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Chitinase-producing bacteria and their role in biocontrol

  • Received: 31 March 2017 Accepted: 19 July 2017 Published: 04 August 2017
  • Chitin is an important component of the exteriors of insects and fungi. Upon degradation of chitin by a number of organisms, severe damage and even death may occur in pathogens and pests whose external surfaces contain this polymer. Currently, chemical fungicides and insecticides are the major means of controlling these disease-causing agents. However, due to the potential harm that these chemicals cause to the environment and to human and animal health, new strategies are being developed to replace or reduce the use of fungal- and pest-killing compounds in agriculture. In this context, chitinolytic microorganisms are likely to play an important role as biocontrol agents and pathogen antagonists and may also function in the control of postharvest rot. In this review, we discuss the literature concerning chitin and the basic knowledge of chitin-degrading enzymes, and also describe the biocontrol effects of chitinolytic microorganisms and their potential use as more sustainable pesticides and fungicides in the field.

    Citation: Esteban A. Veliz, Pilar Martínez-Hidalgo, Ann M. Hirsch. Chitinase-producing bacteria and their role in biocontrol[J]. AIMS Microbiology, 2017, 3(3): 689-705. doi: 10.3934/microbiol.2017.3.689

    Related Papers:

  • Chitin is an important component of the exteriors of insects and fungi. Upon degradation of chitin by a number of organisms, severe damage and even death may occur in pathogens and pests whose external surfaces contain this polymer. Currently, chemical fungicides and insecticides are the major means of controlling these disease-causing agents. However, due to the potential harm that these chemicals cause to the environment and to human and animal health, new strategies are being developed to replace or reduce the use of fungal- and pest-killing compounds in agriculture. In this context, chitinolytic microorganisms are likely to play an important role as biocontrol agents and pathogen antagonists and may also function in the control of postharvest rot. In this review, we discuss the literature concerning chitin and the basic knowledge of chitin-degrading enzymes, and also describe the biocontrol effects of chitinolytic microorganisms and their potential use as more sustainable pesticides and fungicides in the field.


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    [1] Stoykov MY, Pavlov AI, Krastanov AI (2015) Chitinase biotechnology: production, purification, and application. Eng Life Sci 15: 30–38. doi: 10.1002/elsc.201400173
    [2] Oerke EC, Dehne HW, Schonbeck F, et al. (1994) Crop production and crop protection: estimated losses in major food and cash crops, Amsterdam, Netherlands: Elsevier.
    [3] Russell PE (2006) The development of commercial disease control. Plant Pathol 55: 585–594. doi: 10.1111/j.1365-3059.2006.01440.x
    [4] Jørgensen LF, Kjær J, Olsen P, et al. (2012) Leaching of azoxystrobin and its degradation product R234886 from Danish agricultural field sites. Chemosphere 88: 554–562. doi: 10.1016/j.chemosphere.2012.03.027
    [5] Damalas CA, Eleftherohorinos IG (2011) Pesticide exposure, safety issues, and risk assessment indicators. Int J Environ Res Public Health 8: 1402–1419. doi: 10.3390/ijerph8051402
    [6] Chiesa LM, Labella GF, Giorgi A, et al. (2016) The occurrence of pesticides and persistent organic pollutants in Italian organic honeys from different productive areas in relation to potential environmental pollution. Chemosphere 154: 482–490. doi: 10.1016/j.chemosphere.2016.04.004
    [7] Liu D, Cai J, Xie C, et al. (2010) Purification and partial characterization of a 36-kDa chitinase from Bacillus thuringiensis subsp. colmeri, and its biocontrol potential. Enzyme Microb Technol 46: 252–256.
    [8] Beier S, Bertilsson S (2013) Bacterial chitin degradation-mechanisms and ecophysiological strategies. Front Microbiol 4: 149.
    [9] Edreva A (2005) Pathogenesis-related proteins: research progress in the last 15 years. Gen Appl Plant Physiol 31: 105–124.
