Abstract
Agar is a major cell wall carbohydrate of red macroalgae (Rhodophyta). Sugars derived from agar, such as agarooligosaccharides (AOSs), neoagarooligosaccharides (NAOSs), neoagarobiose (NAB), and 3,6-anhydro-l-galactose (L-AHG), possess various physiological activities. These agar-derived sugars can be produced by hydrolysis using chemicals or agarolytic enzymes. Despite the industrial potential of agar-derived sugars, their application has been hampered mainly due to the absence of efficient processes for the liquefaction and saccharification of agar. In this review, we have focused on strategies for producing high value-added sugars from agarose via chemical or enzymatic liquefaction and enzymatic saccharification. The liquefaction of agarose is a key step for preventing gelling and increasing the solubility of agarose in water by prehydrolyzing agarose into AOSs or NAOSs. For the industrial use of agar-derived sugars, AOS, NAOS, NAB, and L-AHG can be used as functional biomaterials owing to their physiological activities such as antiinflammation, skin whitening, and moisturizing. Recently, it was reported that AHG could be considered as a new anticariogenic sugar to replace xylitol. This review provides a comprehensive overview of processes for the hydrolysis of agar or agarose to produce high value-added sugars and the industrial application of these sugars.
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References
Armisén R, Galatas F (1987) Production, properties and uses of agar. In: McHugh DJ (ed) Production and utilization of products from commercial seaweeds. FAO Fisheries Technical Paper 288. FAO, Rome, pp 1–57
Bindels LB, Delzenne NM, Cani PD, Walter J (2015) Towards a more comprehensive concept for prebiotics. Nat Rev Gastroenterol Hepatol 12(5):303–310
Brinker CJ, Scherer GW (1990) Sol−gel science: the physics and chemistry of sol−gel processing. Academic Press
Budavari S, O'Neil M, Smith A, Heckelman P, Obenchain J (1996) The Merck index, 12th edn. CRC Press, Boca Raton, p 34
Chen H, Yan X, Zhu P, Lin J (2006) Antioxidant activity and hepatoprotective potential of agaro-oligosaccharides in vitro and in vivo. Nutr J 5(31):1–12
Cui F, Dong S, Shi X, Zhao X, Zhang X-H (2014) Overexpression and characterization of a novel thermostable β-agarase YM01-3, from marine bacterium Catenovulum agarivorans YM01T. Mar Drugs 12(5):2731–2747
Delattre C, Fenoradosoa TA, Michaud P (2011) Galactans: an overview of their most important sourcing and applications as natural polysaccharides. Braz Arch Biol Technol 54:1075–1092
Ekborg NA, Taylor LE, Longmire AG, Henrissat B, Weiner RM, Hutcheson SW (2006) Genomic and proteomic analyses of the agarolytic system expressed by Saccharophagus degradans 2-40. Appl Environ Microbiol 72(5):3396–3405
Enoki T, Okuda S, Kudo Y, Takashima F, Sagawa H, Kato I (2010) Oligosaccharides from agar inhibit pro-inflammatory mediator release by inducing heme oxygenase 1. Biosci Biotechnol Biochem 74(4):766–770
Flament D, Barbeyron T, Jam M, Potin P, Czjzek M, Kloareg B, Michel G (2007) Alpha-agarases define a new family of glycoside hydrolases, distinct from beta-agarase families. Appl Environ Microbiol 73(14):4691–4694
Fujii T, Yano T, Kumagai H, Miyawaki O (2000) Scaling analysis on elasticity of agarose gel near the sol—gel transition temperature. Food Hydrocolloids 14(4):359–363
Goh CS, Lee KT (2010) A visionary and conceptual macroalgae-based third-generation bioethanol (TGB) biorefinery in Sabah, Malaysia as an underlay for renewable and sustainable development. Renew Sus Energ Rev 14(2):842–848
Ha SC, Lee S, Lee J, Kim HT, Ko H-J, Kim KH, Choi I-G (2011) Crystal structure of a key enzyme in the agarolytic pathway, α-neoagarobiose hydrolase from Saccharophagus degradans 2–40. Biochem Biophys Res Commun 412(2):238–244
Hassairi I, Ben Amar R, Nonus M, Gupta BB (2001) Production and separation of α-agarase from Altermonas agarlyticus strain GJ1B. Bioresour Technol 79(1):47–51
Hehemann J-H, Smyth L, Yadav A, Vocadlo DJ, Boraston AB (2012) Analysis of keystone enzyme in agar hydrolysis provides insight into the degradation (of a polysaccharide from) red seaweeds. J Biol Chem 287(17):13985–13995
