microalgal industry in china: challenges and prospects

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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, and Haematococcus, 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 , and inorganic nutrients (N, P, K, etc.) into O 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 [email protected] Jun Chen [email protected] Yan Wang [email protected] John R. Benemann [email protected] Xuecheng Zhang [email protected] Hongjun Hu [email protected] 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

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Page 1: Microalgal industry in China: challenges and prospects

1ST INTERNATIONAL COASTAL BIOLOGY CONGRESS, YANTAI, CHINA

Microalgal industry in China: challenges and prospects

Jun Chen1,2& Yan Wang1 & John R. Benemann3

& Xuecheng Zhang4 & Hongjun Hu5&

Song Qin1

Received: 5 May 2015 /Accepted: 23 September 2015# Springer Science+Business Media Dordrecht 2015

Abstract Over the past 15 years, China has become the majorproducer of microalgal biomass in the world. Spirulina(Arthrospira) is the largest microalgal product by tonnage andvalue, followed by Chlorella, Dunaliella, and Haematococcus,the four main microalgae grown commercially. China’s produc-tion is estimated at about two-thirds of global microalgae bio-mass of which roughly 90 % is sold for human consumption ashuman nutritional products (‘nutraceuticals’), with smaller mar-kets in animal feeds mainly for marine aquaculture. Research isalso ongoing in China, as in the rest of the world, for other high-value as well as commodity microalgal products, from

pharmaceuticals to biofuels andCO2 capture and utilization. Thispaper briefly reviews the main challenges and potential solutionsfor expanding commercial microalgae production in China andthe markets for microalgae products. The Chinese MicroalgaeIndustry Alliance (CMIA), a network founded by Chinesemicroalgae researchers and commercial enterprises, supports thisindustry by promoting improved safety and quality standards,and advancement of technologies that can innovate and increasethe markets for microalgal products. Microalgae are a growingsource of human nutritional products and could become a futuresource of sustainable commodities, from foods and feeds, to,possibly, fuels and fertilizers.

Keywords Microalgae . Spirulina .Chlorella .Dunaliella .

Haematococcus . Nutritional products .Microalgaemassculture

Introduction

Microalgae are microscopic plants that typically growsuspended in water using photosynthesis to convert sunlight,water, CO2, and inorganic nutrients (N, P, K, etc.) into O2 and abiomass high in protein, vitamins, antioxidants, and other nu-trients required by humans and animals. Some microalgae canalso grow heterotrophically by fermentation in the dark usingsugars and other organic substrates. Thousands of microalgalspecies are described in the literature, but only a handful ofgenera and species are currently produced commercially pho-tosynthetically namely Spirulina, a cyanobacterium (a prokary-ote, scientific nameArthrospira,with the two species cultivatedcommercially, A. platensis and A. maxima) and four genera thatbelong to the eukaryotic green algae (Chlorophyceae):Chlorel-la vulgaris and C. pyrenoidosa, Dunaliella salina, andHaematococcus pluvialis.

* Song [email protected]

Jun [email protected]

Yan [email protected]

John R. [email protected]

Xuecheng [email protected]

Hongjun [email protected]

1 Yantai Institute of Coastal Zone Research, Chinese Academy ofSciences, 17 Chunhui Road, Laishan District, Yantai 264003, China

2 University of Chinese Academy of Sciences, Beijing, China3 MicroBio Engineering, Inc, PO Box 15821, San Luis

Obispo, CA 93406, USA4 Ocean University of China, 238 Songling Road, Laoshan District,

Qingdao 266100, China5 Wuhan Botanical Garden, Chinese Academy of Sciences, 1 Lumo

Road, Hongshan District, Wuhan 430074, China

J Appl PhycolDOI 10.1007/s10811-015-0720-4

Page 2: Microalgal industry in China: challenges and prospects

Chlorella is also produced commercially in several coun-tries, including China, both by photosynthesis (‘autotrophic’)and fermentation (‘heterotrophic’, on sugars in the dark insterilized reactors) (Shi et al. 1999; Ip and Chen 2005; Wangand Peng 2008; Han et al. 2013). Chlorella production byfermentation processes has recently expanded with two majorUS and European companies, Solazyme (in the USA) andRoquette (in France), now offering human nutritional and bulkfood ingredients. The non-photosynthetic dinoflagellateCrypthecodinium 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 fermentationprocesses are not discussed in this review and neither ismixotrophic production, in which microalgae are grownmixotrophically 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. Thefocus herein is on the current and potential commercial produc-tion of microalgae in China using sunlight energy and CO2.

