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Microalgal industry in China: challenges and prospects

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Over the past 15 years, China has become the major producer of microalgal biomass in the world. Spirulina (Arthrospira) is the largest microalgal product by tonnage and value, followed by Chlorella, Dunaliella, and Haematococcus, the four main microalgae grown commercially. China's production is estimated at about two-thirds of global microalgae bio-mass of which roughly 90 % is sold for human consumption as human nutritional products ('nutraceuticals'), with smaller markets in animal feeds mainly for marine aquaculture. Research is also ongoing in China, as in the rest of the world, for other high-value as well as commodity microalgal products, from pharmaceuticals to biofuels and CO 2 capture and utilization. This paper briefly reviews the main challenges and potential solutions for expanding commercial microalgae production in China and the markets for microalgae products. The Chinese Microalgae Industry Alliance (CMIA), a network founded by Chinese microalgae researchers and commercial enterprises, supports this industry by promoting improved safety and quality standards, and advancement of technologies that can innovate and increase the markets for microalgal products. Microalgae are a growing source of human nutritional products and could become a future source of sustainable commodities, from foods and feeds, to, possibly, fuels and fertilizers.
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1ST INTERNATIONAL COASTAL BIOLOGY CONGRESS, YANTAI, CHINA
Microalgal industry in China: challenges and prospects
Jun Chen
1,2
&Yan Wang
1
&John R. Benemann
3
&Xuecheng Zhang
4
&Hongjun Hu
5
&
Song Qin
1
Received: 5 May 2015 /Accepted: 23 September 2015
#Springer Science+Business Media Dordrecht 2015
Abstract Over the past 15 years, China has become the major
producer of microalgal biomass in the world. Spirulina
(Arthrospira) is the largest microalgal product by tonnage and
value, followed by Chlorella,Dunaliella,andHaematococcus,
the four main microalgae grown commercially. Chinas produc-
tion is estimated at about two-thirds of global microalgae bio-
mass of which roughly 90 % is sold for human consumption as
human nutritional products (nutraceuticals), with smaller mar-
kets in animal feeds mainly for marine aquaculture. Research is
also ongoing in China, as in the rest of the world, for other high-
value as well as commodity microalgal products, from
pharmaceuticals to biofuels and CO
2
capture and utilization. This
paper briefly reviews the main challenges and potential solutions
for expanding commercial microalgae production in China and
the markets for microalgae products. The Chinese Microalgae
Industry Alliance (CMIA), a network founded by Chinese
microalgae researchers and commercial enterprises, supports this
industry by promoting improved safety and quality standards,
and advancement of technologies that can innovate and increase
the markets for microalgal products. Microalgae are a growing
source of human nutritional products and could become a future
source of sustainable commodities, from foods and feeds, to,
possibly, fuels and fertilizers.
Keywords Microalgae .Spirulina .Chlorella .Dunaliella .
Haematococcus .Nutritional products .Microalgae mass
culture
Introduction
Microalgae are microscopic plants that typically grow
suspended in water using photosynthesis to convert sunlight,
water, CO
2
,andinorganicnutrients(N,P,K,etc.)intoO
2
and a
biomass high in protein, vitamins, antioxidants, and other nu-
trients required by humans and animals. Some microalgae can
also grow heterotrophically by fermentation in the dark using
sugars and other organic substrates. Thousands of microalgal
species are described in the literature, but only a handful of
genera and species are currently produced commercially pho-
tosynthetically namely Spirulina, a cyanobacterium (a prokary-
ote, scientific name Arthrospira, with the two species cultivated
commercially, A. platensis and A. maxima) and four genera that
belong to the eukaryotic green algae (Chlorophyceae): Chlorel-
la vulgaris and C. pyrenoidosa,Dunaliella salina,and
Haematococcus pluvialis.
*Song Qin
sqin@yic.ac.cn
Jun Chen
junchen@yic.ac.cn
Yan Wa n g
ywang@yic.ac.cn
John R. Benemann
jbenemann@aol.com
Xuecheng Zhang
xczhang8@163.com
Hongjun Hu
hjh34@wbgcas.cn
1
Yantai Institute of Coastal Zone Research, Chinese Academy of
Sciences, 17 Chunhui Road, Laishan District, Yantai 264003, China
2
University of Chinese Academy of Sciences, Beijing, China
3
MicroBio Engineering, Inc, PO Box 15821, San Luis
Obispo, CA 93406, USA
4
Ocean University of China, 238 Songling Road, Laoshan District,
Qingdao 266100, China
5
Wuhan Botanical Garden, Chinese Academy of Sciences, 1 Lumo
Road, Hongshan District, Wuhan 430074, China
J Appl Phycol
DOI 10.1007/s10811-015-0720-4
Chlorella is also produced commercially in several coun-
tries, including China, both by photosynthesis (autotrophic)
and fermentation (heterotrophic, on sugars in the dark in
sterilized reactors) (Shi et al. 1999; Ip and Chen 2005; Wang
and Peng 2008; Han et al. 2013). Chlorella production by
fermentation processes has recently expanded with two major
US and European companies, Solazyme (in the USA) and
Roquette (in France), now offering human nutritional and bulk
food ingredients. The non-photosynthetic dinoflagellate
Crypthecodinium cohnii, a source of the long-chain polyun-
saturated fatty acid (LC-PUFA) docosahexaenoic acid (DHA)
used in infant formula, is another alga produced by fermenta-
tions in the dark on sugars, including in China (Jiang et al.
