Microalgal Industry in China: Challenges and Prospects

J Appl Phycol DOI 10.1007/s10811-015-0720-4

1ST INTERNATIONAL COASTAL BIOLOGY CONGRESS, YANTAI, CHINA

Microalgal industry in China: challenges and prospects

Jun Chen1,2 & Yan Wang1 & John R. Benemann3 & Xuecheng Zhang 4 & 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 major pharmaceuticals to biofuels and CO2 capture and utilization. This producer of microalgal biomass in the world. Spirulina paper briefly reviews the main challenges and potential solutions (Arthrospira) is the largest microalgal product by tonnage and for expanding commercial microalgae production in China and value, followed by Chlorella, Dunaliella,andHaematococcus, the markets for microalgae products. The Chinese Microalgae the four main microalgae grown commercially. China’s produc- Industry Alliance (CMIA), a network founded by Chinese tion is estimated at about two-thirds of global microalgae bio- microalgae researchers and commercial enterprises, supports this mass of which roughly 90 % is sold for human consumption as industry by promoting improved safety and quality standards, human nutritional products (‘nutraceuticals’), with smaller mar- and advancement of technologies that can innovate and increase kets in animal feeds mainly for marine aquaculture. Research is the markets for microalgal products. Microalgae are a growing also ongoing in China, as in the rest of the world, for other high- source of human nutritional products and could become a future value as well as commodity microalgal products, from source of sustainable commodities, from foods and feeds, to, possibly, fuels and fertilizers.

* Song Qin Keywords Microalgae . Spirulina . Chlorella . Dunaliella . [email protected] Haematococcus . Nutritional products . Microalgae mass Jun Chen culture [email protected] Yan Wang [email protected] Introduction John R. Benemann [email protected] Microalgae are microscopic plants that typically grow Xuecheng Zhang suspended in water using photosynthesis to convert sunlight, [email protected] water, CO2,andinorganicnutrients(N,P,K,etc.)intoO2 and a Hongjun Hu biomass high in protein, vitamins, antioxidants, and other nu- [email protected] trients required by humans and animals. Some microalgae can also grow heterotrophically by fermentation in the dark using 1 Yantai Institute of Coastal Zone Research, Chinese Academy of sugars and other organic substrates. Thousands of microalgal Sciences, 17 Chunhui Road, Laishan District, Yantai 264003, China species are described in the literature, but only a handful of 2 University of Chinese Academy of Sciences, Beijing, China genera and species are currently produced commercially pho- 3 MicroBio Engineering, Inc, PO Box 15821, San Luis tosynthetically namely Spirulina, a cyanobacterium (a prokary- Obispo, CA 93406, USA ote, scientific name Arthrospira, with the two species cultivated 4 Ocean University of China, 238 Songling Road, Laoshan District, commercially, A. platensis and A. maxima) and four genera that Qingdao 266100, China belong to the eukaryotic green algae (Chlorophyceae): Chlorel- 5 Wuhan Botanical Garden, Chinese Academy of Sciences, 1 Lumo la vulgaris and C. pyrenoidosa, Dunaliella salina,and Road, Hongshan District, Wuhan 430074, China Haematococcus pluvialis. J Appl Phycol

