Pectinolytic lyases: a comprehensive review of sources, category, property, structure, and catalytic mechanism of pectate lyases and pectin lyases

Abstract

Pectate lyases and pectin lyases have essential roles in various biotechnological applications, such as textile industry, paper making, pectic wastewater pretreatment, juice clarification and oil extraction. They can effectively cleave the α-1,4-glycosidic bond of pectin molecules back bone by β-elimination reaction to produce pectin oligosaccharides. In this way, it will not generate highly toxic methanol and has the advantages of good enzymatic selectivity, less by-products, mild reaction conditions and high efficiency. However, numerous researches have been done for several decades; there are still no comprehensive reviews to summarize the recent advances of pectate lyases and pectin lyases. This review tries to fill this gap by providing all relevant information, including the substrate, origin, biochemical properties, sequence analysis, mode of action, the three-dimensional structure and catalytic mechanism.

Keywords

Pectin lyase / Pectate lyase / Sequence analysis / Biochemical properties / Structure / Catalytic mechanism

References

[1] Abbott DW, Boraston AB. A family 2 pectate lyase displays a rare fold and transition metal-assisted β-elimination. J Biol Chem, 2007, 282(48): 35328-35336.

[2] Anand G, Yadav S, Yadav D. Production, purification and biochemical characterization of an exo-polygalacturonase from Aspergillusniger MTCC 478 suitable for clarification of orange juice. 3 Biotech, 2017, 7(2): 122.

[3] Bekli S, Aktas B, Gencer D, Aslim B. Biochemical and molecular characterizations of a novel pH- and temperature-stable pectate lyase from Bacillusamyloliquefaciens S6 for industrial application. Mol Biotechnol, 2019, 61(9): 1-13.

[4] Bermúdez-Oria A, Rodríguez-Gutiérrez G, Rodríguez-Juan E, González-Benjumea A, Fernández-Bolaños J. Molecular interactions between 3,4-dihydroxyphenylglycol and pectin and antioxidant capacity of this complex in vitro. Carbohydr Polym, 2018, 197: 260-268.

[5] Boland WE, Henriksen ED, Doran-Peterson J. Characterization of two Paenibacillusamylolyticus Strain 27C64 pectate lyases with activity on highly methylated pectin. Appl Environ Microbiol, 2010, 76(17): 6006-6009.

[6] Bonnin E, Ralet MC, Thibault JF, Schols HA. Enzymes for the valorisation of fruit- and vegetable-based co-products. Handb Waste Manag Co Prod Recovery Food Process, 2009, 27: 257-285.

[7] Charnock SJ, Brown IE, Turkenburg JP, Black GW, Davies GJ. Convergent evolution sheds light on the anti-beta -elimination mechanism common to family 1 and 10 polysaccharide lyases. Proc Natl Acad Sci USA, 2002, 99(19): 12067-12072.

[8] Chen J, Liang R-H, Liu W, Li T, Liu C-M, Wu S-S, Wang Z-J. Pectic-oligosaccharides prepared by dynamic high-pressure microfluidization and their in vitro fermentation properties. Carbohydr Polym, 2013, 91(1): 175-182.

[9] Creze C, Castang S, Derivery E, Haser R, Hugouvieux-Cotte-Pattat N, Shevchik VE, Gouet P. The crystal structure of pectate lyase peli from soft rot pathogen Erwinia chrysanthemi in complex with its substrate. J Biol Chem, 2008, 283(26): 18260-18268.

[10] Damak N, Hadj-Taieb N, Bonnin E, Bacha AB, Gargouri A. Purification and biochemical characterization of a novel thermoactive fungal pectate lyase from Penicilliumoccitanis. Process Biochem, 2011, 46(4): 888-893.

[11] Dong Z, Yang Y, Wang Z, Qin S, Zhao B. Isolation, expression and comparison of a pectate lyase produced by Fusariumoxysporum f. sp. cubense race 1 and race 4. Afr J Biotechnol, 2011, 9(53): 8984-8990.

[12] Gang L, Lang R, Xue Y, Cheng Z, Ma Y. Cloning, expression, and characterization of a highly active alkaline pectate lyase from alkaliphilic Bacillus sp. N16–5. J Microbiol Biotechnol, 2010, 20(4): 670.

