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Agar extraction from Pyropia haitanensis residue after the removal and purification of phycobiliproteins

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Abstract

Pyropia haitanensis is one of the most important and commercial species of edible seaweed in China. However, at its late growth stages it is unsuitable for food processing and is usually treated as waste. The present study investigated the full use of aging Py. haitanensis and attempted to improve its economic value through the purification of R-phycoerythrin combining the extraction of agar from the dry residue after phycobiliprotein extraction. The recovery of R-phycoerythrin from crude extract was 12.12% with a purification ratio of > 4. The agar yield was 5.81% with a gel strength of 796.00 ± 28.10 g cm−2, a gelling temperature of 38.10 ± 0.22 °C, a melting temperature of 89.50 ± 0.55 °C, 3,6-anhydrogalactose content of 34% ± 3.16%, and sulfate content of 3.01% ± 0.24%. There were no significant differences between these parameters and those from the direct extraction of Py. haitanensis. The agar extracted exhibited some physicochemical properties that have industrial applications. It could also be used as a material for DNA electrophoresis and a bacterial culture medium. This new method of comprehensive extraction reduced use of water and alkali, and waste liquid output, which were 36.52 L, 0.40 L, and 39.15 L, respectively, less than that from direct Py. haitanensis extraction. Total nitrogen, suspended solids, phosphorus, ammonia-nitrogen, chemical oxygen demand, and biochemical oxygen demand of the extract after 5 days were 38.37 mg, 4.72 × 103 mg, 62.82 mg, 18.32 mg, 8.46 × 103 mg, and 2.21 × 103 mg, respectively, less than that directly from Py. haitanensis.

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References

  • Abe M, Kobayashi M, Fujiyoshi E, Tamaki M, Kikuchi N, Murase N (2013) Use of PCR-RFLP for the discrimination of Japanese Porphyra and Pyropia species (Bangiales, Rhodophyta). J Appl Phycol 25:225–232

    Article  Google Scholar 

  • Armisen R (1995) World-wide use and importance of Gracilaria. J Appl Phycol 7:231–243

    Article  Google Scholar 

  • Bermejo R, Acién FG, Ibáñez MJ, Fernández JM, Molina E, Alvarez-Pez JM (2003) Preparative purification of B-phycoerythrin from the microalga Porphyridium cruentum by expanded-bed adsorption chromatography. J Chromatogr A 790:317–325

    CAS  Google Scholar 

  • Chen X, Wu M, Yang Q, Wang S (2017) Preparation, characterization of food grade phycobiliproteins from Porphyra haitanensis and the application in liposome-meat system. LWT Food Sci Technol 77:468–474

    Article  CAS  Google Scholar 

  • Conley DJ, Paerl HW, Howarth RW, Boesch DF, Seitzinger SP, Havens KE, Lancelot C, Likens GE (2009) Controlling eutrophication: nitrogen and phosphorus. J Sci 323:1014–1015

    CAS  Google Scholar 

  • Craigie JS, Wen ZC (1984) Effects of temperature and tissue age on gel strength and composition of agar from Gracilaria tikvahiae (Rhodophyceae). Can J Bot 62:1665–1670

    Article  CAS  Google Scholar 

  • Donati M, Francesco AD, Delucca F, Paolo MD, Battilani M, Balboni A, Baldelli R, Cevenini R (2011) Antibody-neutralizing activity against all urogenital Chlamydia trachomatis serovars in Chlamydia suis-infected pigs. FEMS Immunol Med Microbiol 61:125–128

    Article  CAS  PubMed  Google Scholar 

  • Fisheries Bureau of Ministry of Agriculture, China (2017) China Fishery Statistical Yearbook. China Agriculture Press, Beijing

  • Freile-Pelegrín Y, Murano E (2005) Agars from three species of Gracilaria (Rhodophyta) from Yucatán peninsula. Bioresour Technol 96:295–302

    Article  CAS  PubMed  Google Scholar 

  • Freile-Pelegrín Y, Robledo D (1997) Effects of season on the agar content and chemical characteristics of Gracilaria cornea from Yucatán, México. Bot Mar 40:285–290

    Article  Google Scholar 

  • Galland-Irmouli AV, Pons L, Luçon M, Villaume C, Mrabet NT, Guéant JL, Fleurence J (2000) One-step purification of R-phycoerythrin from the red macroalga Palmaria palmata using preparative polyacrylamide gel electrophoresis. J Chromatogr B 739:117–123

    Article  CAS  Google Scholar 

  • Gao H, Ji M, Cao W (1993) Comparative studies on structural feature of agar polysaccharides from Porphyra haitanensis grown in south and North China. J Oceanol Limnol 11:25–33

    Article  CAS  Google Scholar 

  • Glazer AN, Lundell DJ, Yamanaka G, Williams RC (1983) The structure of a ‘simple’ phycobilisome. Annales de l'InstitutPasteur / Microbiologie 134:159–180