1999; Wynn et al 2005). However, such dark fermentation
processes are not discussed in this review and neither is
mixotrophic production, in which microalgae are grown
mixotrophically using both sunlight and organic substrates,
such as acetate, glycerol, or sugars. Mixotrophic processes re-
quire sterilized enclosed photobioreactors (PBRs), which can-
not be scaled-up to production scale due to high costs. The
focus herein is on the current and potential commercial produc-
tion of microalgae in China using sunlight energy and CO
2
.
Microalgae grown photosynthetically are sources of carbo-
hydrates, protein, oils, and essential nutrients such as vita-
mins, minerals, carotenoids, long-chain omega-3 fatty acids,
and other phytonutrients. For example, Chlorella contains the
so-called Chlorella growth factor (CGF), which can be isolat-
ed from this alga by hot water extraction and is sold commer-
cially as a health-promoting product (Tang and Suter 2011).
Spirulina contains the so-called calcium spirulin, a sulfated
polysaccharide, and phycocyanin, a protein, both thought to
have health-promoting effects. Phycocyanin is also used as
food colorant, recently permitted in both Europe and the
USA. Dunaliella salina and Haematococcus pluvialis are
commercial sources of the antioxidants carotenoids beta-
carotene (also a pro-vitamin A) and astaxanthin, respectively
(Borowitzka 2013a). These microalgal carotenoid products are
sold as both whole biomass and extracts, in the form of dry
powders, tablets, and oils, the latter typically as soft gel capsules.
Microalgae can be cultivated on either fresh, brackish, or
seawater, with agricultural fertilizers as nutrients and carbon
sources either as CO
2
bubbled into the cultures or from added
bicarbonate or even from air. Both Spirulina and Chlorella are
cultivated in China using paddle wheel mixed raceway ponds.
Commercial production using PBRs is currently limited to the
production of H. pluvialis for the carotenoid astaxanthin. Here,
we review the production of these algae with emphasis on pro-
duction in China. It must be noted, however, at the outset, that it
is difficult to obtain specific data on volumes, prices, and markets
for any of the microalgae products; thus, the data provided in the
following are only the best estimates by the authors.
There is increasing interest in China, as in the world, in
both the established and also new microalgae products, both
high value specialties, such as human nutritional products,
coloring agents, the long-chain omega-3 fatty acids (DHA,
EPA), and also lower-value bulk commodities with extensive
R&D ongoing in all areas of this field. The Chinese
Microalgae Industry Alliance (CMIA) was formed to bring
together industry and researchers in advancing this industry
as discussed herein. First, the current status of this industry is
reviewed.
Spirulina (Arthrospira) production
The largest, by tonnage, commercially produced microalgae
in China and in the world is Spirulina (A. platensis and
A. maxima), a filamentous cyanobacterium(e.g., a prokaryote)
with multicellular spiral shaped filaments. This microalga has
many favorable properties for both cultivation and as both
human and animal feeds. Spirulina is cultivated in highly
alkaline medium, typically 16 g L
-1
of bicarbonate, which
minimizes contamination by other algae. The filamentous spi-
ral shape makes it easy to harvest with relatively large opening
screens. Spirulina is also quite digestible by humans and an-
imals, requiring no cell breakage. It is rich in proteins (typi-
cally about 50 %), vitamins, essential amino acids, minerals,
and essential fatty acids such as γ-linolenic acid (GLA), vita-
min B12, carotenoids, and other antioxidants such phycocya-
nin, already mentioned as above, and other phycobiliproteins
(Belay et al. 1993;Hu2003; Ali and Saleh 2012;Belay2013;
Holman and Malau-Aduli 2013).
Spirulina was first cultivated in China in 1970s, but the
limitations of the technology at that time did not lead to
large-scale production. The first national science and technol-
ogy research project to develop microalgae resources was
funded only in 1986, the first Spirulina experimental base
set up in Chenghai Lake, Yong-shen County, Yunnan Prov-
ince in 1989 (Li and Qi 1997), and the first commercial
Spirulina production by the Shenzhen Lanzao Biotech Corpo-
ration founded in 1991 and continuing to operate at present
(Liang et al. 2004). Since then, Spirulina plants have been
established in almost every provinceor region, from the south-
ern Hainan to Inner Mongolia and from Yunnan to Zhejiang
(Fig. 1) (Lu et al. 2011).