[13] Garron ML, Cygler M. Structural and mechanistic classification of uronic acid-containing polysaccharide lyases. Glycobiology, 2010

[14] Gómez B, Yáñez R, Parajó J, Alonso JL. Production of pectin-derived oligosaccharides from lemon peels by extraction, enzymatic hydrolysis and membrane filtration. J Chem Technol Biotechol, 2014, 91(1): 234-247.

[15] Hamdy HS. Purification and characterization of the pectin lyase produced by Rhizopusoryzae grown on orange peels. Ann Microbiol, 2005, 55(3): 205-211.

[16] Heffron SE, Henrissat B, Yoder M, Lietzke SE, Jurnak F. Structure-based multiple alignment of extracellular pectate lyase sequences. Mol Plant Microbe Interact, 1995, 8(2): 331-334.

[17] Jayani RS, Saxena S, Gupta R. Microbial pectinolytic enzymes: a review. Process Biochem, 2005, 40(9): 2931-2944.

[18] Jenkins J, Shevchik VE, Hugouvieux-Cotte-Pattat N, Pickersgill RW. The crystal structure of pectate lyase Pel9A from Erwiniachrysanthemi. J Biol Chem, 2004, 279(10): 9139-9145.

[19] Kamijo J, Sakai K, Suzuki H, Suzuki K, Kunitake E, Shimizu M, Kato M. Identification and characterization of a thermostable pectate lyase from Aspergillusluchuensis var. saitoi. Food Chem, 2019, 276: 503-510.

[20] Kang HJ, Jo C, Kwon JH, Son JH, An BJ, Byun MW. Antioxidant and cancer cell proliferation inhibition effect of citrus pectin-oligosaccharide prepared by irradiation. J Med Food, 2006, 9(3): 313-320.

[21] Kashyap DR, Vohra PK, Chopra S, Tewari R. Applications of pectinases in the commercial sector: a review. Bioresour Technol, 2001, 77(3): 215-227.

[22] Kikuchi T, Shibuya H, Aikawa T, Jones JT. Cloning and characterization of pectate lyases expressed in the esophageal gland of the pine wood nematode Bursaphelenchusxylophilus. Mol Plant Microbe Interact, 2006, 19(3): 280-287.

[23] Kita N, Boyd CM, Garrett MR, Jurnak F, Keen NT. Differential effect of site-directed mutations in pelC on pectate lyase activity, plant tissue maceration, and elicitor activity. J Biol Chem, 1996, 271(43): 26529-26535.

[24] Kohli P, Gupta R. Alkaline pectinases: a review. Biocatal Agric Biotechnol, 2015, 4(3): S1878818115000821.

[25] Lee D-W, Kang JS, Jung CS, Han HR, Moon YS, Park SJ, Koh YH. Identification and biochemical analysis of a novel pectate lyase 3 gene in Bursaphelenchusxylophilus. J Asia Pac Entomol, 2013, 16(3): 335-342.

[26] Li P-J, Xia J-L, Nie Z-Y, Shan Y. Pectic oligosaccharides hydrolyzed from orange peel by fungal multi-enzyme complexes and their prebiotic and antibacterial potentials. LWT Food Sci Technol, 2016, 69: 203-210.

[27] Liang C, Gui X, Cheng Z, Xue Y, Tang SY. Improving the thermoactivity and thermostability of pectate lyase from Bacillus pumilus for ramie degumming. Appl Microbiol Biotechol, 2014, 99(6): 2673-2682.

[28] Lietzke SE, Scavetta RD, Yoder MD, Jurnak F. The refined three-dimensional structure of pectate lyase E from Erwiniachrysanthemi at 2.2 A resolution. Plant Physiol, 1996, 111(1): 73-92.

[29] Lima JO, Pereira JF, Araújo EF, Queiroz MV. Pectin lyase overproduction by Penicillium griseoroseum mutants resistant to catabolite repression. Braz J Microbiol, 2017

[30] Liu M-Q, Huo W-K, Dai X, Dang Y-H. Preparation of low-molecular-weight citrus pectin by recombinant Bacillussubtilis pectate lyase and promotion of growth of Bifidobacteriumlongum. Catal Commun, 2018, 107: 39-42.