    Article  Google Scholar 

  • Jeon Y-J, Athukorala Y, Lee J-H (2005) Characterization of agarose product from agar using DMSO. Algae 20:61–67

    Article  Google Scholar 

  • Kang T-H, Lee S-H, Baik J-S, Kang B-S, Lee J-S, Lee N-H, Jeon Y-J (2011) Preparation of commercial agarose from Jeju seaweed, Gelidium amansii using DMSO extraction and EDTA washing. Kor J Fish Aquat Sci 44:635–643 (Korean with English abstract)

  • Kannaujiya VK, Sinha RP (2016) Thermokinetic stability of phycocyanin and phycoerythrin in food-grade preservatives. J Appl Phycol 28:1063–1070

    Article  CAS  Google Scholar 

  • Kumar V, Fotedar R (2009) Agar extraction process for Gracilaria cliftonii (Withell, Millar, & Kraft, 1994). Carbohydr Polym 78:813–819

    Article  CAS  Google Scholar 

  • Lee W-K, Lim Y-Y, Leow AT-C, Namasivayam P, Abdullah JO, Ho C-L (2017) Biosynthesis of agar in red seaweeds: a review. Carbohydr Polym 164:23–30

    Article  CAS  PubMed  Google Scholar 

  • Liu L-N, Chen X-L, Zhang X-Y, Zhang Y-Z, Zhou B-C (2005) One-step chromatography method for efficient separation and purification of R-phycoerythrin from Polysiphonia urceolata. J Biotechnol 116:91–100

    Article  CAS  PubMed  Google Scholar 

  • Manirafasha E, Ndikubwimana T, Zeng XH, Lu YH, Jing KJ (2016) Phycobiliprotein: potential microalgae derived pharmaceutical and biological reagent. Biochem Eng J 109:282–296

    Article  CAS  Google Scholar 

  • Marinho-Soriano E, Bourret E (2003) Effects of season on the yield and quality of agar from Gracilaria species (Gracilariaceae, Rhodophyta). Bioresour Technol 90:329–333

    Article  CAS  PubMed  Google Scholar 

  • Mu K-F, Wu Y-P, Chen Z-H, Chen J, Yang F, Zhu P (2009) Production process of agar from laver Porphyra haitanensis. Fish Sci 8:010

    Google Scholar 

  • Murano E (1995) Chemical structure and quality of agars from Gracilaria. J Appl Phycol 7:245–254

    Article  CAS  Google Scholar 

  • Niu J-F, Wang G-C, Tseng C-K (2006) Purification method for large-scale isolation and purification of R-phycoerythrin from red alga Polysiphonia urceolata Grev. Protein Expr Purif 49:23–31

    Article  CAS  PubMed  Google Scholar 

  • Niu J-F, Wang G-C, Zhou B-C, Lin X-Z, Chen C-S (2007) Purification of R-phycoerythrin from Porphyra haitanensis (Bangiales, Rhodophyta) using expanded-bed absorption. J Phycol 43:1339–1347

    Article  CAS  Google Scholar 

  • Niu J-F, Chen Z-F, Wang G-C, Zhou B-C (2010) Purification of phycoerythrin from Porphyra yezoensis Ueda (Bangiales, Rhodophyta) using expanded bed absorption. J Appl Phycol 22:25–31

    Article  CAS  Google Scholar 

  • Niu J, Xu M, Wang G, Zhang K, Peng G (2013) Comprehensive extraction of agar and R-phycoerythrin from Gracilaria lemaneiformis (Bangiales, Rhodophyta). Indian J Geo-Mar Sci 42:21–28

    CAS  Google Scholar 

  • Pereira-Pacheco F, Robledo D, Rodríguez-Carvajal L, Freile-Pelegrín Y (2007) Optimization of native agar extraction from Hydropuntia cornea from Yucatán, México. Bioresour Technol 98:1278–1284

    Article  CAS  PubMed  Google Scholar 

  • Raja R, Hemaiswarya S, Kumar NA, Sridhar S, Rengasamy R (2008) A perspective on the biotechnological potential of microalgae. Crit Rev Microbiol 34:77–88

    Article  CAS  PubMed  Google Scholar 

  • Ramos A, Acién FG, Fernández-Sevilla JM, Gonzalez CV, Bermejo R (2010) Large-scale isolation and purification of C-phycocyanin from the cyanobacteria Anabaena marina using expanded bed adsorption chromatography. J Chem Technol Biotechnol 85:783–792

    Article  CAS  Google Scholar 

  • Redlinger T, Gantt E (1981) Phycobilisome structure of Porphyridium cruentum: polypeptide composition. Plant Physiol 68:1375–1379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Remirez D, Fernandez V, Tapia G, González R, Videla LA (2002) Influence of C-phycocyanin on hepatocellular parameters related to liver oxidative stress and Kupffer cell functioning. Inflamm Res 51:351–356