Zhang and Xue (2012) estimated that more than 60
Spirulina plants with 7,500,000 m
2
(750 ha) of cultivation
base produced 9600 t dry powders per year in China with an
annual retail value of over four billion Yuan per year (about
US650 million). This would suggest a productivity of about
13 t ha
1
year
1
of biomass and about 70 kg
1
for the products
sold to consumers. Plant production costs would very be gen-
erally about a tenth of retail value, which increases when it
reaches the consumer to account for operating margins, return
on investment, marketing, formulating (e.g., tableting, etc.),
packaging, shipping, distribution, advertising, retail sales,
J Appl Phycol
taxes, etc. Of course, these are very approximate estimates. It
should be noted that Spirulina production in China is still
growing rapidly, close to 10 % per annum. China is now the
largest Spirulina producer worldwide with about two-thirds of
total global production. The bulk of Spirulina production is
sold internally in China with also some exports.
The details of the cultivation process for Spirulina differ in
the geographic regions of China, though all production uses
raceway paddle wheel mixed ponds. In the north, Inner Mon-
golia has become one of the most important centers for com-
mercial production of Spirulina with an output estimated at
about 3000 t year
1
of dry biomass powder. Due to the local
climate, the production system uses raceway ponds under
plastic greenhouses (Fig. 2). This is also the case for other
Spirulina production facilities in north and central China, such
as Heilongjiang province. By contrast, in the south of China,
for example in Fujian, Yunnan, Guangdong and Hainan prov-
inces with higher year-round temperatures, the production
systems use open-air raceway ponds without covering the
greenhouses (Fig. 3). Zhang and Xue (2012) reported that
Spirulina was cultivated in north China only from May to
the beginning of October, such as in Inner Mongolia and the
Heilongjiang province, while in Hainan, Guangdong, and
Guangxi, it was cultivated all year round (see Table 1for
details on Spirulina production in China).
Most Spirulina production in China has used a combina-
tion of bicarbonate and air for the required CO
2
supply, while
Chlorella production requires CO
2
fertilization, provided as
compressed, liquefied CO
2
from commercial sources
(Bmerchant CO
2
^). It is likely that merchant CO
2
is also in-
creasingly being used for Spirulina production as the cost of
bicarbonate has greatly increased, and a significant increase in
productivity can be obtained with such supplemental CO
2
.
Spirulina production requires high bicarbonate concentra-
tions, 16 g L
1
, to maintain pure culture (e.g., to limit invasion
by other microalgae, grazers, etc.). Thus, for a 20-cm deep
pond, 32 t ha
1
is needed to start up production. However, this
can be extensively recycled as long as CO
2
is supplied from a
concentrated source, in which the 32-t bicarbonate can be
replaced with only 20 t of the less expensive sodium
Fig. 1 Location of Spirulina cultivation base in China (the information collected by many methods, including field survey, searches from the Internet,
and others)
J Appl Phycol
carbonate. This has been the practice in the USA and other
countries for Spirulina production since the start of the indus-
try 30 years ago, and is likely that this process will be increas-
ingly adopted in China, as once-through bicarbonate utiliza-
tion becomes more costly.
Almost all of the production of Spirulina is used for human
consumption as nutritional supplements (Bnutraceuticals^).
Spirulina biomass is typically produced as a spray dried pow-
der and generally sold and mostly used as such by consumers
in China who typically add it to fruit juices or other foods.
Algal powders are also converted into tablets and capsules.
Relatively smaller amounts are used for animal feeds; mainly
ornamental fish feeds (e.g., Koi, tropical aquarium fish).
Recently, there has been increasing interest in the use of
Spirulina for aquaculture feeds (Burr et al. 2012), as it is
reported to benefit fish health, improve growth, and reduce
mortality. However, the current price is too high for wide
applications as aquaculture or animal feeds.
Spirulina contains, as noted already, phycocyanin, a blue
protein that has been sold for over 30 years in Japan as a food
coloring agent. Phycocyanin has been extensively commer-
cialized as a colorant in food such as chewing gum, dairy
products, jellies, and other food products (Santiago-Santos
et al. 2004; Sekar and Chandramohan 2008). Phycocyanin is
also used as fluorescent agents applied in flow cytometry and
immunological analysis (Glazer 1994) and pharmaceuticals
Fig. 2 Vi ew s of Spirulina
production pond systems in Inner
Mongolia (photograph by John R.