[31] Ma G, Zhu W, Liu Y. QM/MM studies on the calcium-assisted β-elimination mechanism of pectate lyase from Bacillussubtilis. Proteins, 2016

[32] Michener W, Bomble YJ, Lunin E. The catalytic mechanism and unique low pH optimum of Caldicellulosiruptorbescii family 3 pectate lyase. Acta Crystallogr D Biol Crystallogr, 2015

[33] Novoa de Armas H, Verboven C, De Ranter C, Desair J, Vande Broek A, Vanderleyden J, Rabijns A. Azospirillumirakense pectate lyase displays a toroidal fold. Acta Crystallogr D Biol Crystallogr, 2004, 60(6): 999-1007.

[34] Ogawa A, Sawada K, Saito K, Hakamada Y, Ito S. A new high-alkaline and high-molecular-weight pectate lyase from a Bacillus isolate: enzymatic properties and cloning of the gene for the enzyme. Biosci Biotechnol Bioch, 2000, 64(6): 1133-1141.

[35] Olano-martin E, Gibson GR, Rastall RA. Comparison of the in vitro bifidogenic properties of pectins and pectic, ligosaccharides. J Appl Microbiol, 2002, 93(3): 505.

[36] Pérez S, Mazeau K, Penhoat CH. The three-dimensional structures of the pectic polysaccharides. Plant Physiol Bioch, 2000, 38(1–2): 37-55.

[37] Pickersgill R, Jenkins J, Harris G, Nasser W, Robert-Baudouy J. The structure of Bacillussubtilis pectate lyase in complex with calcium. Nat Struct Mol Biol, 1994, 1(10): 717-723.

[38] Saharan R, Sharma KP. Production, purification and characterization of pectin lyase from Bacillussubtilis isolated from moong beans leaves (Vigna radiata). Biocatal Agric Biotechnol, 2019, 21: 101306.

[39] Sakiyama C, Paula EM, Pereira PC, Borges AC, Silva DO. Characterization of pectin lyase produced by an endophytic strain isolated from coffee cherries. Lett Appl Microbiol, 2010, 33(2): 117-121.

[40] Sassi AH, Trigui-Lahiani H, Abdeljalil S, Gargouri A. Enhancement of solubility, purification and inclusion-bodies-refolding of an active pectin lyase from Penicilliumoccitanis expressed in Escherichiacoli. Int J Biol Macromol, 2017, 95: 256-262.

[41] Scavetta RD. Structure of a plant cell wall fragment complexed to pectate lyase C. Plant Cell, 1999, 11(6): 1081-1092.

[42] Scavetta RD, Herron SR, Hotchkiss AT, Kita N, Keen NT, Benen JA, Jurnak F. Structure of a plant cell wall fragment complexed to pectate lyase C. Plant Cell, 1999, 11(6): 1081-1092.

[43] Seyedarabi A, To TT, Ali S, Hussain S, Fries M, Madsen R, Pickersgill RW. Structural insights into substrate specificity and the anti beta-elimination mechanism of pectate lyase. Biochemistry, 2010, 49(3): 539-546.

[44] Sharma HP, Patel H, Sugandha S. Enzymatic extraction and clarification of juice from various fruits: a review. Crit Rev Food Sci Nutr, 2016

[45] Sinitsyna OA, Fedorova EA, Semenova MV, Gusakov AV, Sokolova LM, Bubnova TM, Sinitsyn AP. Isolation and characterization of extracellular pectin lyase from Penicilliumcanescens. Biochemistry, 2007, 72(5): 565-571.

[46] Tang Q, Liu YP, Ren ZG, Yan XX, Zhang LQ. 1.37 Å Crystal structure of pathogenic factor pectate lyase from Acidovoraxcitrulli. Proteins, 2013, 81(8): 1485-1490.

[47] Tobias W, Anna N, Stefan C-L. Reassessment of chitosanase substrate specificities and classification. Nat Commun, 2017

[48] Trollinger D, Berry S, Belser W, Keen NT. Cloning and characterization of a pectate lyase gene from Erwiniacarotovora EC153. Mol Plant Microbe Interact, 1989, 2(1): 17-25.

[49] Vasco-Correa J, Zapata Zapata AD. Enzymatic extraction of pectin from passion fruit peel (Passifloraedulis f. flavicarpa) at laboratory and bench scale. LWT Food Sci Technol, 2017, 80: 280-285.

