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 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. China’s production is estimated at about two-thirds of global microalgae biomass 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 highvalue as well as commodity microalgal products, from

pharmaceuticals to biofuels and CO2 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.

* Song Qin [email protected]

Keywords Microalgae . Spirulina . Chlorella . Dunaliella . Haematococcus . Nutritional products . Microalgae mass culture

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

Introduction Microalgae are microscopic plants that typically grow suspended in water using photosynthesis to convert sunlight, water, CO2, and inorganic nutrients (N, P, K, etc.) into O2 and a biomass high in protein, vitamins, antioxidants, and other nutrients 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 photosynthetically namely Spirulina, a cyanobacterium (a prokaryote, 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): Chlorella vulgaris and C. pyrenoidosa, Dunaliella salina, and Haematococcus pluvialis.

J Appl Phycol

Chlorella is also produced commercially in several countries, 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 polyunsaturated fatty acid (LC-PUFA) docosahexaenoic acid (DHA) used in infant formula, is another alga produced by fermentations 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 require sterilized enclosed photobioreactors (PBRs), which cannot be scaled-up to production scale due to high costs. The focus herein is on the current and potential commercial production of microalgae in China using sunlight energy and CO2. Microalgae grown photosynthetically are sources of carbohydrates, protein, oils, and essential nutrients such as vitamins, 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 isolated from this alga by hot water extraction and is sold commercially 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 betacarotene (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 CO2 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 production 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 spiral shape makes it easy to harvest with relatively large opening screens. Spirulina is also quite digestible by humans and animals, requiring no cell breakage. It is rich in proteins (typically about 50 %), vitamins, essential amino acids, minerals, and essential fatty acids such as γ-linolenic acid (GLA), vitamin B12, carotenoids, and other antioxidants such phycocyanin, 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 the limitations of the technology at that time did not lead to large-scale production. The first national science and technology 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 Province in 1989 (Li and Qi 1997), and the first commercial Spirulina production by the Shenzhen Lanzao Biotech Corporation founded in 1991 and continuing to operate at present (Liang et al. 2004). Since then, Spirulina plants have been established in almost every province or region, from the southern 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 m2 (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 generally 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

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 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 Mongolia has become one of the most important centers for commercial 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 provinces 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 1 for details on Spirulina production in China). Most Spirulina production in China has used a combination of bicarbonate and air for the required CO2 supply, while Chlorella production requires CO2 fertilization, provided as compressed, liquefied CO 2 from commercial sources (Bmerchant CO2^). It is likely that merchant CO2 is also increasingly 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 CO2. Spirulina production requires high bicarbonate concentrations, 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 CO2 is supplied from a concentrated source, in which the 32-t bicarbonate can be 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 countries for Spirulina production since the start of the industry 30 years ago, and is likely that this process will be increasingly adopted in China, as once-through bicarbonate utilization 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 powder 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). Fig. 3 Views of Spirulina production pond systems in the Hainan Province (photograph supplied by King Dnarmsa Spirulina Co., Ltd)

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 commercialized 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

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 Yunnan, Sichuan

From the mid of April to the beginning of November From the mid of April to the mid-month of November

>2000 t >1000 t

Fujian Hainan, Guangdong

From the beginning of April to the end of November All year round

>200 t >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 coloring in Europe and the USA, and that is now leading to rapidly increasing production of this protein with markets being developed for the residual biomass (about 90 % of total) in aquaculture feeds. The isolation and commercial production of high-value products from Spirulina, including phycobiliproteins, peptides, and polysaccharides, is the subject 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, but the limitations 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, overtaking 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 technically more challenging and expensive production process, compared to Spirulina, due to greater potential for contamination and the need for centrifuges for harvesting these microscopic cells. This contrasts to the easier harvesting of the filamentous Spirulina and fewer problems of contamination due to the high bicarbonate growth medium. There is little information on Chlorella production in China—centrifugation is used to harvest the algal biomass, and CO2 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 carotenoids 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). βCarotene 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). However, this is for synthetic beta-carotene. BASF (a German chemical company) is the undisputed world leader in natural betacarotene production from Dunaliella salina, with over a thousand 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 Mongolia 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 Israel 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

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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 aquaculture 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 crustaceans, molluscs, etc., being raised by the aquaculture operations. Of particular interest are the long-chain C20 and C22 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 sufficient amounts has proven challenging. Thus, producing algae 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 temperatures, 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. Storing 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 Biotech 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 aquaculture 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 supply, thus presents a large, highest-value, near-term market for bulk microalgae as aquaculture and animal feeds generally.

Biofuels and CO2 capture and utilization R&D The National Development and Reform Commission of the People’s Republic of China (NDRC) 2007 (http://www. c c c h i n a . g o v. c n / We b S i t e / C C C h i n a / U p F i l e / 2 0 0 7 / 20079583745145.pdf) promulgated the Medium and LongTerm Development Plan for Renewable Energy, which projected that the consumption of biodiesel in China could reach two million tons in 2020. Microalgae biodiesel production has been suggested to have the advantage of greatly exceeding 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 CO2 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 information in peer-reviewed publications that provides information on the advances being made. The following are few examples: & &

&

Han et al (2012) devised a novel 96-well microplate swivel system (M96SS) for high-throughput screening of microalgae strains for CO2 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 CO2 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 (CO2 flue gas) for

J Appl Phycol

microalgae cultivation and the first to produce the seawater Nannochloropsis commercially, selling into the aquaculture 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 value commodities, such as feeds and fuels, with extensive R&D ongoing. This interest is being driven by the demand of sustainable, green energy and products, as well as national objectives of reducing CO2 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 regarding 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 CMIA was 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 production and to the proposed solutions, as discussed next.