Benemann)
Fig. 3 Vi ew s of Spirulina
production pond systems in the
Hainan Province (photograph
supplied by King Dnarmsa
Spirulina Co., Ltd)
J Appl Phycol
(Hu et al. 2008). Phycocyanin was recently approved for food
coloring in Europe and the USA, and that is now leading to
rapidly increasing production of this protein with markets be-
ing developed for the residual biomass (about 90 % oftotal) in
aquaculture feeds. The isolation and commercial production
of high-value products from Spirulina, including
phycobiliproteins, peptides, and polysaccharides, is the sub-
ject of a currently ongoing multi-laboratory projects funded by
the Chinese Government.
Chlorella production
Chlorella was first cultivated commercially in Japan and also
in China in the 1960s, earlier than Spirulina,butthelimita-
tions of the technology at that time did not lead to large-scale
production in China. Over the past decade, China has also
become the major worldwide producer of Chlorella,overtak-
ing the traditional production in Japan. Chlorella production is
overall considerably smaller in volume than that of Spirulina,
probably a quarter, but price per ton is significantly higher.
Many of the Spirulina production enterprises produce
Chlorella alongside with Spirulina, generally as a smaller part
of the larger Spirulina production process. Chlorella is a tech-
nically more challenging and expensive production process,
compared to Spirulina, due to greater potential for contamina-
tion and the need for centrifuges for harvesting these micro-
scopic cells. This contrasts to the easier harvesting of the fil-
amentous Spirulina and fewer problems of contamination due
to the high bicarbonate growth medium.
There is little information on Chlorella production in Chi-
nacentrifugation is used to harvest the algal biomass, and
CO
2
is used to provide the carbon. Chlorella is spray dried and
sold similarly to Spirulina, as a human nutritional supplement,
both as a powder and in tablet and capsule form. The so-called
CGF extract is also mentioned. Chlorella decolorized protein
powders have recently been developed, although thus far only
from biomass produced by dark fermentations, that have
potential applications in replacing conventional wheat flours
in dietary (weight loss) products, a potentially very large
market.
Dunaliella and Haematococcus production
The other two microalgae grown commercially with sunlight
are Dunaliella (grown at very high salinity) and
Haematococcus (a freshwater species) with high-value carot-
enoids extracted from their biomass, beta-carotene, and
astaxanthin, respectively.
Dunaliella was first commercialized in Australia and Israel
in the 1980s (Ben Amotz et al. 1988; Borowitzka and
Borowitzka 1990; Schlipalius 1991; Borowitzka 2013b). β-
Carotene is the main source of pro-vitamin A and is widely
used as a food colorant, with a global market estimated to
surpass US280 million in 2015 (Ribeiro et al. 2011). Howev-
er, this is for synthetic beta-carotene. BASF (a German chem-
ical company) is the undisputed world leader in natural beta-
carotene production from Dunaliella salina, with over a thou-
sand hectares of production ponds in two plants in Australia
(acquired as part of its take over a few years ago of Cognis)
(Borowitzka 2013b). BASF has announced expansion with a
possibly even larger production system currently being
established in Saudi Arabia, a local joint venture with the
National Aquaculture Group. Dunaliella salina production
for beta-carotene in China was carried out by the Inner Mon-
golia Lantai Industrial Co., Ltd (Inner Mongolia) and Salt
Research Institute, China National Salt Industry Corp
(Tianjin) (Yin et al. 2013).
Haematococcus was commercialized for astaxanthin in Is-
rael and USA (Boussiba 2000; Lorenz and Cysewski 2000)
and is now also ongoing in China (http://www.algachina.com;
http://www.e-asta.cn;http://www.astawefirst.com). The
principal existing market for astaxanthin is for use as a feed
additive for farmed salmon and trout to pigment the fish flesh,
with about 200 t of synthetic astaxanthin sold for about US200
million. However, as for natural beta-carotene, currently the
Tabl e 1 The main location, period, and annual output of Spirulina cultivation in China
Location Cultivation period Annual output (dw)
Inner Mongolia, Heilongjiang From May to the beginning of October >3000 t
Henan, Jiangsu, Shandong From May to the mid-month of October >500 t
Jiangxi From the mid of April to the beginning of November >2000 t
Yunnan, Sichuan From the mid of April to the mid-month of November >1000 t
Fujian From the beginning of April to the end of November >200 t
Hainan, Guangdong All year round >1000 t
Guangxi All year round >800 t
The main location and period of Spirulina cultivation in China isbased fromZhang and Xue (2012). The annual output was estimated by visiting leading
enterprises and discussing with several leaders of leading enterprises and other methods
J Appl Phycol
only market for natural astaxanthin from microalgae is for
human nutritional applications, mainly because of its high
selling price, up to about 10,000 kg
1
, or almost 10-fold
higher than the current price for synthetic astaxanthin used
in aquaculture. Haematococcus pluvialis production for
astaxanthin in China is developing rapidly, mainly in Yunnan
and the Hubei Province. There, several dozen companies are
developing the production process, though only a handful are
currently in production including one large operation in China
using PBRs, such as Yunnan Alphy Biotech Co. Ltd
(Chuxiong, in Yunnan province) (Fig. 5).