    [10] Jang MK, Kong BG, Jeong YI, et al. (2004) Physicochemical characterization of alpha-chitin, beta-chitin, and gamma-chitin separated from natural resources. J Polym Sci A Polym Chem 42: 3423–3432. doi: 10.1002/pola.20176
    [11] Gooday GW (1990) Physiology of microbial degradation of chitin and chitosan. Biodegradation 1: 177–190. doi: 10.1007/BF00058835
    [12] Adrangi S, Faramarzi MA (2013) From bacteria to human: A journey into the world of chitinases. Biotechnol Adv 31: 1786–1795. doi: 10.1016/j.biotechadv.2013.09.012
    [13] Cohen-Kupiec R, Chet I (1998) The molecular biology of chitin digestion. Curr Opin Biotechnol 9: 270–277. doi: 10.1016/S0958-1669(98)80058-X
    [14] Nagpure A, Choudhary B, Gupta RK (2014) Chitinases: in agriculture and human healthcare. Crit Rev Biotechnol 34: 215–232. doi: 10.3109/07388551.2013.790874
    [15] Dahiya N, Tewari R, Hoondal GS (2006) Biotechnological aspects of chitinolytic enzymes: a review. Appl Microbiol Biotechnol 71: 773–782. doi: 10.1007/s00253-005-0183-7
    [16] Herrera-Estrella A, Chet I (1999) Chitinases in biological control. EXS 87: 171–184.
    [17] Souza CP, Almeida BC, Colwell RR, et al. (2011) The importance of chitin in the marine environment. Mar Biotechnol 13: 823. doi: 10.1007/s10126-011-9388-1
    [18] Geisseler D, Horwath WR, Joergensen RG, et al. (2010) Pathways of nitrogen utilization by soil microorganisms-a review. Soil Biol Biochem 42: 2058–2067. doi: 10.1016/j.soilbio.2010.08.021
    [19] Brzezinska MS, Jankiewicz U, Walczak M (2013) Biodegradation of chitinous substances and chitinase production by the soil actinomycete Streptomyces rimosus. Int Biodeterior Biodegradation 84: 104–110. doi: 10.1016/j.ibiod.2012.05.038
    [20] Patil RS, Ghormade V, Deshpande MV (2000) Chitinolytic enzymes: an exploration. Enzyme Microb Technol 26: 473–483. doi: 10.1016/S0141-0229(00)00134-4
    [21] Li H, Greene LH (2010) Sequence and structural analysis of the chitinase insertion domain reveals two conserved motifs involved in chitin-binding. PLoS One 5: e8654. doi: 10.1371/journal.pone.0008654
    [22] Horn SJ, Sørbotten A, Synstad B, et al. (2006) Endo/exo mechanism and processivity of family 18 chitinases produced by Serratia marcescens. FEBS J 273: 491–503. doi: 10.1111/j.1742-4658.2005.05079.x
    [23] Kawase T, Saito A, Sato T, et al. (2004) Distribution and phylogenetic analysis of family 19 chitinases in actinobacteria. Appl Environ Microbiol 70: 1135–1144. doi: 10.1128/AEM.70.2.1135-1144.2004
    [24] Prakash NAU, Jayanthi M, Sabarinathan R, et al. (2010) Evolution, homology conservation, and identification of unique sequence signatures in GH19 family chitinases. J Mol Evol 70: 466–478. doi: 10.1007/s00239-010-9345-z
    [25] Watanabe T, Kanai R, Kawase T, et al. (1999) Family 19 chitinases of Streptomyces species: characterization and distribution. Microbiology 145: 3353–3363. doi: 10.1099/00221287-145-12-3353
    [26] Manjeet K, Purushotham P, Neeraja C, et al. (2013) Bacterial chitin binding proteins show differential substrate binding and synergy with chitinases. Microbiol Res 168: 461–468. doi: 10.1016/j.micres.2013.01.006
    [27] Purushotham P, Arun PVPS, Prakash JSS, et al. (2012) Chitin binding proteins act synergistically with chitinases in Serratia proteamaculans 568. PLoS One 7: e36714. doi: 10.1371/journal.pone.0036714
    [28] Vaaje-Kolstad G, Horn SJ, Sørlie M, et al. (2013) The chitinolytic machinery of Serratia marcescens-a model system for enzymatic degradation of recalcitrant polysaccharides. FEBS J 280: 3028–3049. doi: 10.1111/febs.12181
    [29] Frändberg E, Schnürer J (1994) Chitinolytic properties of Bacillus pabuli K1. J Appl Bacteriol 76: 361–367. doi: 10.1111/j.1365-2672.1994.tb01641.x
    [30] Gupta R, Saxena RK, Chaturvedi P, et al. (1995) Chitinase production by Streptomyces viridificans: its potential in fungal cell wall lysis. J Appl Bacteriol 78: 378–383. doi: 10.1111/j.1365-2672.1995.tb03421.x
    [31] Saito A, Fujii T, Yoneyama T, et al. (1998) glkA is involved in glucose repression of chitinase production in Streptomyces lividans. J Bacteriol 180: 2911–2914.
