cultivation of carbohydrate rich macroalgae, a possible
and its characteristics. Renew. Sust. Energy Rev. 16, 2070–2093.
solution for sustainable biofuel production. Mitig. Adapt. Strat. Gl.. http://
Becker, E.W., 1994. Microalgae: Biotechnology and Microbiology. Cambridge
dx.doi.org/10.1007/s11027-010-9275-5.
University Press.
Lahaye, M., Robic, A., 2007. Structure and functional properties of ulvan, a
Bixler, H.J., Porse, H., 2011. A decade of change in the seaweed hydrocolloids
polysaccharide from green seaweeds. Biomacromolecules 8, 1765–1774.
industry. J. Appl. Phycol. 23, 321–335.
Lammens, T.M., Franssen, M.C.R., Scott, E.L., Sanders, J.P.M., 2012. Availability of
Brown, M.R., 1991. The amino-acid and sugar composition of 16 species of
protein-derived amino acids as feedstock for the production of bio-based
microalgae used in mariculture. J. Exp. Mar. Biol. Ecol. 145, 79–99.
chemicals. Biomass Bioenerg. 44, 168–181.
Bruton, T., Lyons, H., Lerat, Y., Stanley, M., Rasmussen, M.B., 2009. A Review of the
Lee, S.-M., Lee, J.-H., 2012. Ethanol production from Laminaria japonica: effect of
Potential of Marine Algae as a Source of Biofuel in Ireland. Available from:
metal ion adsorption. J. Ind. Eng. Chem.. http://dx.doi.org/10.1016/
<http://www.seambiotic.com/uploads/algae%20report%2004%202009.pdf>.
j.jiec.2012.03.002.
Chang, H., Kim, N.-J., Kang, J., Jeong, C., 2010. Biomass-derived volatile fatty acid
Lemus, R., Brummer, E.C., Moore, K.J., Molstad, N.E., Burras, C.L., Barker, M.F., 2002.
platform for fuels and chemicals. Biotechnol. Bioprocess Eng. 15, 1–10.
Biomass yield and quality of 20 switchgrass populations in southern Iowa, USA.
Choi, D., Sim, H.S., Piao, Y.L., Ying, W., Cho, H., 2009. Sugar production from raw
Biomass Bioenerg. 23, 433–442.
seaweed using the enzyme method. J. Ind. Eng. Chem. 15, 12–15.
Lewis, L.A., McCourt, R.M., 2004. Green algae and the origin of land plants. Am. J.
Chung, I., Beardall, J., Mehta, S., Sahoo, D., Stojkovic, S., 2011. Using marine
Bot. 91, 1535–1556.
macroalgae for carbon sequestration: a critical appraisal. J. Appl. Phycol. 23,
Li, B., Lu, F., Wei, X., Zhao, R., 2008. Fucoidan: structure and bioactivity. Molecules
877–886.
13, 1671–1695.
Costa, J.C., Gonçalves, P.R., Nobre, A., Alves, M.M., 2012. Biomethanation potential of
Lobban, C.S., Harrison, P.J., Duncan, M.J., 1985. The Physiological Ecological of
macroalgae Ulva spp. and Gracilaria spp. and in co-digestion with waste
Seaweed. Cambridge University Press.
activated sludge. Bioresour. Technol. 114, 320–326.
Lobban, C.S., Wynne, M.J., 1981. The Biology of seaweeds, firstst ed. Blackwell
Critchley, A.T., Ohno, M., Largo, D.B., Gillespie, R.D., 1998. Seaweed Resources of the
Scientific Publications.
World. Japan International Cooperation Agency.
Lorenz, R.T., Cysewski, G.R., 2000. Commercial potential for Haematococcus
Dominguez-Faus, R., Powers, S.E., Burken, J.G., Alvarez, P.J., 2009. The water
microalgae as a natural source of astaxanthin. Trends Biotechnol. 18, 160–167.
footprint of biofuels: a drink or drive issue? Environ. Sci. Technol. 43, 3005–
Mautner, H., 1954. The chemistry of brown algae. Econ. Bot. 8, 174–192.
3010.