Microalgae for aquaculture feeds
Microalgae are also of great importance and interest as aquacul-
ture feeds (Benemann 1992). A number of marine microalgae
species are used as aquaculture feeds but only in relatively small
amounts, kilograms not tons. The main species used are from the
genera such as Nannochloropsis,Pavlova,Isochrysis,
Tetraselmis,Thalassiosira,Chaetoceros, and Skeletonema.
These are particularly rich in the nutrients required by the larval
and juvenile stages of the fish, penaeid shrimp and other crusta-
ceans, molluscs, etc., being raised by the aquaculture operations.
Of particular interest are the long-chain C
20
and C
22
omega-3
fatty acids eicosapentaenoic acid (EPA) and docosahexaenoic
acid (DHA) required in fish nutrition. In some cases, the algae
are used to feed rotifers and brine shrimp that are then used to
feed the juvenile animals (Borowitzka 1997; Hemaiswarya et al.
2011). Microalgae, in larger quantities, in particular Spirulina,
are also used as a source of natural pigments for the culture of
prawns, salmonid fish, ornamental fish, and other high-value fish
(Priyadarshani and Rath 2012).
The major challenge in aquaculture operations is that for
just hatched and juvenile animals (e.g., hatchery and nursery
operations), the algal feeds have to be live or at least have
dispersed unicellular dispersions and cannot be spray-dried,
and even freeze drying is often not successful. Thus, typically,
microalgae are produced on-site as needed, in a few cubic
meters of culture, and then fed directly, without harvesting,
to the fish, shrimp, or bivalve larval and juvenile cultures,
which require live microalgae feeds. This has been, however,
a major bottleneck for aquaculture operations worldwide, as
growing the algae when needed, at the right time, and in suf-
ficient amounts has proven challenging. Thus, producing al-
gae remotely and shipping them to where and when required
is attractive but requires concentrating (e.g., centrifuging to a
high solids paste) and storing of the algal cells at low temper-
atures, typically with a cryoprotectant added, for use when
needed. This has been a major limitation, as the product has
to be shipped refrigerated and has very limited shelf life. Stor-
ing at 18 °C without cryoprotectant can reduce the nutrition
loss less than other various cryoprotectants and cooling
methods (Yu et al. 2013). Freeze drying can be used but also
has some challenges. Some enterprises themselves cultivate
and use microalgae biomass to rear rotifers or larvae of marine
finfish and crustaceans. For example, Tianjin Ocean Pal Bio-
tech Co., Ltd., a member of CMIA, cultivates Chlorella with
seawater in Hainan, to meet their needs in rearing rotifers
which are then used to feed shrimp larvae.
In 1999, the production of microalgae for aquaculture
reached reportedly 1000 t (about 62 % for molluscs, 21 %
for shrimps, and 16 % for fish) (Hemaiswarya et al. 2011),
though this figure is likely a high estimate. However, it is the
much larger-scale production of microalgae to replace aqua-
culture feeds currently produced from fish meal and fish oils
that has the greatest near-term potential for large-scale
microalgae biomass production. This is a very large, several
million tons per year, market with increasingly rising costs for
fish meal/oil, currently over US 3000 t
1
, and uncertain sup-
ply, thus presents a large, highest-value, near-term market for
bulk microalgae as aquaculture and animal feeds generally.
Biofuels and CO
2
capture and utilization R&D
The National Development and Reform Commission of the
Peoples Republic of China (NDRC) 2007 (http://www.
ccchina.gov.cn/WebSite/CCChina/UpFile/2007/
20079583745145.pdf) promulgated the Medium and Long-
Term Development Plan for Renewable Energy, which
projected that the consumption of biodiesel in China could
reach two million tons in 2020. Microalgae biodiesel produc-
tion has been suggested to have the advantage of greatly ex-
ceeding the productivity of agricultural oleaginous crops,
without competing for arable land (Wijffels and Barbosa
2010). Over the past 5 years, the production of biofuel from
microalgae, in conjunction with CO
2
capture and utilization,
has also gained increased interest in China. Li et al. (2011)
listed a number of research group and corporations actively
involved in this research in detail (Li et al. 2011).
However, there is an increasing amount of published infor-
mation in peer-reviewed publications that provides informa-
tion on the advances being made. The following are few
examples:
&Han et al (2012) devised a novel 96-well microplate swiv-
el system (M96SS) for high-throughput screening of
microalgae strains for CO
2
fixation (Han et al. 2012).