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 theso-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 sulfatedpolysaccharide, and phycocyanin, a protein, both thought tohave health-promoting effects. Phycocyanin is also used asfood colorant, recently permitted in both Europe and theUSA. Dunaliella salina and Haematococcus pluvialis arecommercial sources of the antioxidants carotenoids beta-carotene (also a pro-vitamin A) and astaxanthin, respectively(Borowitzka 2013a). These microalgal carotenoid products aresold as both whole biomass and extracts, in the form of drypowders, tablets, and oils, the latter typically as soft gel capsules.

Microalgae can be cultivated on either fresh, brackish, orseawater, with agricultural fertilizers as nutrients and carbonsources either as CO2 bubbled into the cultures or from addedbicarbonate or even from air. Both Spirulina and Chlorella arecultivated in China using paddle wheel mixed raceway ponds.Commercial production using PBRs is currently limited to theproduction 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 itis difficult to obtain specific data on volumes, prices, andmarketsfor any of the microalgae products; thus, the data provided in thefollowing are only the best estimates by the authors.

There is increasing interest in China, as in the world, inboth 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 extensiveR&D ongoing in all areas of this field. The ChineseMicroalgae Industry Alliance (CMIA) was formed to bringtogether industry and researchers in advancing this industryas discussed herein. First, the current status of this industry isreviewed.

Spirulina (Arthrospira) production

The largest, by tonnage, commercially produced microalgaein China and in the world is Spirulina (A. platensis andA.maxima), a filamentous cyanobacterium (e.g., a prokaryote)with multicellular spiral shaped filaments. This microalga hasmany favorable properties for both cultivation and as bothhuman and animal feeds. Spirulina is cultivated in highlyalkaline medium, typically 16 g L-1 of bicarbonate, whichminimizes contamination by other algae. The filamentous spi-ral shape makes it easy to harvest with relatively large openingscreens. 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; Hu 2003; Ali and Saleh 2012; Belay 2013;Holman and Malau-Aduli 2013).

Spirulina was first cultivated in China in 1970s, but thelimitations of the technology at that time did not lead tolarge-scale production. The first national science and technol-ogy research project to develop microalgae resources wasfunded only in 1986, the first Spirulina experimental baseset up in Chenghai Lake, Yong-shen County, Yunnan Prov-ince in 1989 (Li and Qi 1997), and the first commercialSpirulina 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 beenestablished in almost every province or 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 60Spirulina plants with 7,500,000 m2 (750 ha) of cultivationbase produced 9600 t dry powders per year in China with anannual retail value of over four billion Yuan per year (aboutUS650 million). This would suggest a productivity of about13 t ha−1 year−1 of biomass and about 70 kg−1 for the productssold to consumers. Plant production costs would very be gen-erally about a tenth of retail value, which increases when itreaches the consumer to account for operating margins, returnon investment, marketing, formulating (e.g., tableting, etc.),packaging, shipping, distribution, advertising, retail sales,

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taxes, etc. Of course, these are very approximate estimates. Itshould be noted that Spirulina production in China is stillgrowing rapidly, close to 10 % per annum. China is now thelargest Spirulina producer worldwide with about two-thirds oftotal global production. The bulk of Spirulina production issold internally in China with also some exports.