Higashimura Y, Naito Y, Takagi T, Mizushima K, Hirai Y, Harusato A, Ohnogi H, Yamaji R, Inui H, Nakano Y, Yoshikawa T (2013) Oligosaccharides from agar inhibit murine intestinal inflammation through the induction of heme oxygenase-1 expression. J Gastroenterol 48(8):897–909
Higashimura Y, Naito Y, Takagi T, Uchiyama K, Mizushima K, Ushiroda C, Ohnogi H, Kudo Y, Yasui M, Inui S, Hisada T, Honda A, Matsuzaki Y, Yoshikawa T (2016) Protective effect of agaro-oligosaccharides on gut dysbiosis and colon tumorigenesis in high-fat diet-fed mice. Am J Physiol Gastrointest Liver Physiol 310(6):G367–G375
Hu B, Gong Q, Wang Y, Ma Y, Li J, Yu W (2006) Prebiotic effects of neoagaro-oligosaccharides prepared by enzymatic hydrolysis of agarose. Anaerobe 12(5–6):260–266
Indovina PL, Tettamanti E, Micciancio-Giammarinaro MS, Palma MU (1979) Thermal hysteresis and reversibility of gel–sol transition in agarose–water systems. J Chem Phys 70(6):2841–2847
Jang M-K, Lee D-G, Kim N-Y, Yu K-H, Jang H-J, Lee SW, Jang HJ, Lee YJ, Lee S-H (2009) Purification and characterization of neoagarotetraose from hydrolyzed agar. J Microbiol Biotechnol 19(10):1197–1200
Jung S, Lee C-R, Chi W-J, Bae C-H, Hong S-K (2017) Biochemical characterization of a novel cold-adapted GH39 β-agarase, AgaJ9, from an agar-degrading marine bacterium Gayadomonas joobiniege G7. Appl Microbiol Biotechnol 101(5):1965–1974
Kim C, Ryu HJ, Kim SH, Yoon J-J, Kim HS, Kim YJ (2010a) Acidity tunable ionic liquids as catalysts for conversion of agar into mixed sugars. Bull Kor Chem Soc 31(2):511–514
Kim HT, Lee S, Kim KH, Choi I-G (2012) The complete enzymatic saccharification of agarose and its application to simultaneous saccharification and fermentation of agarose for ethanol production. Bioresour Technol 107:301–306
Kim HT, Lee S, Lee D, Kim H-S, Bang W-G, Kim KH, Choi I-G (2010b) Overexpression and molecular characterization of Aga50D from Saccharophagus degradans 2-40: an exo-type β-agarase producing neoagarobiose. Appl Microbiol Biotechnol 86(1):227–234
Kim HT, Yun EJ, Wang D, Chung JH, Choi I-G, Kim KH (2013a) High temperature and low acid pretreatment and agarase treatment of agarose for the production of sugar and ethanol from red seaweed biomass. Bioresour Technol 136:582–587
Kim JH, Yun EJ, Seo N, Yu S, Kim DH, Cho KM, An HJ, Kim J-H, Choi I-G, Kim KH (2017) Enzymatic liquefaction of agarose above the sol–gel transition temperature using a thermostable endo-type β-agarase, Aga16B. Appl Microbiol Biotechnol 101(3):1111–1120
Kim KH, Choi IG, Kang NJ, Yun EJ, Lee SY, Kim JH, Kim YA, Kim BB, Baek EJ (2013b) Method for preparing 3,6-anhydro-L-galactose, and use thereof. PCT/KR2013/000423, World Intellectual Property Organization
Knutsen SH, Myslabodski DE, Larsen B, Usov AI (1994) A modified system of nomenclature for red algal galactans. Bot Mar 37(2):163–169
Knuuttila MLE, Mäkinen KK (1975) Effect of xylitol on the growth and metabolism of Streptococcus mutans. Caries Res 9(3):177–189
Kobayashi R, Takisada M, Suzuki T, Kirimura K, Usami S (1997) Neoagarobiose as a novel moisturizer with whitening effect. Biosci Biotechnol Biochem 61(1):162–163
Lahaye M, Yaphe W, Viet MTP, Rochas C (1989) 13C-N.M.R. spectroscopic investigation of methylated and charged agarose oligosaccharides and polysaccharides. Carbohydr Res 190(2):249–265
Lee CH, Kim HT, Yun EJ, Lee AR, Kim SR, Kim J-H, Choi I-G, Kim KH (2014) A novel agarolytic β-galactosidase acts on agarooligosaccharides for complete hydrolysis of agarose into monomers. Appl Environ Microbiol 80(19):5965–5973
Lee CH, Yun EJ, Kim HT, Choi I-G, Kim KH (2015) Saccharification of agar using hydrothermal pretreatment and enzymes supplemented with agarolytic β-galactosidase. Process Biochem 50(10):1629–1633
Li G, Sun M, Wu J, Ye M, Ge X, Wei W, Li H, Hu F (2015) Identification and biochemical characterization of a novel endo-type β-agarase AgaW from Cohnella sp. strain LGH. Appl Microbiol Biotechnol 99(23):10019–10029
Li M, Li G, Zhu L, Yin Y, Zhao X, Xiang C, Yu G, Wang X (2014) Isolation and characterization of an agaro-oligosaccharide (AO)-hydrolyzing bacterium from the gut microflora of Chinese individuals. PLoS One 9(3):e91106