Chlorella is also produced commercially in several coun- high value specialties, such as human nutritional products, tries, including China, both by photosynthesis (‘autotrophic’) coloring agents, the long-chain omega-3 fatty acids (DHA, and fermentation (‘heterotrophic’, on sugars in the dark in EPA), and also lower-value bulk commodities with extensive sterilized reactors) (Shi et al. 1999; Ip and Chen 2005; Wang R&D ongoing in all areas of this field. The Chinese and Peng 2008; Han et al. 2013). Chlorella production by Microalgae Industry Alliance (CMIA) was formed to bring fermentation processes has recently expanded with two major together industry and researchers in advancing this industry US and European companies, Solazyme (in the USA) and as discussed herein. First, the current status of this industry is Roquette (in France), now offering human nutritional and bulk reviewed. food ingredients. The non-photosynthetic dinoflagellate Crypthecodinium cohnii, a source of the long-chain polyun- saturated fatty acid (LC-PUFA) docosahexaenoic acid (DHA) Spirulina (Arthrospira) production used in infant formula, is another alga produced by fermentations in the dark on sugars, including in China (Jiang et al. The largest, by tonnage, commercially produced microalgae 1999; Wynn et al 2005). However, such dark fermentation in China and in the world is Spirulina (A. platensis and processes are not discussed in this review and neither is A. maxima), a filamentous cyanobacterium (e.g., a prokaryote) mixotrophic production, in which microalgae are grown with multicellular spiral shaped filaments. This microalga has mixotrophically using both sunlight and organic substrates, many favorable properties for both cultivation and as both such as acetate, glycerol, or sugars. Mixotrophic processes re- human and animal feeds. Spirulina is cultivated in highly quire sterilized enclosed photobioreactors (PBRs), which can- alkaline medium, typically 16 g L-1 of bicarbonate, which not be scaled-up to production scale due to high costs. The minimizes contamination by other algae. The filamentous spi- focus herein is on the current and potential commercial produc- ral shape makes it easy to harvest with relatively large opening tion of microalgae in China using sunlight energy and CO2. screens. Spirulina is also quite digestible by humans and an- Microalgae grown photosynthetically are sources of carbo- imals, requiring no cell breakage. It is rich in proteins (typi- hydrates, protein, oils, and essential nutrients such as vita- cally about 50 %), vitamins, essential amino acids, minerals, mins, minerals, carotenoids, long-chain omega-3 fatty acids, and essential fatty acids such as γ-linolenic acid (GLA), vita- and other phytonutrients. For example, Chlorella contains the min B12, carotenoids, and other antioxidants such phycocya- so-called Chlorella growth factor (CGF), which can be isolat- nin, already mentioned as above, and other phycobiliproteins ed from this alga by hot water extraction and is sold commer- (Belay et al. 1993;Hu2003; Ali and Saleh 2012;Belay2013; cially as a health-promoting product (Tang and Suter 2011). Holman and Malau-Aduli 2013). Spirulina contains the so-called “calcium spirulin”, a sulfated Spirulina was first cultivated in China in 1970s, but the polysaccharide, and phycocyanin, a protein, both thought to limitations of the technology at that time did not lead to have health-promoting effects. Phycocyanin is also used as large-scale production. The first national science and technol- food colorant, recently permitted in both Europe and the ogy research project to develop microalgae resources was USA. Dunaliella salina and Haematococcus pluvialis are funded only in 1986, the first Spirulina experimental base commercial sources of the antioxidants carotenoids beta- set up in Chenghai Lake, Yong-shen County, Yunnan Prov- carotene (also a pro-vitamin A) and astaxanthin, respectively ince in 1989 (Li and Qi 1997), and the first commercial (Borowitzka 2013a). These microalgal carotenoid products are Spirulina production by the Shenzhen Lanzao Biotech Corpo- sold as both whole biomass and extracts, in the form of dry ration founded in 1991 and continuing to operate at present powders, tablets, and oils, the latter typically as soft gel capsules. (Liang et al. 2004). Since then, Spirulina plants have been Microalgae can be cultivated on either fresh, brackish, or established in almost every province or region, from the south- seawater, with agricultural fertilizers as nutrients and carbon ern Hainan to Inner Mongolia and from Yunnan to Zhejiang sources either as CO2 bubbled into the cultures or from added (Fig. 1) (Lu et al. 2011). bicarbonate or even from air. Both Spirulina and Chlorella are Zhang and Xue (2012) estimated that more than 60 cultivated in China using paddle wheel mixed raceway ponds. Spirulina plants with 7,500,000 m2 (750 ha) of cultivation Commercial production using PBRs is currently limited to the base produced 9600 t dry powders per year in China with an production of H. pluvialis for the carotenoid astaxanthin. Here, annual retail value of over four billion Yuan per year (about we review the production of these algae with emphasis on pro- US650 million). This would suggest a productivity of about duction in China. It must be noted, however, at the outset, that it 13 t ha−1 year−1 of biomass and about 70 kg−1 for the products is difficult to obtain specific data on volumes, prices, and markets sold to consumers. Plant production costs would very be gen- for any of the microalgae products; thus, the data provided in the erally about a tenth of retail value, which increases when it following are only the best estimates by the authors. reaches the consumer to account for operating margins, return There is increasing interest in China, as in the world, in on investment, marketing, formulating (e.g., tableting, etc.), both the established and also new microalgae products, both packaging, shipping, distribution, advertising, retail sales, J Appl Phycol