    [32] Xiayun J, Chen D, Shenle H, et al. (2012) Identification, characterization and functional analysis of a GH-18 chitinase from Streptomyces roseolus. Carbohydr Polym 87: 2409–2415. doi: 10.1016/j.carbpol.2011.11.008
    [33] Bélanger RR (2001) Biological control in greenhouse systems. Annu Rev Phytopathol 39: 103–133. doi: 10.1146/annurev.phyto.39.1.103
    [34] Kalia A, Gosal SK (2011) Effect of pesticide application on soil microorganisms. Arch Agron Soil Sci 57: 569–596. doi: 10.1080/03650341003787582
    [35] Schuster E, Schroeder D (1990) Side-effects of sequentially-and simultaneously-applied pesticides on non-target soil microorganisms: laboratory experiments. Soil Biol Biochem 22: 375–383. doi: 10.1016/0038-0717(90)90116-H
    [36] Carozzi NB, Koziel M (2005) Chitinase for insect control, In: Carozzi NB, Koziel M, Editors, Advances in insect control: the role of transgenic plants, London: Taylor & Francis, 211–220.
    [37] Brandt CR, Adang MJ, Spence KD (1978) The peritrophic membrane: ultrastructural analysis and function as a mechanical barrier to microbial infection in Orgyia pseudotsugata. J Invertebr Pathol 32: 12–24. doi: 10.1016/0022-2011(78)90169-6
    [38] Regev A, Keller M, Strizhov N, et al. (1996) Synergistic activity of a Bacillus thuringiensis delta-endotoxin and a bacterial endochitinase against Spodoptera littoralis larvae. Appl Environ Microbiol 62: 3581–3586.
    [39] Barka EA, Vatsa P, Sanchez L, et al. (2016) Taxonomy, physiology, and natural products of actinobacteria. Microbiol Mol Biol Rev 80: 1–43. doi: 10.1128/MMBR.00019-15
    [40] Gonzalez-Franco AC, Deobald LA, Spivak A, et al. (2003) Actinobacterial chitinase-like enzymes: profiles of rhizosphere versus non-rhizosphere isolates. Can J Microbiol 49: 683–698. doi: 10.1139/w03-089
    [41] Metcalfe AC, Krsek M, Gooday GW, et al. (2002) Molecular analysis of a bacterial chitinolytic community in an upland pasture. Appl Environ Microbiol 68: 5042–5050. doi: 10.1128/AEM.68.10.5042-5050.2002
    [42] Bai Y, Eijsink VGH, Kielak AM, et al. (2016) Genomic comparison of chitinolytic enzyme systems from terrestrial and aquatic bacteria. Environ Microbiol 18: 38–49. doi: 10.1111/1462-2920.12545
    [43] Boer WD, Gerards S, Gunnewiek PJAK, et al. (1999) Response of the chitinolytic microbial community to chitin amendments of dune soils. Biol Fertil Soils 29: 170–177. doi: 10.1007/s003740050541
    [44] Kawase T, Yokokawa S, Saito A, et al. (2006) Comparison of enzymatic and antifungal properties between family 18 and 19 chitinases from S. coelicolor A3(2). Biosci Biotechnol Biochem 70: 988–998. doi: 10.1271/bbb.70.988
    [45] Tsujibo H, Kubota T, Yamamoto M, et al. (2003) Characterization of chitinase genes from an alkaliphilic actinomycete, Nocardiopsis prasina OPC-131. Appl Environ Microbiol 69: 894–900. doi: 10.1128/AEM.69.2.894-900.2003
    [46] Prapagdee B, Kuekulvong C, Mongkolsuk S (2008) Antifungal potential of extracellular metabolites produced by Streptomyces hygroscopicus against phytopathogenic fungi. Int J Biol Sci 4: 330–337.