The details of the cultivation process for Spirulina differ inthe geographic regions of China, though all production usesraceway 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 atabout 3000 t year−1 of dry biomass powder. Due to the localclimate, the production system uses raceway ponds underplastic greenhouses (Fig. 2). This is also the case for otherSpirulina production facilities in north and central China, suchas 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 productionsystems use open-air raceway ponds without covering thegreenhouses (Fig. 3). Zhang and Xue (2012) reported that

Spirulina was cultivated in north China only from May tothe beginning of October, such as in Inner Mongolia and theHeilongjiang province, while in Hainan, Guangdong, andGuangxi, it was cultivated all year round (see Table 1 fordetails on Spirulina production in China).

Most Spirulina production in China has used a combina-tion of bicarbonate and air for the required CO2 supply, whileChlorella production requires CO2 fertilization, provided ascompressed, liquefied CO2 from commercial sources(Bmerchant CO2^). It is likely that merchant CO2 is also in-creasingly being used for Spirulina production as the cost ofbicarbonate has greatly increased, and a significant increase inproductivity can be obtained with such supplemental CO2.Spirulina production requires high bicarbonate concentra-tions, 16 g L−1, to maintain pure culture (e.g., to limit invasionby other microalgae, grazers, etc.). Thus, for a 20-cm deeppond, 32 t ha−1 is needed to start up production. However, thiscan be extensively recycled as long as CO2 is supplied from aconcentrated source, in which the 32-t bicarbonate can bereplaced 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)

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carbonate. This has been the practice in the USA and othercountries 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 humanconsumption as nutritional supplements (Bnutraceuticals^).Spirulina biomass is typically produced as a spray dried pow-der and generally sold and mostly used as such by consumersin 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; mainlyornamental fish feeds (e.g., Koi, tropical aquarium fish).

Recently, there has been increasing interest in the use ofSpirulina for aquaculture feeds (Burr et al. 2012), as it isreported to benefit fish health, improve growth, and reducemortality. However, the current price is too high for wideapplications as aquaculture or animal feeds.

Spirulina contains, as noted already, phycocyanin, a blueprotein that has been sold for over 30 years in Japan as a foodcoloring agent. Phycocyanin has been extensively commer-cialized as a colorant in food such as chewing gum, dairyproducts, jellies, and other food products (Santiago-Santoset al. 2004; Sekar and Chandramohan 2008). Phycocyanin isalso used as fluorescent agents applied in flow cytometry andimmunological analysis (Glazer 1994) and pharmaceuticals

Fig. 2 Views of Spirulinaproduction pond systems in InnerMongolia (photograph by John R.Benemann)

Fig. 3 Views of Spirulinaproduction pond systems in theHainan Province (photographsupplied by King DnarmsaSpirulina Co., Ltd)

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(Hu et al. 2008). Phycocyanin was recently approved for foodcoloring in Europe and the USA, and that is now leading torapidly increasing production of this protein with markets be-ing developed for the residual biomass (about 90% of total) inaquaculture feeds. The isolation and commercial productionof high-value products from Spirulina , includingphycobiliproteins, peptides, and polysaccharides, is the sub-ject of a currently ongoingmulti-laboratory projects funded bythe Chinese Government.

Chlorella production

Chlorella was first cultivated commercially in Japan and alsoin China in the 1960s, earlier than Spirulina, but the limita-tions of the technology at that time did not lead to large-scaleproduction in China. Over the past decade, China has alsobecome the major worldwide producer of Chlorella, overtak-ing the traditional production in Japan.Chlorella production isoverall considerably smaller in volume than that of Spirulina,probably a quarter, but price per ton is significantly higher.Many of the Spirulina production enterprises produceChlorella alongside with Spirulina, generally as a smaller partof 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 dueto the high bicarbonate growth medium.

There is little information on Chlorella production in Chi-na—centrifugation is used to harvest the algal biomass, andCO2 is used to provide the carbon.Chlorella is spray dried andsold similarly to Spirulina, as a human nutritional supplement,both as a powder and in tablet and capsule form. The so-calledCGF extract is also mentioned. Chlorella decolorized proteinpowders have recently been developed, although thus far onlyfrom biomass produced by dark fermentations, that have

potential applications in replacing conventional wheat floursin dietary (weight loss) products, a potentially very largemarket.