Fig. 1 Location of Spirulina cultivation base in China (the information collected by many methods, including field survey, searches from the Internet, and others) taxes, etc. Of course, these are very approximate estimates. It Spirulina was cultivated in north China only from May to should be noted that Spirulina production in China is still the beginning of October, such as in Inner Mongolia and the growing rapidly, close to 10 % per annum. China is now the Heilongjiang province, while in Hainan, Guangdong, and largest Spirulina producer worldwide with about two-thirds of Guangxi, it was cultivated all year round (see Table 1 for total global production. The bulk of Spirulina production is details on Spirulina production in China). sold internally in China with also some exports. Most Spirulina production in China has used a combina-

The details of the cultivation process for Spirulina differ in tion of bicarbonate and air for the required CO2 supply, while the geographic regions of China, though all production uses Chlorella production requires CO2 fertilization, provided as raceway paddle wheel mixed ponds. In the north, Inner Mon- compressed, liquefied CO2 from commercial sources golia has become one of the most important centers for com- (Bmerchant CO2^). It is likely that merchant CO2 is also in- mercial production of Spirulina with an output estimated at creasingly being used for Spirulina production as the cost of about 3000 t year−1 of dry biomass powder. Due to the local bicarbonate has greatly increased, and a significant increase in climate, the production system uses raceway ponds under productivity can be obtained with such supplemental CO2. plastic greenhouses (Fig. 2). This is also the case for other Spirulina production requires high bicarbonate concentra- Spirulina production facilities in north and central China, such tions, 16 g L−1, to maintain pure culture (e.g., to limit invasion as Heilongjiang province. By contrast, in the south of China, by other microalgae, grazers, etc.). Thus, for a 20-cm deep for example in Fujian, Yunnan, Guangdong and Hainan prov- pond, 32 t ha−1 is needed to start up production. However, this inces with higher year-round temperatures, the production can be extensively recycled as long as CO2 is supplied from a systems use open-air raceway ponds without covering the concentrated source, in which the 32-t bicarbonate can be greenhouses (Fig. 3). Zhang and Xue (2012) reported that replaced with only 20 t of the less expensive sodium J Appl Phycol

Fig. 2 Views of Spirulina production pond systems in Inner Mongolia (photograph by John R. Benemann)

carbonate. This has been the practice in the USA and other Recently, there has been increasing interest in the use of countries for Spirulina production since the start of the indus- Spirulina for aquaculture feeds (Burr et al. 2012), as it is try 30 years ago, and is likely that this process will be increas- reported to benefit fish health, improve growth, and reduce ingly adopted in China, as once-through bicarbonate utiliza- mortality. However, the current price is too high for wide tion becomes more costly. applications as aquaculture or animal feeds. Almost all of the production of Spirulina is used for human Spirulina contains, as noted already, phycocyanin, a blue consumption as nutritional supplements (Bnutraceuticals^). protein that has been sold for over 30 years in Japan as a food Spirulina biomass is typically produced as a spray dried pow- coloring agent. Phycocyanin has been extensively commer- der and generally sold and mostly used as such by consumers cialized as a colorant in food such as chewing gum, dairy in China who typically add it to fruit juices or other foods. products, jellies, and other food products (Santiago-Santos Algal powders are also converted into tablets and capsules. et al. 2004; Sekar and Chandramohan 2008). Phycocyanin is Relatively smaller amounts are used for animal feeds; mainly also used as fluorescent agents applied in flow cytometry and ornamental fish feeds (e.g., Koi, tropical aquarium fish). immunological analysis (Glazer 1994) and pharmaceuticals