Malihan LB, Nisola GM, Mittal N, Lee S-P, Seo JG, Kim H, Chung W-J (2016) SBA-15 supported ionic liquid phase (SILP) with H2PW12O40 - for the hydrolytic catalysis of red macroalgal biomass to sugars. RSC Adv 6(40):33901–33909
Medina-Esquivel R, Freile-Pelegrin Y, Quintana-Owen P, Yáñez-Limón JM, Alvarado-Gil JJ (2008) Measurement of the sol–gel transition temperature in agar. Int J Thermophys 29(6):2036–2045
Mouradian WE, Wehr E, Crall JJ (2000) Disparities in children’s oral health and access to dental care. J Am Med Assoc 284(20):2625–2631
Ohta Y, Hatada Y, Miyazaki M, Nogi Y, Ito S, Horikoshi K (2005) Purification and characterization of a novel α-agarase from a Thalassomonas sp. Curr Microbiol 50(4):212–216
Ohta Y, Hatada Y, Nogi Y, Li Z, Zhang H-M, Ito S, Horikoshi K (2004) Thermostable beta-agarase from a deep-sea Microbulbifer isolate. J Appl Glycosci 51(3):203–210
Park J-H, Hong J-Y, Jang HC, Oh SG, Kim S-H, Yoon J-J, Kim YJ (2012) Use of Gelidium amansii as a promising resource for bioethanol: a practical approach for continuous dilute-acid hydrolysis and fermentation. Bioresour Technol 108:83–88
Pluvinage B, Hehemann J-H, Boraston AB (2013) Substrate recognition and hydrolysis by a family 50 exo-β-agarase, Aga50D, from the marine bacterium Saccharophagus degradans. J Biol Chem 288(39):28078–28088
Potin P, Richard C, Rochas C, Kloareg B (1993) Purification and characterization of the α-agarase from Alteromonas agarlyticus (Cataldi) comb. nov., strain GJ1B. FEBS J 214(2):599–607
Richardson TH, Tan XQ, Frey G, Callen W, Cabell M, Lam D, Macomber J, Short JM, Robertson DE, Miller C (2002) A novel, high performance enzyme for starch liquefaction—discovery and optimization of a low pH, thermostable α-amylase. J Biol Chem 277(29):26501–26507
Saha D, Bhattacharya S (2010) Hydrocolloids as thickening and gelling agents in food: a critical review. J Food Sci Technol 47(6):587–597
Scott TA (1988) The concise encyblopedia of biochemistry. Biochem Educ 16(4):208–210
Usov AI (1998) Structural analysis of red seaweed galactans of agar and carrageenan groups. Food Hydrocolloids 12(3):301–308
Wei N, Quarterman J, Jin Y-S (2013) Marine macroalgae: an untapped resource for producing fuels and chemicals. Trends Biotechnol 31(2):70–77
Yang B, Yu G, Zhao X, Jiao G, Ren S, Chai W (2009) Mechanism of mild acid hydrolysis of galactan polysaccharides with highly ordered disaccharide repeats leading to a complete series of exclusively odd-numbered oligosaccharides. FEBS J 276(7):2125–2137
Yun EJ, Choi I-G, Kim KH (2015a) Red macroalgae as a sustainable resource for bio-based products. Trends Biotechnol 33(5):247–249
Yun EJ, Kim HT, Cho KM, Yu S, Kim S, Choi I-G, Kim KH (2016a) Pretreatment and saccharification of red macroalgae to produce fermentable sugars. Bioresour Technol 199:311–318
Yun EJ, Lee AR, Kim JH, Cho KM, Kim KH (2017) 3,6-Anhydro-L-galactose, a rare sugar from agar, a new anticariogenic sugar to replace xylitol. Food Chem 221:976–983
Yun EJ, Lee S, Kim HT, Pelton JG, Kim S, Ko H-J, Choi I-G, Kim KH (2015b) The novel catabolic pathway of 3,6-anhydro-L-galactose, the main component of red macroalgae, in a marine bacterium. Environ Microbiol 17(5):1677–1688
Yun EJ, Lee S, Kim JH, Kim BB, Kim HT, Lee SH, Pelton JG, Kang NJ, Choi I-G, Kim KH (2013) Enzymatic production of 3,6-anhydro-L-galactose from agarose and its purification and in vitro skin whitening and anti-inflammatory activities. Appl Microbiol Biotechnol 97(7):2961–2970
Acknowledgements
This work was supported by a grant from the Korean Ministry of Trade, Industry & Energy (10052721). This study was performed at the Korea University Food Safety Hall for the Institute of Biomedical Science and Food Safety.
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Yun, E.J., Yu, S. & Kim, K.H. Current knowledge on agarolytic enzymes and the industrial potential of agar-derived sugars. Appl Microbiol Biotechnol 101, 5581–5589 (2017). https://doi.org/10.1007/s00253-017-8383-5
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DOI: https://doi.org/10.1007/s00253-017-8383-5