&Li et al (2013) designed transparent covers for a raceway
pond, which directly touched the surface of culture, and
investigated CO
2
fixation; efficiency increased to 95 %
under intermittent gas sparging (Li et al. 2013).
&Yantai Hearol Biology Technology Co., Ltd, a CMIA
member company, was the first commercial plant in the
world using power plant flue gas (CO
2
flue gas) for
J Appl Phycol
microalgae cultivation and the first to produce the seawa-
ter Nannochloropsis commercially, selling into the aqua-
culture market (Fig. 4).
The Chinese Microalgae Industry Alliance (CMIA)
There is increasing interest and intensive R&D ongoing in
China, as in the whole world, on both the current and also
new microalgae products, both high-value specialty products,
such as the current human nutritional products and lower val-
ue commodities, such as feeds and fuels, with extensive R&D
ongoing. This interest is being driven by the demand of sus-
tainable, green energy and products, as well as national objec-
tives of reducing CO
2
emission from fossil fuels, in particular,
coal-fired power plants.
Meanwhile, the more immediate issues currently faced by
the Chinese microalgae industry are public perceptions re-
garding the wholesomeness of microalgae foods, as well as
the high costs of production, which limit both domestic or
international markets. To help address these challenges, the
CMIAwas established on December 9, 2010 in Yantai, China,
led by a group of Chinese-leading microalgal specialists and
enterprise leaders, bringing together industry and researchers.
The CMIA now includes 14 leading microalgae-producing
enterprises (Table 2). The objective of the CMIA is to address
these two major challenges in commercial microalgae produc-
tion and to the proposed solutions, as discussed next.
Challenge I: the microalgae food standard system
required improvement
In China, food standards are the reference points for market
regulation, including safety, quality, production, and other stan-
dards (Chen and Li 2014). The National Health and Family
Planning Commission of the Peoples Republic of China
(NHFPC) announced the BFood Standards System Improvement
Projects,^which include plans for improving quality and safety
standards for agricultural products and food hygienic, quality,
and industrial standards in 2012 (http://www.moh.gov.cn/sps/
s3594/201210/fc63695b7417477eac341507854f8525.shtml).
After 2 years of deliberation, the BNational Food Safety
Standards Formulated and Revised Proposal^was published
by the NHFPC in 2014 (http://www.nhfpc.gov.cn/sps/s3593/
201309/50799b73ad7c49c482da524231523573.shtml).
According to this proposal, BAlgae Products Hygienic Standard^
should be improved and re-named as BAlgae and Their Products
Food Safety National Standard.^This standard will be manda-
tory, applying to all algae products brought to market, and will
ensure the safety and quality of microalgae products. Actually
applying these standards in the market will be the first challenge
for improving public confidence in microalgae products and ad-
vancing the development of the Chinese microalgae industry.
Challenge II: production costs cannot meet market
requirements
There is a strong global market demands of selected microalgal
high-value products, including carotenoids (beta-carotene, lutein,
Fig. 4 Vi ew s of
Nannochloropsis pond systems
cultivated with flue gas in Yantai
Hearol Biology Technology Co.,
Ltd (photograph downloaded
from this enterpriseswebsite)
J Appl Phycol
astaxanthin), fatty acids (long-chain omega-3, EPA, DHA), and
phycobiliproteins (e.g., phycocyanin, etc.) (Borowitzka 2013a;
Markou and Nerantzis 2013). However, production costs of even
such high-value products are still too high to meet most require-
ments from domestic and international markets for larger vol-
umes at lower prices. Alternative, lower-cost sources for these
products are currently available, both synthetic and natural,
which limit the potential of microalgae products to small niche
markets such as vegetarian EPA and DHA (vs. fish oil-derived
products) or natural carotenoids (vs. synthetics or even other
natural sources).
Solution I: improving safety and quality standards
nationally and regionally
To improve safety and quality standards is the key strategy to
build public confidence in microalgae healthy food. The first
three meetings of CMIA discussed the necessity of improving
safety and quality standards nationally, regionally, and
through organization and rules of the CMIA. The fourth meet-
ing of the CMIA focused on the quality control of microalgal
products for sustainable development. Several important pa-
rameters of quality control points were determined. The fifth
meeting of the CMIAwas held in Qingdao, with a background
of public doubt regarding the biosafety of Spirulina healthy
food, with the CMIA providing a clear voice to the public at
this meeting. In 2014, the eighth meeting was held in Qing-
dao, China. This conference reached consensus that BAlgae
and Their Products Food Safety National Standard^being
developed should also apply for microalgae products not just
to macroalgal products, and the CMIA submitted several ad-
visories, which include quality testing data and current market
statutes.
The CMIA is also currently improving the Food Grade
Spirulina Powders Quality National Standard to keep the pace
with market developments. To improve these standards scien-
tifically, many algae researchers in the CMIA test the quality
of Spirulina dry powders as a public service.