Fig. 3 Views of Spirulina production pond systems in the Hainan Province (photograph supplied by King Dnarmsa Spirulina Co., Ltd) J Appl Phycol

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 and Xue (2012). The annual output was estimated by visiting leading enterprises and discussing with several leaders of leading enterprises and other methods

(Hu et al. 2008). Phycocyanin was recently approved for food potential applications in replacing conventional wheat flours coloring in Europe and the USA, and that is now leading to in dietary (weight loss) products, a potentially very large rapidly increasing production of this protein with markets be- market. ing developed for the residual biomass (about 90 % of total) in aquaculture feeds. The isolation and commercial production of high-value products from Spirulina, including Dunaliella and Haematococcus production phycobiliproteins, peptides, and polysaccharides, is the sub- ject of a currently ongoing multi-laboratory projects funded by The other two microalgae grown commercially with sunlight the Chinese Government. are Dunaliella (grown at very high salinity) and Haematococcus (a freshwater species) with high-value carotenoids extracted from their biomass, beta-carotene, and astaxanthin, respectively. Chlorella production Dunaliella was first commercialized in Australia and Israel in the 1980s (Ben Amotz et al. 1988; Borowitzka and Chlorella was first cultivated commercially in Japan and also Borowitzka 1990; Schlipalius 1991; Borowitzka 2013b). β- in China in the 1960s, earlier than Spirulina,butthelimita- Carotene is the main source of pro-vitamin A and is widely tions of the technology at that time did not lead to large-scale used as a food colorant, with a global market estimated to production in China. Over the past decade, China has also surpass US280 million in 2015 (Ribeiro et al. 2011). Howev- become the major worldwide producer of Chlorella,overtak- er, this is for synthetic beta-carotene. BASF (a German chem- ing the traditional production in Japan. Chlorella production is ical company) is the undisputed world leader in natural beta- overall considerably smaller in volume than that of Spirulina, carotene production from Dunaliella salina, with over a thou- probably a quarter, but price per ton is significantly higher. sand hectares of production ponds in two plants in Australia Many of the Spirulina production enterprises produce (acquired as part of its take over a few years ago of Cognis) Chlorella alongside with Spirulina, generally as a smaller part (Borowitzka 2013b). BASF has announced expansion with a of the larger Spirulina production process. Chlorella is a tech- possibly even larger production system currently being nically more challenging and expensive production process, established in Saudi Arabia, a local joint venture with the compared to Spirulina, due to greater potential for contamina- National Aquaculture Group. Dunaliella salina production tion and the need for centrifuges for harvesting these micro- for beta-carotene in China was carried out by the Inner Mon- scopic cells. This contrasts to the easier harvesting of the fil- golia Lantai Industrial Co., Ltd (Inner Mongolia) and Salt amentous Spirulina and fewer problems of contamination due Research Institute, China National Salt Industry Corp to the high bicarbonate growth medium. (Tianjin) (Yin et al. 2013). There is little information on Chlorella production in Chi- Haematococcus was commercialized for astaxanthin in Is- na—centrifugation is used to harvest the algal biomass, and rael and USA (Boussiba 2000; Lorenz and Cysewski 2000) CO2 is used to provide the carbon. Chlorella is spray dried and and is now also ongoing in China (http://www.algachina.com; sold similarly to Spirulina, as a human nutritional supplement, http://www.e-asta.cn; http://www.astawefirst.com). The both as a powder and in tablet and capsule form. The so-called principal existing market for astaxanthin is for use as a feed CGF extract is also mentioned. Chlorella decolorized protein additive for farmed salmon and trout to pigment the fish flesh, powders have recently been developed, although thus far only with about 200 t of synthetic astaxanthin sold for about US200 from biomass produced by dark fermentations, that have million. However, as for natural beta-carotene, currently the J Appl Phycol only market for natural astaxanthin from microalgae is for methods (Yu et al. 2013). Freeze drying can be used but also human nutritional applications, mainly because of its high has some challenges. Some enterprises themselves cultivate selling price, up to about 10,000 kg−1, or almost 10-fold and use microalgae biomass to rear rotifers or larvae of marine higher than the current price for synthetic astaxanthin used finfish and crustaceans. For example, Tianjin Ocean Pal Bio- in aquaculture. Haematococcus pluvialis production for tech Co., Ltd., a member of CMIA, cultivates Chlorella with astaxanthin in China is developing rapidly, mainly in Yunnan seawater in Hainan, to meet their needs in rearing rotifers and the Hubei Province. There, several dozen companies are which are then used to feed shrimp larvae. developing the production process, though only a handful are In 1999, the production of microalgae for aquaculture currently in production including one large operation in China reached reportedly 1000 t (about 62 % for molluscs, 21 % using PBRs, such as Yunnan Alphy Biotech Co. Ltd for shrimps, and 16 % for fish) (Hemaiswarya et al. 2011), (Chuxiong, in Yunnan province) (Fig. 5). though this figure is likely a high estimate. However, it is the much larger-scale production of microalgae to replace aquaculture feeds currently produced from fish meal and fish oils Microalgae for aquaculture feeds that has the greatest near-term potential for large-scale microalgae biomass production. This is a very large, several Microalgae are also of great importance and interest as aquacul- million tons per year, market with increasingly rising costs for ture feeds (Benemann 1992). A number of marine microalgae fish meal/oil, currently over US 3000 t−1, and uncertain sup- species are used as aquaculture feeds but only in relatively small ply, thus presents a large, highest-value, near-term market for amounts, kilograms not tons. The main species used are from the bulk microalgae as aquaculture and animal feeds generally. genera such as Nannochloropsis, Pavlova, Isochrysis, Tetraselmis, Thalassiosira, Chaetoceros, and Skeletonema. These are particularly rich in the nutrients required by the larval Biofuels and CO2 capture and utilization R&D and juvenile stages of the fish, penaeid shrimp and other crustaceans, molluscs, etc., being raised by the aquaculture operations. The National Development and Reform Commission of the