Dunaliella and Haematococcus production

The other two microalgae grown commercially with sunlightare Dunaliella (grown at very high salinity) andHaematococcus (a freshwater species) with high-value carot-enoids extracted from their biomass, beta-carotene, andastaxanthin, respectively.

Dunaliellawas first commercialized in Australia and Israelin the 1980s (Ben Amotz et al. 1988; Borowitzka andBorowitzka 1990; Schlipalius 1991; Borowitzka 2013b). β-Carotene is the main source of pro-vitamin A and is widelyused as a food colorant, with a global market estimated tosurpass 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 apossibly even larger production system currently beingestablished in Saudi Arabia, a local joint venture with theNational Aquaculture Group. Dunaliella salina productionfor beta-carotene in China was carried out by the Inner Mon-golia Lantai Industrial Co., Ltd (Inner Mongolia) and SaltResearch 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). Theprincipal existing market for astaxanthin is for use as a feedadditive for farmed salmon and trout to pigment the fish flesh,with about 200 t of synthetic astaxanthin sold for about US200million. However, as for natural beta-carotene, currently the

Table 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 is based from Zhang andXue (2012). The annual output was estimated by visiting leadingenterprises and discussing with several leaders of leading enterprises and other methods

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only market for natural astaxanthin from microalgae is forhuman nutritional applications, mainly because of its highselling price, up to about 10,000 kg−1, or almost 10-foldhigher than the current price for synthetic astaxanthin usedin aquaculture. Haematococcus pluvialis production forastaxanthin in China is developing rapidly, mainly in Yunnanand the Hubei Province. There, several dozen companies aredeveloping the production process, though only a handful arecurrently in production including one large operation in Chinausing 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 microalgaespecies are used as aquaculture feeds but only in relatively smallamounts, kilograms not tons. Themain species used are from thegenera such as Nannochloropsis, Pavlova, Isochrysis,Tetraselmis, Thalassiosira, Chaetoceros, and Skeletonema.These are particularly rich in the nutrients required by the larvaland 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 C20 and C22 omega-3fatty acids eicosapentaenoic acid (EPA) and docosahexaenoicacid (DHA) required in fish nutrition. In some cases, the algaeare used to feed rotifers and brine shrimp that are then used tofeed 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 ofprawns, salmonid fish, ornamental fish, and other high-value fish(Priyadarshani and Rath 2012).

The major challenge in aquaculture operations is that forjust hatched and juvenile animals (e.g., hatchery and nurseryoperations), the algal feeds have to be live or at least havedispersed 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 cubicmeters 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, asgrowing 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 requiredis attractive but requires concentrating (e.g., centrifuging to ahigh solids paste) and storing of the algal cells at low temper-atures, typically with a cryoprotectant added, for use whenneeded. This has been a major limitation, as the product hasto be shipped refrigerated and has very limited shelf life. Stor-ing at −18 °C without cryoprotectant can reduce the nutritionloss less than other various cryoprotectants and cooling

methods (Yu et al. 2013). Freeze drying can be used but alsohas some challenges. Some enterprises themselves cultivateand use microalgae biomass to rear rotifers or larvae of marinefinfish and crustaceans. For example, Tianjin Ocean Pal Bio-tech Co., Ltd., a member of CMIA, cultivates Chlorella withseawater in Hainan, to meet their needs in rearing rotiferswhich are then used to feed shrimp larvae.

In 1999, the production of microalgae for aquaculturereached 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 themuch larger-scale production of microalgae to replace aqua-culture feeds currently produced from fish meal and fish oilsthat has the greatest near-term potential for large-scalemicroalgae biomass production. This is a very large, severalmillion tons per year, market with increasingly rising costs forfish meal/oil, currently over US 3000 t−1, and uncertain sup-ply, thus presents a large, highest-value, near-term market forbulk microalgae as aquaculture and animal feeds generally.