&Lirong Songs research group (Institute Hydrobiology,
Chinese Academy of Sciences) tested microcytic toxins.
&Xiaojun Yans research group (Ningbo University) tested
carotenoid content.
&Song Qins research group (Yantai Institute of Coastal
Zone Research, Chinese Academy of Sciences) tested wa-
ter, heavy metals (lead, mercury, cadmium, arsenic), and
phycocyanin contents.
Regional quality standards will be advanced for continuing
sustainable development of the microalgae healthy food in-
dustry in China.
Solution II: promoting technology innovation
Promoting technology innovation will be important for
microalgae industry transformation and upgrading, such as
Tab l e 2 Leading enterprises in the Chinese Microalgae Industry
Alliance
Enterprise Location Products
Beihai SBD bio science
technology Co., Ltd
Guangxi Food grade: Spirulina
powders and tables
C.B.N Spirulina group Co.,
Ltd
Jiangsu Food grade: Spirulina
powders, tables Chlorella
powders or tablets,
phycocyanin, Spirulina
polysaccharide
King Dnarmsa Spirulina
Co., Ltd
Hainan,
Fujian,
Jiangxi
Food grade: spirulina
powders and tables
Chlorella powders or
tablets, phycocyanin
Inner Mongolia Rejuv
Biotech Co., Ltd
Inner
Mongolia
Food grade: Spirulina
powders, tablets, capsules
Sanya Neptunus Marine
Biological Technology
Co., Ltd
Hainan Food grade: seawater
Spirulina powders,
seawater Spirulina
tablets, Spirulina
polysaccharide
Feed grade: seawater
Chlorella biomass,
seawater Chlorella
concentrated solution
Yantai Hearol Biology
Technology Co., Ltd
Shandong Feed grade:
Nannochloropsis
oceanica powders and
Nannochloropsis
oceanica concentrated
solution
Zhongsan Lanzao Biology
Food Co., Ltd
Guangxi Food grade: Spirulina
powders and tablets
Chenghai Baoer Biological
Development Co., Ltd
Yunnan Food grade: spirulina
Spirulina powders and
tablets
Guangxi Agricultural
Reclamation Lvxian
Biology healthy food Co.,
Ltd
Guangxi Food grade: Spirulina
powders and tablets
Dongying Diazen
Biological Engineering
Co., Ltd
Shandong Food grade: Spirulina
tablets; Feed grade:
seawater Chlorella
concentrated solution
Dongying Haifu Biological
Engineering Co., Ltd
Shandong Food grade: Spirulina
tablets and some
Spirulina composited
food, Spirulina capsule
Inner Mongolia Meangjiali
Spirulina Co., Ltd
Inner
Mongolia
Food grade: Spirulina
powders and tablets
Shandong Tianshun
pharmacy Co., Ltd
Shandong Pharmaceutical grade:
Spirulina tablet, Spirulina
capsule;
Tianjing Ocean Pal Carol
Biotech Co., Ltd
Hainan Feed grade: Chlorella
concentrated solution
J Appl Phycol
further process improvements and value-added products, and
most importantly, lower-cost production. The CMIA has sup-
plied various platforms for members to achieve a fast trans-
formation from test tube in the laboratory to production plant
and markets.
For example of such research applied to microalgae pro-
duction, this laboratory in Yantai, developed methods for ex-
traction of phycobilins from Spirulina by response surface
analysis (Shao et al. 2013a), their purification by a single step
chromatography (Shao et al. 2013b), and the antioxidant pep-
tides from phycobilins by an enzymatic process (Tang et al.
2012); phycocyanin microcapsules extrusion using alginate
and chitosan as coating materials (Yan et al. 2014). The pat-
ents of the production methods of food grade
phycobiliproteins on plant scale has been used by a
cooperating enterprise, C.B.N. Spirulina Co., Ltd., and obtain-
ed good economic effects.
For another example, Wei Congsresearchgroup(inBei-
jing) designed and developed an economical device for CO
2
supplementation in large-scale microalgae production, and the
gaseous absorptivity was enhanced to nearly 80 % (Su et al.
2008). Then, they estimated the effects of initial total carbon
concentrations, suspension depths, and pH values on the CO
2
absorptivity. The results indicated that an average CO
2
absorp-
tivity of 86 % and CO
2
utilization efficiency of 79 % were
achieved using this device in large-scale cultivation of
Spirulina, with an initial total carbon concentration of
0.06 mol L
1
and pH 9.8 (Bao et al. 2012).
Yuanguang Lis research group (in Shanghai) investigated
that the effects of temperature on the variations of biomass
concentration, lipid content, and fatty acid composition for
production of biofuels under a light-dark cyclic culture of
Chlorella pyrenoidosa cooperated with the Jiaxing Zeyuan
Bio-products Co., Ltd. (Jiaxing, Zhejiang province). The re-
sults showed that by keeping culture broth at above 30 °C
during the daytime, net biomass and lipid productivity was
increased by about 38 and 45 %, respectively (Han et al.