    [47] Tahtamouni MEW, Hameed KM, Saadoun IM (2006) Biological control of Sclerotinia sclerotiorum using indigenous chitinolytic actinomycetes in Jordan. Plant Pathol J 22: 107–114. doi: 10.5423/PPJ.2006.22.2.107
    [48] Sadeghi A, Hessan AR, Askari H, et al. (2006) Biological control potential of two Streptomyces isolates on Rhizoctonia solani, the causal agent of damping-off of sugar beet. Pak J Biol Sci 9: 904–910. doi: 10.3923/pjbs.2006.904.910
    [49] Gherbawy Y, Elhariry H, Altalhi A, et al. (2012) Molecular screening of Streptomyces isolates for antifungal activity and family 19 chitinase enzymes. J Microbiol 50: 459–468. doi: 10.1007/s12275-012-2095-4
    [50] El-Tarabily KA, Soliman MH, Nassar AH, et al. (2000) Biological control of Sclerotinia minor using a chitinolytic bacterium and actinomycetes. Plant Pathol 49: 573–583. doi: 10.1046/j.1365-3059.2000.00494.x
    [51] Lee SY, Tindwa H, Lee YS, et al. (2012) Biocontrol of anthracnose in pepper using chitinase, beta-1, 3 glucanase, and 2-furancarboxaldehyde produced by Streptomyces cavourensis SY224. J Microbiol Biotechnol 22: 1359–1366. doi: 10.4014/jmb.1203.02056
    [52] Chen YL, Lu W, Chen YH, et al. (2007) Cloning, expression and sequence analysis of chiA, chiB in Bacillus thuringiensis subsp. colmeri 15A3. Wei Sheng Wu Xue Bao 47: 843–848.
    [53] Hollensteiner J, Wemheuer F, Harting R, et al. (2017) Bacillus thuringiensis and Bacillus weihenstephanensis inhibit the growth of phytopathogenic Verticillium Species. Front Microbiol 7: 2171.
    [54] Prasanna L, Eijsink VG, Meadow R, et al. (2013) A novel strain of Brevibacillus laterosporus produces chitinases that contribute to its biocontrol potential. Appl Microbiol Biotechnol 97: 1601–1611. doi: 10.1007/s00253-012-4019-y
    [55] Kramer KJ, Muthukrishnan S (1997) Insect chitinases: molecular biology and potential use as biopesticides. Insect Biochem Molec 27: 887–900. doi: 10.1016/S0965-1748(97)00078-7
    [56] Liu C, Wu K, Wu Y, et al. (2009) Reduction of Bacillus thuringiensis Cry1Ac toxicity against Helicoverpa armigera by a soluble toxin-binding cadherin fragment. J Insect Physiol 55: 686–693. doi: 10.1016/j.jinsphys.2009.05.001
    [57] Li JG, Jiang ZQ, Xu P, et al. (2008) Characterization of chitinase secreted by Bacillus cereus strain CH2 and evaluation of its efficacy against Verticillium wilt of eggplant. Biocontrol 53: 931–944. doi: 10.1007/s10526-007-9144-7
    [58] Rishad KS, Rebello S, Shabanamol PS, et al. (2016) Biocontrol potential of halotolerant bacterial chitinase from high yielding novel Bacillus pumilus MCB-7 autochthonous to mangrove ecosystem. Pestic Biochem Physiol 137: 36–41.
    [59] Jung SJ, An KN, Jin YL, et al. (2002) Effect of chitinase-producing Paenibacillus illinoisensis KJA-424 on egg hatching of root-knot nematode (Meloidogyne incognita). J Microbiol Biotechnol 12: 865–871.
    [60] Singh AK, Singh A, Joshi P (2016) Combined application of chitinolytic bacterium Paenibacillus sp. D1 with low doses of chemical pesticides for better control of Helicoverpa armigera. Int J Pest Manage 62: 222–227.