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

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 standards (Chen and Li 2014). The National Health and Family Planning Commission of the People’s 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 mandatory, 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 advancing 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,

J Appl Phycol Table 2 Alliance

Leading enterprises in the Chinese Microalgae Industry

Enterprise

Location

Products

Beihai SBD bio science technology Co., Ltd

Guangxi

Food grade: Spirulina powders and tables

C.B.N Spirulina group Co., Jiangsu Ltd

King Dnarmsa Spirulina Co., Ltd

Inner Mongolia Rejuv Biotech Co., Ltd Sanya Neptunus Marine Biological Technology Co., Ltd

Yantai Hearol Biology Technology Co., Ltd

Zhongsan Lanzao Biology Food Co., Ltd Chenghai Baoer Biological Development Co., Ltd

Hainan, Fujian, Jiangxi

Food grade: Spirulina powders, tables Chlorella powders or tablets, phycocyanin, Spirulina polysaccharide Food grade: spirulina powders and tables Chlorella powders or tablets, phycocyanin

Inner Food grade: Spirulina Mongolia powders, tablets, capsules Hainan Food grade: seawater Spirulina powders, seawater Spirulina tablets, Spirulina polysaccharide Feed grade: seawater Chlorella biomass, seawater Chlorella concentrated solution Shandong Feed grade: Nannochloropsis oceanica powders and Nannochloropsis oceanica concentrated solution Guangxi Food grade: Spirulina powders and tablets Yunnan Food grade: spirulina Spirulina powders and tablets Guangxi Food grade: Spirulina powders and tablets

Guangxi Agricultural Reclamation Lvxian Biology healthy food Co., Ltd Dongying Diazen Shandong Biological Engineering Co., Ltd

Food grade: Spirulina tablets; Feed grade: seawater Chlorella concentrated solution Food grade: Spirulina tablets and some Spirulina composited food, Spirulina capsule

Dongying Haifu Biological Engineering Co., Ltd

Shandong

Inner Mongolia Meangjiali Spirulina Co., Ltd

Inner Food grade: Spirulina Mongolia powders and tablets Shandong Pharmaceutical grade: Spirulina tablet, Spirulina capsule; Hainan Feed grade: Chlorella concentrated solution

Shandong Tianshun pharmacy Co., Ltd Tianjing Ocean Pal Carol Biotech Co., Ltd

such high-value products are still too high to meet most requirements from domestic and international markets for larger volumes 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 meeting of the CMIA focused on the quality control of microalgal products for sustainable development. Several important parameters of quality control points were determined. The fifth meeting of the CMIA was 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 Qingdao, 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 advisories, 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 scientifically, many algae researchers in the CMIA test the quality of 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) tested carotenoid content. Song Qin’s research group (Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences) tested water, heavy metals (lead, mercury, cadmium, arsenic), and phycocyanin contents.

Regional quality standards will be advanced for continuing sustainable development of the microalgae healthy food industry in China. Solution II: promoting technology innovation

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

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

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further process improvements and value-added products, and most importantly, lower-cost production. The CMIA has supplied various platforms for members to achieve a fast transformation from test tube in the laboratory to production plant and markets. For example of such research applied to microalgae production, this laboratory in Yantai, developed methods for extraction 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 peptides 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 patents 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 obtained good economic effects. For another example, Wei Cong’s research group (in Beijing) designed and developed an economical device for CO2 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 CO2 absorptivity. The results indicated that an average CO2 absorptivity of 86 % and CO2 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 Li’s 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 results showed that by keeping culture broth at above 30 °C during the daytime, net biomass and lipid productivity was Fig. 5 Views of Haematococcus pluvialis production with photobioreactors in Yunnan Province (supplied by Prof. Jianguo Liu )

increased by about 38 and 45 %, respectively (Han et al. 2013). Tianzhong Liu’s team (in Qingdao) invented an attached cultivation technology for production of microalgae biofuels with microalgae cells growing on the surface of vertical artificial 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 CaCO3 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 Liu’s 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) (Liu et al. 2006).

Conclusion: microalgae for sustainable development Increasing microalgae markets are necessary to promote microalgae’s sustainable development. In 2014, the seventh CMIA meeting was held in Tianjin, China. This meeting mainly focused on the necessity, feasibility, and key technologies and difficulties of producing microalgae as feeds/diets for aquaculture animals. Six roundtables discussed the nutrient 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

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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, research 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 Technology Research Funds Projects of the Ocean (201205027). We also wish to thank Inner Mongolia Rejuv Biotech Co. Ltd and Yantai Hearol Biology 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. 3 and Prof. Jianguo Liu (Institute of Oceanology, Chinese Academy of Sciences, Qingdao) for supplying us Fig. 5.

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