Of particular interest are the long-chain C20 and C22 omega-3 People’s Republic of China (NDRC) 2007 (http://www. fatty acids eicosapentaenoic acid (EPA) and docosahexaenoic ccchina.gov.cn/WebSite/CCChina/UpFile/2007/ acid (DHA) required in fish nutrition. In some cases, the algae 20079583745145.pdf) promulgated the Medium and Long- are used to feed rotifers and brine shrimp that are then used to Term Development Plan for Renewable Energy, which feed the juvenile animals (Borowitzka 1997; Hemaiswarya et al. projected that the consumption of biodiesel in China could 2011). Microalgae, in larger quantities, in particular Spirulina, reach two million tons in 2020. Microalgae biodiesel produc- are also used as a source of natural pigments for the culture of tion has been suggested to have the advantage of greatly ex- prawns, salmonid fish, ornamental fish, and other high-value fish ceeding the productivity of agricultural oleaginous crops, (Priyadarshani and Rath 2012). without competing for arable land (Wijffels and Barbosa The major challenge in aquaculture operations is that for 2010). Over the past 5 years, the production of biofuel from just hatched and juvenile animals (e.g., hatchery and nursery microalgae, in conjunction with CO2 capture and utilization, operations), the algal feeds have to be live or at least have has also gained increased interest in China. Li et al. (2011) dispersed unicellular dispersions and cannot be spray-dried, listed a number of research group and corporations actively and even freeze drying is often not successful. Thus, typically, involved in this research in detail (Li et al. 2011). microalgae are produced on-site as needed, in a few cubic However, there is an increasing amount of published infor- meters of culture, and then fed directly, without harvesting, mation in peer-reviewed publications that provides informa- to the fish, shrimp, or bivalve larval and juvenile cultures, tion on the advances being made. The following are few which require live microalgae feeds. This has been, however, examples: a major bottleneck for aquaculture operations worldwide, as growing the algae when needed, at the right time, and in suf- & Han et al (2012) devised a novel 96-well microplate swiv- ficient amounts has proven challenging. Thus, producing al- el system (M96SS) for high-throughput screening of gae remotely and shipping them to where and when required microalgae strains for CO2 fixation (Han et al. 2012). is attractive but requires concentrating (e.g., centrifuging to a & Li et al (2013) designed transparent covers for a raceway high solids paste) and storing of the algal cells at low temper- pond, which directly touched the surface of culture, and atures, typically with a cryoprotectant added, for use when investigated CO2 fixation; efficiency increased to 95 % needed. This has been a major limitation, as the product has under intermittent gas sparging (Li et al. 2013). to be shipped refrigerated and has very limited shelf life. Stor- & Yantai Hearol Biology Technology Co., Ltd, a CMIA ing at −18 °C without cryoprotectant can reduce the nutrition member company, was the first commercial plant in the loss less than other various cryoprotectants and cooling world using power plant flue gas (CO2 flue gas) for J Appl Phycol