McHugh, D.J., 2003. A Guide to the Seaweed Industry. Available from: <http://
Draget, K.I., Smidsrød, O., Skjåk-Bræk, G., 2005. Alginates from algae. In:
www.fao.org/docrep/006/y4765e/y4765e00.htm#Contents>.
Biopolymers Online. Wiley-VCH Verlag GmbH & Co. KGaA.
Meinita, M., Hong, Y.-K., Jeong, G.-T., 2012a. Detoxification of acidic catalyzed hydro-
Duarte, M.E.R., Cardoso, M.A., Noseda, M.D., Cerezo, A.S., 2001. Structural studies on
lysate of Kappaphycus alvarezii (cottonii). Bioprocess Biosyst. Eng. 35, 93–98.
fucoidans from the brown seaweed Sargassum stenophyllum. Carbohydr. Res.
Meinita, M., Kang, J.-Y., Jeong, G.-T., Koo, H., Park, S., Hong, Y.-K., 2012b. Bioethanol
333, 281–293.
production from the acid hydrolysate of the carrageenophyte Kappaphycus
Erasmus, J.H., Cook, P.A., Coyne, V.E., 1997. The role of bacteria in the digestion of
alvarezii (cottonii). J. Appl. Phycol. 24, 857–862.
seaweed by the abalone Haliotis midae. Aquaculture 155, 377–386.
Muraoka, D., 2004. Seaweed resources as a source of carbon fixation. Bull. Fish. Res.
FAO (Food and Agriculture Organization of the United Nations), 2012a. 2010 Fishery
Agen. Suppl. 1, 59–63.
and Aquaculture Statistics. Available from: <ftp://ftp.fao.org/FI/CDrom/
Park, J.-H., Hong, J.-Y., Jang, H.C., Oh, S.G., Kim, S.-H., Yoon, J.-J., Kim, Y.J., 2012. Use of
CD_yearbook_2010/index.htm>.
Gelidium amansii as a promising resource for bioethanol: a practical approach
FAO (Food and Agriculture Organization of the United Nations), 2012b. FAO
for continuous dilute-acid hydrolysis and fermentation. Bioresour. Technol.
Statistical Yearbook 2012: World Food and Agriculture. Available from: <http://
108, 83–88.
faostat.fao.org/>.
Pulz, O., Gross, W., 2004. Valuable products from biotechnology of microalgae. Appl.
FAO (Food and Agriculture Organization of the United Nations), 1997. Renewable
Microbiol. Biotechnol. 65, 635–648.
Biological Systems for Alternative Sustainable Energy Production (FAO
Qin, S., Jiang, P., Tseng, C.K., 2004. Molecular biotechnology of marine algae in China.
Agricultural Services Bulletin-128). Available from: <http://www.fao.org/
Hydrobiologia 512, 21–26.
docrep/w7241e/w7241e00.htm#Contents>.
Ragauskas, A.J., Williams, C.K., Davison, B.H., Britovsek, G., Cairney, J., Eckert, C.A.,
Fargione, J., Hill, J., Tilman, D., Polasky, S., Hawthorne, P., 2008. Land clearing and the
Frederick, W.J., Hallett, J.P., Leak, D.J., Liotta, C.L., Mielenz, J.R., Murphy, R.,
biofuel carbon debt. Science 319, 1235–1238.
Templer, R., Tschaplinski, T., 2006. The path forward for biofuels and
Gao, K., McKinley, K., 1994. Use of macroalgae for marine biomass production and
biomaterials. Science 311, 484–489.
CO2 remediation: a review. J. Appl. Phycol. 6, 45–60.
Ratledge, C., 2004. Fatty acid biosynthesis in microorganisms being used for single
Ge, L., Wang, P., Mou, H., 2011. Study on saccharification techniques of seaweed
cell oil production. Biochimie 86, 807–815.
wastes for the transformation of ethanol. Renew. Energy 36, 84–89.
Reddy, C., Gupta, M., Mantri, V., Jha, B., 2008. Seaweed protoplasts: status,
Guiry, M.D., 2012. The Seaweed Site: Information on Marine Algae. Available from:
biotechnological perspectives and needs. J. Appl. Phycol. 20, 619–632.
<http://www.seaweed.ie/algae/index.html>.