[50] Vincent L, Hemalatha GR, Elodie D, Coutinho PM, Bernard H. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res, 2013

[51] Vitali J, Schick B, Kester HC, Visser J, Jurnak F. The three-dimensional structure of Aspergillusniger pectin lyase B at 1.7-Å resolution. Plant Physiol, 1998, 116(1): 69-80.

[52] Wang H, Li X, Ma Y, Song J. Characterization and high-level expression of a metagenome-derived alkaline pectate lyase in recombinant Escherichiacoli. Process Biochem, 2014, 49(1): 69-76.

[53] Wang Z, Xu B, Luo H, Meng K, Tu T. Production pectin oligosaccharides using Humicolainsolens Y1-derived unusual pectate lyase. J Biosci Bioeng, 2019, 129(1): 16.

[54] Wu P, Yang S, Zhan Z, Zhang G. Origins and features of pectate lyases and their applications in industry. Appl Microbiol Biotechnol, 2020

[55] Yadav S, Yadav PK, Yadav D, Yadav K. Purification and characterisation of an acidic pectin lyase produced by Aspergillusficuum strain MTCC 7591 suitable for clarification of fruit juices. Ann Microbiol, 2008, 58(1): 61-65.

[56] Yadav S, Yadav PK, Yadav D, Yadav KD. Purification and characterization of an alkaline pectin lyase from Aspergillusflavus. Process Biochem, 2008, 43(5): 547-552.

[57] Yadav S, Yadav PK, Yadav D, Yadav K. Purification and characterization of pectin lyase produced by Aspergillusterricola and its application in retting of natural fibers. Appl Biochem Biotechnol, 2009, 159(1): 270-283.

[58] Yadav S, Yadav PK, Yadav D, Yadav KDS. Pectin lyase: a review. Process Biochem, 2009, 44(1): 1-10.

[59] Yan Z, Ye Y, Xinyu Z. Screening of a novel polysaccharide lyase family 10 pectate lyase from Paenibacilluspolymyxa KF-1: cloning expression and characterization. Molecules, 2018

[60] Yang G, Chen W, Tan H, Li K, Li J, Yin H. Biochemical characterization and evolutionary analysis of a novel pectate lyase from Aspergillusparasiticus. Int J Biol Macromol, 2020, 152: 180-188.

[61] Yoder MD, Keen NT, Jurnak F. New domain motif: the structure of pectate lyase C, a secreted plant virulence factor. Science, 1993, 260(5113): 1503.

[62] Yuan P, Meng K, Wang Y, Luo H, Shi P, Huang H, Yao B. A low-temperature-active alkaline pectate lyase from Xanthomonascampestris ACCC 10048 with high activity over a wide pH range. Appl Biochem Biotechnol, 2012, 168(6): 1489-1500.

[63] Zhai C, Cao J, Wang Y. Cloning and expression of a pectate lyase gene from Bacillusalcalophillus NTT33. Enzyme MicrobTechnol, 2003, 33(2–3): 173-178.

[64] Zheng Y, Huang CH, Liu W, Ko TP, Xue Y, Zhou C, Ma Y. Crystal structure and substrate-binding mode of a novel pectate lyase from AlkaliphilicBacillus sp. N16–5. Biochem Biophys Res Commun, 2012, 420(2): 274.

[65] Zhou C, Xue Y, Ma Y. Characterization and overproduction of a thermo-alkaline pectate lyase from alkaliphilic Bacillus licheniformis with potential in ramie degumming. Process Biochem, 2017, 54: 49-58.

[66] Zhou Z, Liu Y, Chang Z, Wang H, Leier A, Marquez-Lago TT, Song J. Structure-based engineering of a pectate lyase with improved specific activity for ramie degumming. Appl Microbiol Biotechnol, 2017, 101(7): 2919-2929.

[67] Zhu R, Wang C, Zhang L, Wang Y, Chen G, Fan J, Ning C. Pectin oligosaccharides from fruit of Actinidiaarguta: structure-activity relationship of prebiotic and antiglycation potentials. Carbohydr Polym, 2019, 217: 90-97.

Funding

national natural science foundation of china(31601410)