microalgae cultivation and the first to produce the seawa- Challenge I: the microalgae food standard system ter Nannochloropsis commercially, selling into the aqua- required improvement culture market (Fig. 4). In China, food standards are the reference points for market regulation, including safety, quality, production, and other standards (Chen and Li 2014). The National Health and Family Planning Commission of the People’s Republic of China The Chinese Microalgae Industry Alliance (CMIA) (NHFPC) announced the BFood Standards System Improvement Projects,^ which include plans for improving quality and safety There is increasing interest and intensive R&D ongoing in standards for agricultural products and food hygienic, quality, China, as in the whole world, on both the current and also and industrial standards in 2012 (http://www.moh.gov.cn/sps/ new microalgae products, both high-value specialty products, s3594/201210/fc63695b7417477eac341507854f8525.shtml). such as the current human nutritional products and lower val- After 2 years of deliberation, the BNational Food Safety ue commodities, such as feeds and fuels, with extensive R&D Standards Formulated and Revised Proposal^ was published ongoing. This interest is being driven by the demand of sus- by the NHFPC in 2014 (http://www.nhfpc.gov.cn/sps/s3593/ tainable, green energy and products, as well as national objec- 201309/50799b73ad7c49c482da524231523573.shtml). tives of reducing CO2 emission from fossil fuels, in particular, According to this proposal, BAlgae Products Hygienic Standard^ coal-fired power plants. should be improved and re-named as BAlgae and Their Products Meanwhile, the more immediate issues currently faced by Food Safety National Standard.^ This standard will be manda- the Chinese microalgae industry are public perceptions re- tory, applying to all algae products brought to market, and will garding the wholesomeness of microalgae foods, as well as ensure the safety and quality of microalgae products. Actually the high costs of production, which limit both domestic or applying these standards in the market will be the first challenge international markets. To help address these challenges, the for improving public confidence in microalgae products and ad- CMIAwas established on December 9, 2010 in Yantai, China, vancing the development of the Chinese microalgae industry. led by a group of Chinese-leading microalgal specialists and enterprise leaders, bringing together industry and researchers. Challenge II: production costs cannot meet market The CMIA now includes 14 leading microalgae-producing requirements enterprises (Table 2). The objective of the CMIA is to address these two major challenges in commercial microalgae produc- There is a strong global market demands of selected microalgal tion and to the proposed solutions, as discussed next. high-value products, including carotenoids (beta-carotene, lutein,

Fig. 4 Views of Nannochloropsis pond systems cultivated with flue gas in Yantai Hearol Biology Technology Co., Ltd (photograph downloaded from this enterprise’swebsite) J Appl Phycol