Biofuels and CO2 capture and utilization R&D

The National Development and Reform Commission of thePeople’s Republic of China (NDRC) 2007 (http://www.ccch ina .gov.cn /WebSi te /CCChina /UpFi le /2007 /20079583745145.pdf) promulgated the Medium and Long-Term Development Plan for Renewable Energy, whichprojected that the consumption of biodiesel in China couldreach 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 Barbosa2010). Over the past 5 years, the production of biofuel frommicroalgae, in conjunction with CO2 capture and utilization,has also gained increased interest in China. Li et al. (2011)listed a number of research group and corporations activelyinvolved 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 fewexamples:

& Han et al (2012) devised a novel 96-well microplate swiv-el system (M96SS) for high-throughput screening ofmicroalgae strains for CO2 fixation (Han et al. 2012).

& Li et al (2013) designed transparent covers for a racewaypond, which directly touched the surface of culture, andinvestigated CO2 fixation; efficiency increased to 95 %under intermittent gas sparging (Li et al. 2013).

& Yantai Hearol Biology Technology Co., Ltd, a CMIAmember company, was the first commercial plant in theworld using power plant flue gas (CO2 flue gas) for

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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 inChina, as in the whole world, on both the current and alsonew 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&Dongoing. This interest is being driven by the demand of sus-tainable, green energy and products, as well as national objec-tives of reducing CO2 emission from fossil fuels, in particular,coal-fired power plants.

Meanwhile, the more immediate issues currently faced bythe Chinese microalgae industry are public perceptions re-garding the wholesomeness of microalgae foods, as well asthe high costs of production, which limit both domestic orinternational markets. To help address these challenges, theCMIAwas established on December 9, 2010 in Yantai, China,led by a group of Chinese-leading microalgal specialists andenterprise leaders, bringing together industry and researchers.The CMIA now includes 14 leading microalgae-producingenterprises (Table 2). The objective of the CMIA is to addressthese two major challenges in commercial microalgae produc-tion and to the proposed solutions, as discussed next.

Challenge I: the microalgae food standard systemrequired improvement

In China, food standards are the reference points for marketregulation, including safety, quality, production, and other stan-dards (Chen and Li 2014). The National Health and FamilyPlanning Commission of the People’s Republic of China(NHFPC) announced the BFood Standards System ImprovementProjects,^ which include plans for improving quality and safetystandards 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 SafetyStandards Formulated and Revised Proposal^ was publishedby 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 ProductsFood Safety National Standard.^ This standard will be manda-tory, applying to all algae products brought to market, and willensure the safety and quality of microalgae products. Actuallyapplying these standards in the market will be the first challengefor improving public confidence in microalgae products and ad-vancing the development of the Chinese microalgae industry.

Challenge II: production costs cannot meet marketrequirements

There is a strong global market demands of selected microalgalhigh-value products, including carotenoids (beta-carotene, lutein,

Fig. 4 Views ofNannochloropsis pond systemscultivated with flue gas in YantaiHearol Biology Technology Co.,Ltd (photograph downloadedfrom this enterprise’s website)

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astaxanthin), fatty acids (long-chain omega-3, EPA, DHA), andphycobiliproteins (e.g., phycocyanin, etc.) (Borowitzka 2013a;Markou andNerantzis 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 theseproducts are currently available, both synthetic and natural,which limit the potential of microalgae products to small nichemarkets such as vegetarian EPA and DHA (vs. fish oil-derivedproducts) or natural carotenoids (vs. synthetics or even othernatural sources).

Solution I: improving safety and quality standardsnationally and regionally

To improve safety and quality standards is the key strategy tobuild public confidence in microalgae healthy food. The firstthree meetings of CMIA discussed the necessity of improvingsafety and quality standards nationally, regionally, andthrough organization and rules of the CMIA. The fourth meet-ing of the CMIA focused on the quality control of microalgalproducts for sustainable development. Several important pa-rameters of quality control points were determined. The fifthmeeting of the CMIAwas held in Qingdao, with a backgroundof public doubt regarding the biosafety of Spirulina healthyfood, with the CMIA providing a clear voice to the public atthis meeting. In 2014, the eighth meeting was held in Qing-dao, China. This conference reached consensus that BAlgaeand Their Products Food Safety National Standard^ beingdeveloped should also apply for microalgae products not justto macroalgal products, and the CMIA submitted several ad-visories, which include quality testing data and current marketstatutes.