2013).
Tianzhong Lius team (in Qingdao) invented an attached
cultivation technology for production of microalgae biofuels
with microalgae cells growing on the surface of vertical arti-
ficial supporting material to form an algal biofilm. Multiple
such algal biofilms were assembled in an array fashion to
dilute solar irradiation thus facilitating high photosynthetic
efficiency (Liu et al. 2013). They also investigated methods
of CaCO
3
addition and intermittent sparging, finding that
these have great potential to overcome the inhibition of flue
gas for cultivation of Scenedesmus dimorphus (Jiang et al.
2013).
As a final example, one reaching large-scale production,
Jianguo Lius research group (in Qingdao) designed a photo
bioreactor for a pilot-scale culture of H. pluvialis, and the
technology has been used in Yunna Alphy Biotech Co., Ltd.
to produce astaxanthin, enhancing the production efficiency in
H. pluvialis of about 35-fold above the traditional method
(Fig. 5)(Liuetal.2006).
Conclusion: microalgae for sustainable development
Increasing microalgae markets are necessary to promote
microalgaes sustainable development. In 2014, the seventh
CMIA meeting was held in Tianjin, China. This meeting
mainly focused on the necessity, feasibility, and key technol-
ogies and difficulties of producing microalgae as feeds/diets
for aquaculture animals. Six roundtables discussed the nutri-
ent evaluation of Spirulina,Chlorella, and other microalgae
for use as aquaculture feeds, how to reduce the costs of
microalgae feeds production, and the logistics of microalgae
aquaculture feeds. The meeting made achieving 3000 t
microalgae biomass with the cost being about US3000 t
1
for the aquaculture market as a goal. Reducing the cost and
Fig. 5 Vi ew s of Haematococcus
pluvialis production with
photobioreactors in Yunnan
Province (supplied by Prof.
Jianguo Liu )
J Appl Phycol
enhancing the biomass quality remain as the key issue for the
microalgae industry. When the output of microalgae biomass
achieves between 0.1 and 1 million ton, microalgae biomass
will become a clear vision as a key protein resource for human
population. When the output of microalgae biomass reaches 1
to 10 million tons, microalgae biomass will become a strategic
food and feed resource.
In the past 30 years, the Chinese microalgae industry has
increased influence on the world microalgae industry. The
BMicroalgae Dream of Chinese People^is to provide healthy
food for people directly or indirectly, fix carbon dioxide, and
reduce eutrophication, promoting microalgae to keep the pace
with evolution of our earth friendly. Institution building, re-
search progress, technological development, and microalgae
culture system construction could be the important impetus for
the sustainable development of the microalgae industry.
Acknowledgments This work was supported by the National Natural
Science Foundation of China (408760862) and Public Science and Tech-
nology Research Funds Projects of the Ocean (201205027). We also wish
to thank Inner Mongolia Rejuv Biotech Co. Ltd and Yantai Hearol Biol-
ogy Technology Co. Ltd for permitting us to use the pictures in Figs. 2
and 4. We are grateful to King Dnarmsa Spirulina Co. Ltd for supplying
us the pictures Fig. 3and Prof. Jianguo Liu (Institute of Oceanology,
Chinese Academy of Sciences, Qingdao) for supplying us Fig. 5.
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... In addition, the filament lengths of spirulina cultured under different aeration intensities were not significantly different (oneway ANOVA, p = 0.593). The culture period lasted until the 21st day of culture with several growth phases of spirulina observed distinctly: the lag phase (days 0-6), the exponential phase (days 7-9), the stationary phase (days [10][11][12][13][14][15][16][17][18], and the decline phase (days 19-21) as shown in Fig. 2A. Moreover, there were significant differences in the cell productivity, maximum specific growth rate, and doubling time in spirulina cultured at varying aeration intensities (Supplementary Table 2). ...
... Internationally, large-scale commercial production of spirulina has been performed in Europe (e.g., Germany, France, Spain, and Italy) [4], China [11], Inner Mongolia [31], the United States of America [29,54], Central and South America [6,29], India [43], and South Africa [22]. The spirulina production system determines the value of the products for which they can be applied [4]. ...
... In Europe, 71% of spirulina production uses photobioreactor systems while 19% uses pond systems [4]. In the rest of the spirulina-producing countries, a raceway pond system equipped with mechanized agitation, filtering, and drying systems is used [6,11,22,29,31,40,56]. Currently, the spirulina industry is beset by problems of high production costs, which cannot meet market requirements [11], and a lack of standard product systems, which complicate regulatory and administrative procedures [4,11,13]. ...
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