    Article  CAS  PubMed  Google Scholar 

  • Richa KVK, Kesheri M, Singh G, Sinha RP (2011) Biotechnological potentials of phycobiliproteins. Int J Pharm Bio Sci 2:446–454

    CAS  Google Scholar 

  • Rossano R, Ungaro N, D'Ambrosio A, Liuzzi GM, Riccio P (2003) Extracting and purifying R-phycoerythrin from Mediterranean red algae Corallina elongata Ellis & Solander. J Biotechnol 101:289–293

    Article  CAS  PubMed  Google Scholar 

  • Santos R, Melo RA (2018) Global shortage of technical agars: back to basics (resource management). J Appl Phycol 30:2463–2473

    Article  PubMed  PubMed Central  Google Scholar 

  • Sasuga K, Yamanashi T, Nakayama S, Ono S, Mikami K (2017) Optimization of yield and quality of agar polysaccharide isolated from the marine red macroalga Pyropia yezoensis. Algal Res 26:123–130

    Article  Google Scholar 

  • Sousa AMM, Alves VD, Morais S, Delerue-Matos C, Gonçalves MP (2010) Agar extraction from integrated multitrophic aquacultured Gracilaria vermiculophylla: evaluation of a microwave-assisted process using response surface methodology. Bioresour Technol 101:3258–3267

    Article  CAS  PubMed  Google Scholar 

  • Villanueva RD, Sousa AMM, Gonçalves MP, Nilsson M, Hilliou I (2010) Production and properties of agar from the invasive marine alga, Gracilaria vermiculophylla (Gracilariales, Rhodophyta). J Appl Phycol 22:211–220

    Article  CAS  Google Scholar 

  • Wang L, Liu L, Wang Y, Yuan Q, Li Z, Xu Z (2001) Comparative research on the structures and physical-chemical properties of agars from several agarophyta. Oceanol Limnol Sin 32:658–664

    CAS  Google Scholar 

  • Wang G, Sun H, Fan X, Tseng C (2002) Large-scale isolation and purification of R-phycoerythrin from red alga Palmaria palmata using the expanded bed adsorption method. Acta Bot Sin 44:541–546

    CAS  Google Scholar 

  • Wang T-P, Chang L-L, Chang S-N, Wang E-C, Hwang L-C, Chen Y-H, Wang Y-M (2012) Successful preparation and characterization of biotechnological grade agarose from indigenous Gelidium amansii of Taiwan. Process Biochem 47:550–554

    Article  CAS  Google Scholar 

  • Wang Y, Gong X, Wang S, Chen L, Sun L (2014a) Separation of native allophycocyanin and R-phycocyanin from marine red macroalga Polysiphonia urceolata by the polyacrylamide gel electrophoresis performed in novel buffer systems. PLoS One 9:e106369

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang L, Qu Y, Fu X, Zhao M, Wang S, Sun L (2014b) Isolation, purification and properties of an R-phycocyanin from the phycobilisomes of a marine red macroalga Polysiphonia urceolata. PLoS One 9:e87833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yaphe W, Arsenault GP (1965) Improved resorcinol reagent for the determination of fructose, and of 3,6-anhydrogalactose in polysaccharides. Anal Biochem 13:143–148

    Article  CAS  Google Scholar 

Download references

Funding

The research was supported by the National Key Research and Development Program of China (No. 2016YFC1400606) and the Natural Science Foundation of China (No. 31470430 and No. 41876197).

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Authors and Affiliations

  1. Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, People’s Republic of China

    Ping Zhao, Jianfeng Niu, Li Huan, Wenhui Gu & Guangce Wang

  2. Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, People’s Republic of China

    Ping Zhao, Jianfeng Niu, Li Huan, Wenhui Gu & Guangce Wang

  3. College of Earth Sciences, University of Chinese Academy of Sciences, Beijing, 100049, People’s Republic of China

    Ping Zhao

  4. Center for Ocean Mega-Science, Chinese Academy of Sciences, 7 Nanhai Road, Qingdao, 266071, Shandong, People’s Republic of China

    Ping Zhao, Jianfeng Niu, Li Huan, Wenhui Gu & Guangce Wang

  5. College of Life and Environmental Science, Wenzhou University, Wenzhou, China

    Mingjiang Wu

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  1. Ping Zhao
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  2. Jianfeng Niu
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Correspondence to Guangce Wang.

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Zhao, P., Niu, J., Huan, L. et al. Agar extraction from Pyropia haitanensis residue after the removal and purification of phycobiliproteins. J Appl Phycol 31, 2497–2505 (2019). https://doi.org/10.1007/s10811-019-1735-z

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