    [61] Suzuki K, Sugawara N, Suzuki M, et al. (2002) Chitinases A, B, and C1 of Serratia marcescens 2170 produced by recombinant Escherichia coli: enzymatic properties and synergism on chitin degradation. Biosci Biotechnol Biochem 66: 1075–1083. doi: 10.1271/bbb.66.1075
    [62] Vaaje-Kolstad G, Houston DR, Riemen AHK, et al. (2005) Crystal structure and binding properties of the Serratia marcescens chitin-binding protein CBP21. J Biol Chem 280: 11313–11319. doi: 10.1074/jbc.M407175200
    [63] Someya N, Nakajima M, Hirayae K, et al. (2001) Synergistic antifungal activity of chitinolytic enzymes and prodigiosin produced by biocontrol bacterium, Serratia marcescens strain B2 against gray mold pathogen, Botrytis cinerea. J Gen Plant Pathol 67: 312–317. doi: 10.1007/PL00013038
    [64] Okamoto H, Koiso Y, Iwasaki S, et al. (1998) Identification of antibiotic red pigments of Serratia marcescens F-1-1, a biocontrol agent of damping-off of cucumber, and antimicrobial activity against other plant pathogens. Jpn J Phytopathol 64: 294–298. doi: 10.3186/jjphytopath.64.294
    [65] Suryanto D, Wahyuni S, Siregar EBM, et al. (2014) Utilization of chitinolytic bacterial isolates to control anthracnose of cocoa leaf caused by Colletotrichum gloeosporioides. Afr J Biotechnol 13: 1631–1637. doi: 10.5897/AJB11.3687
    [66] Cronin D, Moënne-Loccoz, Y, Dunne C, et al. (1997) Inhibition of egg hatch of the potato cyst nematode Globodera rostochiensis by chitinase-producing bacteria. Eur J Plant Pathol 103: 433–440. doi: 10.1023/A:1008662729757
    [67] Sindhu SS, Dadarwal KR (2001) Chitinolytic and cellulolytic Pseudomonas sp. antagonistic to fungal pathogens enhances nodulation by Mesorhizobium sp. Cicer in chickpea. Microbiol Res 156: 353–358.
    [68] Zhong W, Ding S, Guo H, et al. (2015) The chitinase C gene PsChiC from Pseudomonas sp. and its synergistic effects on larvicidal activity. Genet Mol Biol 38: 366–372.
    [69] Kharade SS, McBride MJ (2014) Flavobacterium johnsoniae chitinase ChiA is required for chitin utilization and is secreted by the type IX secretion system. J Bacteriol 196: 961–970. doi: 10.1128/JB.01170-13
    [70] Winson MK, Camara M, Latifi A, et al. (1995) Multiple N-acyl-L-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 92: 9427–9431. doi: 10.1073/pnas.92.20.9427
    [71] Chernin LS, Winson MK, Thompson JM, et al. (1998) Chitinolytic activity in Chromobacterium violaceum: substrate analysis and regulation by quorum sensing. J Bacteriol 180: 4435–4441.
    [72] Johnson GI, Sanghote S (1993) Control of postharvest diseases of tropical fruits: Challenges for the 21st century, Australian Centre for International Agricultural Research, 140–167.
    [73] Swain MR, Ray RC, Nautiyal CS (2008) Biocontrol efficacy of Bacillus subtilis strains isolated from cow dung against postharvest yam (Dioscorea rotundata L.) pathogens. Curr Microbiol 57: 407.
    [74] Essghaier B, Abdeljabbar H, Hajlaoui MR, et al. (2012) In vivo and in vitro evaluation of antifungal activities from a halotolerant Bacillus subtilis strain J9. Afr J Microbiol Res 6: 4073–4083. doi: 10.5897/AJMR11.403
    [75] Wang X, Xu F, Wang J, et al. (2013) Bacillus cereus AR156 induces resistance against Rhizopus rot through priming of defense responses in peach fruit. Food Chem 136: 400–406. doi: 10.1016/j.foodchem.2012.09.032
    [76] Zhang Q, Yong D, Zhang Y, et al. (2016) Streptomyces rochei A-1 induces resistance and defense-related responses against Botryosphaeria dothidea in apple fruit during storage. Postharvest Biol Technol 115: 30–37. doi: 10.1016/j.postharvbio.2015.12.013
    [77] Melchers LS, Lageweg W, Stuiver MH (1998) The utility of PR genes to develop disease resistance in transgenic crops, In: 5th international workshop on pathogenesis-related proteins. Signalling pathways and biological activities, Aussois, France, 46.