Table 2 Leading enterprises in the Chinese Microalgae Industry such high-value products are still too high to meet most require- Alliance ments from domestic and international markets for larger vol- Enterprise Location Products umes at lower prices. Alternative, lower-cost sources for these products are currently available, both synthetic and natural, Beihai SBD bio science Guangxi Food grade: Spirulina which limit the potential of microalgae products to small niche technology Co., Ltd powders and tables markets such as vegetarian EPA and DHA (vs. fish oil-derived C.B.N Spirulina group Co., Jiangsu Food grade: Spirulina products) or natural carotenoids (vs. synthetics or even other Ltd powders, tables Chlorella powders or tablets, natural sources). phycocyanin, Spirulina polysaccharide Solution I: improving safety and quality standards King Dnarmsa Spirulina Hainan, Food grade: spirulina nationally and regionally Co., Ltd Fujian, powders and tables Jiangxi Chlorella powders or tablets, phycocyanin To improve safety and quality standards is the key strategy to Inner Mongolia Rejuv Inner Food grade: Spirulina build public confidence in microalgae healthy food. The first Biotech Co., Ltd Mongolia powders, tablets, capsules three meetings of CMIA discussed the necessity of improving Sanya Neptunus Marine Hainan Food grade: seawater safety and quality standards nationally, regionally, and Biological Technology Spirulina powders, through organization and rules of the CMIA. The fourth meet- Co., Ltd seawater Spirulina ing of the CMIA focused on the quality control of microalgal tablets, Spirulina polysaccharide products for sustainable development. Several important pa- Feed grade: seawater rameters of quality control points were determined. The fifth Chlorella biomass, meeting of the CMIAwas held in Qingdao, with a background seawater Chlorella of public doubt regarding the biosafety of Spirulina healthy concentrated solution food, with the CMIA providing a clear voice to the public at Yantai Hearol Biology Shandong Feed grade: Technology Co., Ltd Nannochloropsis this meeting. In 2014, the eighth meeting was held in Qing- oceanica powders and dao, China. This conference reached consensus that BAlgae Nannochloropsis and Their Products Food Safety National Standard^ being oceanica concentrated developed should also apply for microalgae products not just solution to macroalgal products, and the CMIA submitted several ad- Zhongsan Lanzao Biology Guangxi Food grade: Spirulina Food Co., Ltd powders and tablets visories, which include quality testing data and current market Chenghai Baoer Biological Yunnan Food grade: spirulina statutes. Development Co., Ltd Spirulina powders and The CMIA is also currently improving the Food Grade tablets Spirulina Powders Quality National Standard to keep the pace Guangxi Agricultural Guangxi Food grade: Spirulina with market developments. To improve these standards scien- Reclamation Lvxian powders and tablets tifically, many algae researchers in the CMIA test the quality Biology healthy food Co., Ltd of Spirulina dry powders as a public service. Dongying Diazen Shandong Food grade: Spirulina Biological Engineering tablets; Feed grade: & Lirong Song’s research group (Institute Hydrobiology, Co., Ltd seawater Chlorella Chinese Academy of Sciences) tested microcytic toxins. concentrated solution & Xiaojun Yan’s research group (Ningbo University) tested Dongying Haifu Biological Shandong Food grade: Spirulina Engineering Co., Ltd tablets and some carotenoid content. Spirulina composited & Song Qin’s research group (Yantai Institute of Coastal food, Spirulina capsule Zone Research, Chinese Academy of Sciences) tested wa- Inner Mongolia Meangjiali Inner Food grade: Spirulina ter, heavy metals (lead, mercury, cadmium, arsenic), and Spirulina Co., Ltd Mongolia powders and tablets phycocyanin contents. Shandong Tianshun Shandong Pharmaceutical grade: pharmacy Co., Ltd Spirulina tablet, Spirulina Regional quality standards will be advanced for continuing capsule; sustainable development of the microalgae healthy food in- Tianjing Ocean Pal Carol Hainan Feed grade: Chlorella Biotech Co., Ltd concentrated solution dustry in China.