Renn, D., 1997. Biotechnology and the red seaweed polysaccharide industry: status,
Gunaseelan, V.N., 1997. Anaerobic digestion of biomass for methane production: a
needs and prospects. Trends Biotechnol. 15, 9–14.
review. Biomass Bioenerg. 13, 83–114.
RFA (Renewable Fuels Association), 2008. The Gallagher Review of the Indirect
Gupta, S., Abu-Ghannam, N., Scannell, A.G.M., 2011. Growth and kinetics of
Effects of Biofuels Production. Available from: <http://www.renewablefuelsa-
Lactobacillus plantarum in the fermentation of edible Irish brown seaweeds.
gency.gov.uk/_db/_documents/Report_of_the_Gallagher_review.pdf>.
Food Bioprod. Process. 89, 346–355.
Roesijadi, G., Jones, S.B., Snowden-Swan, L.J., Zhu, Y., 2010. Macroalgae as a Biomass
Heady, D., Fan, S., 2008. Anatomy of a Crisis: The Causes and Consequences of
Feedstock: A Preliminary Analysis (PNNL-19944). Available from: <http://
Surging Food Prices (IFPRI Discussion Paper 00831). The International Food
www.pnl.gov/main/publications/external/technical_reports/PNNL-19944.pdf>.
Policy Research Institute. Available from: <http://www.ifpri.org/sites/default/
Ross, A.B., Jones, J.M., Kubacki, M.L., Bridgeman, T., 2008. Classification of
files/publications/ifpridp00831.pdf>.
macroalgae as fuel and its thermochemical behaviour. Bioresour. Technol. 99,
Hejazi, M.A., Wijffels, R.H., 2004. Milking of microalgae. Trends Biotechnol. 22, 189–
6494–6504.
194.
190 K.A Jung et al. / Bioresource Technology 135 (2013) 182–190
Sánchez, Ó.J., Cardona, C.A., 2008. Trends in biotechnological production of fuel
ethanol from different feedstocks. Bioresour. Technol. 99, 5270–5295.
Santelices, B., 1991. Production ecology of Gelidium. Hydrobiologia 221, 31–44.
Shinners, K.J., Binversie, B.N., 2007. Fractional yield and moisture of corn stover
biomass produced in the Northern US corn belt. Biomass Bioenerg. 31, 576–584.
Sze, P., 1993. A Biology of the algae, second ed. Wm. C. Brown Publishers.
Turvey, J.R., Christison, J., 1967. The hydrolysis of algal galactans by enzymes from a
Cytophaga species. Biochem. J. 105, 311–316.
Veeken, A., Kalyuzhnyi, S., Scharff, H., Hamelers, B., 2000. Effect of pH and VFA on
hydrolysis of organic solid waste. J. Environ. Eng. 126, 1076–1081.
Vera, J., Castro, J., Gonzalez, A., Moenne, A., 2011. Seaweed polysaccharides and
derived oligosaccharides stimulate defense responses and protection against
pathogens in plants. Mar. Drugs 9, 2514–2525.
Wargacki, A.J., Leonard, E., Win, M.N., Regitsky, D.D., Santos, C.N.S., Kim, P.B., Cooper,
S.R., Raisner, R.M., Herman, A., Sivitz, A.B., Lakshmanaswamy, A., Kashiyama, Y.,
Baker, D., Yoshikuni, Y., 2012. An engineered microbial platform for direct
biofuel production from brown macroalgae. Science 335, 308–313.
Wegeberg, S., Felby, C. 2010. Algae Biomass for Bioenergy in Denmark: Biological/
Technical Challenges and Opportunities. Available from: <http://www.
bio4bio.dk/~/media/Bio4bio/publications/Review_of_algae_biomass_for_energy_
SW_CF_April2010.ashx>.
Yanagisawa, M., Nakamura, K., Ariga, O., Nakasaki, K., 2011. Production of high
concentrations of bioethanol from seaweeds that contain easily hydrolyzable
polysaccharides. Process Biochem. 46, 2111–2116.
Yu, S., Blennow, A., Bojko, M., Madsen, F., Olsen, C.E., Engelsen, S.B., 2002. Physico-
chemical characterization of floridean starch of red algae. Starch 54, 66–74.