The CMIA is also currently improving the Food GradeSpirulina Powders Quality National Standard to keep the pacewith market developments. To improve these standards scien-tifically, many algae researchers in the CMIA test the qualityof Spirulina dry powders as a public service.

& Lirong Song’s research group (Institute Hydrobiology,Chinese Academy of Sciences) tested microcytic toxins.

& Xiaojun Yan’s research group (Ningbo University) testedcarotenoid content.

& Song Qin’s research group (Yantai Institute of CoastalZone Research, Chinese Academy of Sciences) tested wa-ter, heavy metals (lead, mercury, cadmium, arsenic), andphycocyanin contents.

Regional quality standards will be advanced for continuingsustainable development of the microalgae healthy food in-dustry in China.

Solution II: promoting technology innovation

Promoting technology innovation will be important formicroalgae industry transformation and upgrading, such as

Table 2 Leading enterprises in the Chinese Microalgae IndustryAlliance

Enterprise Location Products

Beihai SBD bio sciencetechnology Co., Ltd

Guangxi Food grade: Spirulinapowders and tables

C.B.N Spirulina group Co.,Ltd

Jiangsu Food grade: Spirulinapowders, tables Chlorellapowders or tablets,phycocyanin, Spirulinapolysaccharide

King Dnarmsa SpirulinaCo., Ltd

Hainan,Fujian,Jiangxi

Food grade: spirulinapowders and tablesChlorella powders ortablets, phycocyanin

Inner Mongolia RejuvBiotech Co., Ltd

InnerMongolia

Food grade: Spirulinapowders, tablets, capsules

Sanya Neptunus MarineBiological TechnologyCo., Ltd

Hainan Food grade: seawaterSpirulina powders,seawater Spirulinatablets, Spirulinapolysaccharide

Feed grade: seawaterChlorella biomass,seawater Chlorellaconcentrated solution

Yantai Hearol BiologyTechnology Co., Ltd

Shandong Feed grade:Nannochloropsisoceanica powders andNannochloropsisoceanica concentratedsolution

Zhongsan Lanzao BiologyFood Co., Ltd

Guangxi Food grade: Spirulinapowders and tablets

Chenghai Baoer BiologicalDevelopment Co., Ltd

Yunnan Food grade: spirulinaSpirulina powders andtablets

Guangxi AgriculturalReclamation LvxianBiology healthy food Co.,Ltd

Guangxi Food grade: Spirulinapowders and tablets

Dongying DiazenBiological EngineeringCo., Ltd

Shandong Food grade: Spirulinatablets; Feed grade:seawater Chlorellaconcentrated solution

Dongying Haifu BiologicalEngineering Co., Ltd

Shandong Food grade: Spirulinatablets and someSpirulina compositedfood, Spirulina capsule

Inner Mongolia MeangjialiSpirulina Co., Ltd

InnerMongolia

Food grade: Spirulinapowders and tablets

Shandong Tianshunpharmacy Co., Ltd

Shandong Pharmaceutical grade:Spirulina tablet, Spirulinacapsule;

Tianjing Ocean Pal CarolBiotech Co., Ltd

Hainan Feed grade: Chlorellaconcentrated solution

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further process improvements and value-added products, andmost 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 plantand 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 surfaceanalysis (Shao et al. 2013a), their purification by a single stepchromatography (Shao et al. 2013b), and the antioxidant pep-tides from phycobilins by an enzymatic process (Tang et al.2012); phycocyanin microcapsules extrusion using alginateand chitosan as coating materials (Yan et al. 2014). The pat-en t s o f the p roduc t ion me thods o f food gradephycobiliproteins on plant scale has been used by acooperating enterprise, C.B.N. Spirulina Co., Ltd., and obtain-ed good economic effects.