Solution II: promoting technology innovation astaxanthin), fatty acids (long-chain omega-3, EPA, DHA), and phycobiliproteins (e.g., phycocyanin, etc.) (Borowitzka 2013a; Promoting technology innovation will be important for Markou and Nerantzis 2013). However, production costs of even microalgae industry transformation and upgrading, such as J Appl Phycol further process improvements and value-added products, and increased by about 38 and 45 %, respectively (Han et al. most importantly, lower-cost production. The CMIA has sup- 2013). plied various platforms for members to achieve a fast trans- Tianzhong Liu’s team (in Qingdao) invented an attached formation from test tube in the laboratory to production plant cultivation technology for production of microalgae biofuels and markets. with microalgae cells growing on the surface of vertical arti- For example of such research applied to microalgae pro- ficial supporting material to form an algal biofilm. Multiple duction, this laboratory in Yantai, developed methods for ex- such algal biofilms were assembled in an array fashion to traction of phycobilins from Spirulina by response surface dilute solar irradiation thus facilitating high photosynthetic analysis (Shao et al. 2013a), their purification by a single step efficiency (Liu et al. 2013). They also investigated methods chromatography (Shao et al. 2013b), and the antioxidant pep- of CaCO3 addition and intermittent sparging, finding that tides from phycobilins by an enzymatic process (Tang et al. these have great potential to overcome the inhibition of flue 2012); phycocyanin microcapsules extrusion using alginate gas for cultivation of Scenedesmus dimorphus (Jiang et al. and chitosan as coating materials (Yan et al. 2014). The pat- 2013). ents of the production methods of food grade As a final example, one reaching large-scale production, phycobiliproteins on plant scale has been used by a Jianguo Liu’s research group (in Qingdao) designed a photo cooperating enterprise, C.B.N. Spirulina Co., Ltd., and obtain- bioreactor for a pilot-scale culture of H. pluvialis, and the ed good economic effects. technology has been used in Yunna Alphy Biotech Co., Ltd. For another example, Wei Cong’sresearchgroup(inBei- to produce astaxanthin, enhancing the production efficiency in jing) designed and developed an economical device for CO2 H. pluvialis of about 35-fold above the traditional method supplementation in large-scale microalgae production, and the (Fig. 5)(Liuetal.2006). 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 CO2 Conclusion: microalgae for sustainable development absorptivity. The results indicated that an average CO2 absorptivity of 86 % and CO2 utilization efficiency of 79 % were Increasing microalgae markets are necessary to promote achieved using this device in large-scale cultivation of microalgae’s sustainable development. In 2014, the seventh Spirulina, with an initial total carbon concentration of CMIA meeting was held in Tianjin, China. This meeting 0.06 mol L−1 and pH 9.8 (Bao et al. 2012). mainly focused on the necessity, feasibility, and key technol- Yuanguang Li’s research group (in Shanghai) investigated ogies and difficulties of producing microalgae as feeds/diets that the effects of temperature on the variations of biomass for aquaculture animals. Six roundtables discussed the nutri- concentration, lipid content, and fatty acid composition for ent evaluation of Spirulina, Chlorella, and other microalgae production of biofuels under a light-dark cyclic culture of for use as aquaculture feeds, how to reduce the costs of Chlorella pyrenoidosa cooperated with the Jiaxing Zeyuan microalgae feeds production, and the logistics of microalgae Bio-products Co., Ltd. (Jiaxing, Zhejiang province). The re- aquaculture feeds. The meeting made achieving 3000 t sults showed that by keeping culture broth at above 30 °C microalgae biomass with the cost being about US3000 t−1 during the daytime, net biomass and lipid productivity was for the aquaculture market as a goal. Reducing the cost and

Fig. 5 Views 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 Chen JW, Li BZ (2014) China’s food safety standard system: problems – microalgae industry. When the output of microalgae biomass and solutions. Food Sci 35(9):334 338 (in Chinese) Glazer AN (1994) Phycobiliproteins—a family of valuable, widely used achieves between 0.1 and 1 million ton, microalgae biomass fluorophores. J Appl Phycol 6:105–112 will become a clear vision as a key protein resource for human Han FF, Wang WL, Li YG, Shen GM, Wan MX, Wang J (2013) population. When the output of microalgae biomass reaches 1 Changes of biomass, lipid content and fatty acids composi- to 10 million tons, microalgae biomass will become a strategic tion under a light-dark cyclic culture of Chlorella pyrenoidosa in response to different temperature. Bioresour food and feed resource. 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