    [78] Buxton EW, Khalifa O, Ward V (1965) Effect of soil amendment with chitin on pea wilt caused by Fusarium oxysporum f. pisi. Ann Appl Biol 55: 83–88. doi: 10.1111/j.1744-7348.1965.tb07870.x
    [79] Cretoiu MS, Korthals GW, Visser JH, et al. (2013) Chitin amendment increases soil suppressiveness toward plant pathogens and modulates the actinobacterial and oxalobacteraceal communities in an experimental agricultural field. Appl Environ Microbiol 79: 5291–5301. doi: 10.1128/AEM.01361-13
    [80] Jacquiod S, Franqueville L, Cécillon SM, et al. (2013) Soil bacterial community shifts after chitin enrichment: an integrative metagenomic approach. PLoS One 8: e79699. doi: 10.1371/journal.pone.0079699
    [81] Vázquez MM, César, S, Azcón R, et al. (2000) Interactions between arbuscular mycorrhizal fungi and other microbial inoculants (Azospirillum, Pseudomonas, Trichoderma) and their effects on microbial population and enzyme activities in the rhizosphere of maize plants. Appl Soil Ecol 15: 261–272. doi: 10.1016/S0929-1393(00)00075-5
    [82] Vauramo S, Pasonen HL, Pappinen A, et al. (2006) Decomposition of leaf litter from chitinase transgenic silver birch (Betula pendula) and effects on decomposer populations in a field trial. Appl Soil Ecol 32: 338–349. doi: 10.1016/j.apsoil.2005.07.007
    [83] Kaur K, Dattajirao V, Shrivastava V, et al. (2012) Isolation and characterization of chitosan-producing bacterial from beaches of Chennai, India. Enzym Res 42: 1683.
    [84] Kuddus M, Ahmad IZ (2013) Isolation of novel chitinolytic bacteria and production optimization of extracellular chitinase. J Gen Eng Biotech 11: 39–46. doi: 10.1016/j.jgeb.2013.03.001
    [85] Kaplan D, Maymon M, Agapakis CM, et al. (2013) A survey of the microbial community in the rhizosphere of two dominant shrubs of the Negev Desert highlands, Zygophyllum dumosum (Zygophyllaceae) and Atriplex halimus (Amaranthaceae), using cultivation-dependent and cultivation-independent methods. Am J Bot 100: 1713–1725. doi: 10.3732/ajb.1200615
    [86] Howard MB, Ekborg NA, Weiner RM, et al. (2003) Detection and characterization of chitinases and other chitin-modifying enzymes. J Ind Microbiol Biotechnol 30: 627–635. doi: 10.1007/s10295-003-0096-3
    [87] Suginta W, Robertson PAW, Austin B, et al. (2000), Chitinases from Vibrio: activity screening and purification of chiA from Vibrio carchariae. J Appl Microbiol 89: 76–84.
    [88] Ferrari AR, Gaber Y, Fraaije MW (2014) A fast, sensitive and easy colorimetric assay for chitinase and cellulase activity detection. Biotech Biofuels 7: 37. doi: 10.1186/1754-6834-7-37
    [89] Duo-Chuan L (2006) Review of fungal chitinases. Mycopathologia 161: 345–360. doi: 10.1007/s11046-006-0024-y
    [90] Udamale SK, Moharil, MP, Ugale TB, et al. (2013) Differential inhibition of Helicoverpa armigera (Hubner) gut proteinases by proteinase inhibitors of okra and its wild relatives. ISRN Biotechnol 2013: 632173.
    [91] Rajagopal R, Arora N, Sivakumar S, et al. (2009) Resistance of Helicoverpa armigera to Cry1Ac toxin from Bacillus thuringiensis is due to improper processing of the protoxin. Biochem J 419: 309–316. doi: 10.1042/BJ20081152
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