For another example, Wei Cong’s research group (in Bei-jing) designed and developed an economical device for CO2

supplementation in large-scale microalgae production, and thegaseous absorptivity was enhanced to nearly 80 % (Su et al.2008). Then, they estimated the effects of initial total carbonconcentrations, suspension depths, and pH values on the CO2

absorptivity. The results indicated that an average CO2 absorp-tivity of 86 % and CO2 utilization efficiency of 79 % wereachieved using this device in large-scale cultivation ofSpirulina, with an initial total carbon concentration of0.06 mol L−1 and pH 9.8 (Bao et al. 2012).

Yuanguang Li’s research group (in Shanghai) investigatedthat the effects of temperature on the variations of biomassconcentration, lipid content, and fatty acid composition forproduction of biofuels under a light-dark cyclic culture ofChlorella pyrenoidosa cooperated with the Jiaxing ZeyuanBio-products Co., Ltd. (Jiaxing, Zhejiang province). The re-sults showed that by keeping culture broth at above 30 °Cduring the daytime, net biomass and lipid productivity was

increased by about 38 and 45 %, respectively (Han et al.2013).

Tianzhong Liu’s team (in Qingdao) invented an attachedcultivation technology for production of microalgae biofuelswith microalgae cells growing on the surface of vertical arti-ficial supporting material to form an algal biofilm. Multiplesuch algal biofilms were assembled in an array fashion todilute solar irradiation thus facilitating high photosyntheticefficiency (Liu et al. 2013). They also investigated methodsof CaCO3 addition and intermittent sparging, finding thatthese have great potential to overcome the inhibition of fluegas for cultivation of Scenedesmus dimorphus (Jiang et al.2013).

As a final example, one reaching large-scale production,Jianguo Liu’s research group (in Qingdao) designed a photobioreactor for a pilot-scale culture of H. pluvialis, and thetechnology has been used in Yunna Alphy Biotech Co., Ltd.to produce astaxanthin, enhancing the production efficiency inH. pluvialis of about 35-fold above the traditional method(Fig. 5) (Liu et al. 2006).

Conclusion: microalgae for sustainable development

Increasing microalgae markets are necessary to promotemicroalgae’s sustainable development. In 2014, the seventhCMIA meeting was held in Tianjin, China. This meetingmainly focused on the necessity, feasibility, and key technol-ogies and difficulties of producing microalgae as feeds/dietsfor aquaculture animals. Six roundtables discussed the nutri-ent evaluation of Spirulina, Chlorella, and other microalgaefor use as aquaculture feeds, how to reduce the costs ofmicroalgae feeds production, and the logistics of microalgaeaquaculture feeds. The meeting made achieving 3000 tmicroalgae biomass with the cost being about US3000 t−1

for the aquaculture market as a goal. Reducing the cost and

Fig. 5 Views of Haematococcuspluvialis production withphotobioreactors in YunnanProvince (supplied by Prof.Jianguo Liu )

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enhancing the biomass quality remain as the key issue for themicroalgae industry. When the output of microalgae biomassachieves between 0.1 and 1 million ton, microalgae biomasswill become a clear vision as a key protein resource for humanpopulation. When the output of microalgae biomass reaches 1to 10million tons, microalgae biomass will become a strategicfood and feed resource.

In the past 30 years, the Chinese microalgae industry hasincreased influence on the world microalgae industry. TheBMicroalgae Dream of Chinese People^ is to provide healthyfood for people directly or indirectly, fix carbon dioxide, andreduce eutrophication, promoting microalgae to keep the pacewith evolution of our earth friendly. Institution building, re-search progress, technological development, and microalgaeculture system construction could be the important impetus forthe sustainable development of the microalgae industry.

Acknowledgments This work was supported by the National NaturalScience Foundation of China (408760862) and Public Science and Tech-nology Research Funds Projects of the Ocean (201205027). We also wishto thank Inner Mongolia Rejuv Biotech Co. Ltd and Yantai Hearol Biol-ogy Technology Co. Ltd for permitting us to use the pictures in Figs. 2and 4. We are grateful to King Dnarmsa Spirulina Co. Ltd for supplyingus the pictures Fig. 3 and Prof. Jianguo Liu (Institute of Oceanology,Chinese Academy of Sciences, Qingdao) for supplying us Fig. 5.

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