Bacterial chitinase with phytopathogen control capacity from suppressive soil revealed by functional metagenomics

Applied Microbiology and Biotechnology

Volumn 98, Issue 6, 2014, Pages 2819-2828

  Hjort, Karin ^a,c   Presti, Ilaria ^b   Elväng, Annelie ^a   Marinelli, Flavia ^b   Sjöling, Sara ^a  

^a SÖDERTÖRN UNIVERSITY   (Sweden)

^b UNIVERSITY OF INSUBRIA   (Italy)

^c UPPSALA UNIVERSITY   (Sweden)

Author keywords

Antifungal; Chitinolytic enzyme; Heterologous protein expression; Metagenomic library; Phytopathogen control; Soil metagenome

Indexed keywords

AMINO ACIDS; CHITIN; CROPS; ENZYMES; ESCHERICHIA COLI; FUNGI; PROTEINS; SOILS;

ANTI-FUNGAL; CHITINOLYTIC ENZYMES; HETEROLOGOUS PROTEINS; METAGENOMES; METAGENOMIC LIBRARIES; PHYTOPATHOGENS;

PATHOGENS;

CHITINASE;

AMINO ACID; ANTIMICROBIAL ACTIVITY; BACTERIUM; BIOLOGICAL CONTROL; CHITIN; CROP DAMAGE; DISEASE CONTROL; ENZYME ACTIVITY; FUNGAL DISEASE; GENE EXPRESSION; GENOMICS; MICROBIAL COMMUNITY; PEPTIDE; PROTEIN; SOIL MICROORGANISM;

ALTERNARIA ALTERNATA; ANTIFUNGAL ACTIVITY; ARTICLE; ASPERGILLUS NIGER; BACTERIAL GENE; CHI18H8 GENE; COLLETOTRICHUM; ESCHERICHIA COLI; FUNGAL PLANT DISEASE; FUSARIUM GRAMINEARUM; FUSARIUM OXYSPORUM; GENE SEQUENCE; GLOMERELLA CINGULATA; HYPOCREA LIXII; METAGENOMICS; MICROBIAL PEST CONTROL; NONHUMAN; PENICILLIUM CHRYSOGENUM; RHIZOPUS STOLONIFER; SOIL;

BACTERIA; CHITIN; CHITINASE; CLONING, MOLECULAR; DNA, BACTERIAL; ENZYME STABILITY; ESCHERICHIA COLI; FUNGI; GENE EXPRESSION; GENE LIBRARY; HYDROGEN-ION CONCENTRATION; METAGENOMICS; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SEQUENCE ANALYSIS, DNA; SOIL MICROBIOLOGY; TEMPERATURE;

EID: 84905997072     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-013-5287-x     Document Type: Article

References (59)

1. Adesina MF, Lembke A, Costa R, Speksnijder A, Smalla K (2007) Screening of bacterial isolates from various European soils for in vitro antagonistic activity towards Rhizoctonia solani and Fusarium oxysporum: site-dependent composition and diversity revealed. Soil Biol Biochem 39:2818-2828 (Pubitemid 47238911)
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403-410
3. Bhattacharya D, Nagpure A, Gupta RK (2007) Bacterial chitinases: properties and potential. Crit Rev Biotech 27:21-28 (Pubitemid 46425932)
4. Borneman J, Becker JO (2007) Identifying microorganisms involved in specific pathogen suppression in soil. Annu Rev Phytopathol 45:153-172 (Pubitemid 351321390)
5. Cottrell MT, Moore JA, Kirchman DL (1999) Chitinases from uncultured marine microorganisms. Appl Environ Microb 65:2553-2557
6. Dehestani A, Kazemitabar K, Ahmadian G, Jelodar NB, Salmanian AH, Seyedi M, Rahimian H, Ghasemi S (2010) Chitinolytic and antifungal activity of a Bacillus pumilus chitinase expressed in Arabidopsis. Biotechnol Lett 32:539-546
7. Di Maro A, Terracciano I, Sticco L, Fiandra L, Ruocco M, Corrado G, Parente A, Rao R (2010) Purification and characterization of a viral chitinase active against plant pathogens and herbivores from transgenic tobacco. J Biotechnol 147:1-6
8. Gooday GW (1990) The ecology of chitin degradation. Adv Microb Ecol 11:387-430
9. Gherbawy Y, Elhariry H, Altalhi A, El-Deeb B, Khiralla G (2012) Molecular screening of Streptomyces isolates for antifungal activity and family 19 chitinase enzymes. J Microbiol 50:459-468
10. Hassan F, Meens J, Jacobsen HJ, Kiesecker H (2009) A family 19 chitinase (Chit30) from Streptomyces olivaceoviridis ATCC 11238 expressed in transgenic pea affects the development of T. harzianum in vitro. J Biotechnol 143:302-308
11. Hårdeman F, Sjöling S (2007) Metagenomic approach for the isolation of a novel low-temperature-active lipase from uncultured bacteria of marine sediment. FEMS Microbiol Ecol 59:524-534
12. Henrissat B, Bairoch A (1993) New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 293:781-788 (Pubitemid 23244564)
13. Henrissat B, Davies G (2000) Glycoside hydrolases and glycosyltransferases: families, modules and implications for genomics. Plant Physiol 124:1515-1520
14. Herrera-Estrella A, Chet I (1999) Chitinases in biological control. In: Jollès P, Muzzarelli RAA (eds) Chitin and chitinases EXS 87. Birkhäuser Verlag, Basel, pp 171-184
15. Hjort K, Lembke A, Speksnijder A, Smalla K, Jansson JK (2007) Community structure of actively growing bacterial populations in plant pathogen suppressive soil. Microb Ecol 53:399-413 (Pubitemid 46716626)
16. Hjort K, Bergström M, Adesina MF, Jansson JK, Smalla K, Sjöling S (2010) Chitinase genes revealed and compared in bacterial isolates, DNA extracts and a metagenomic library from a phytopathogen-suppressive soil. FEMS Microbiol Ecol 71:197-207
17. Hobel CFV, Marteinsson VT, Hauksdottir S, Fridjonsson OH, Skirnisdottir S, Hreggvidsson GO, Kristjansson JK (2004) Use of low nutrient enrichments to access novel amylase genes in silent diversity of thermophiles. World J Microb Biot 20:801-809 (Pubitemid 40099315)
18. Hobel CF, Marteinsson VT, Hreggvidsson GO, Kristjansson JK (2005) Investigation of the microbial ecology of intertidal hot springs by using diversity analysis of 16S rRNA and chitinase genes. Appl Environ Microb 71:2771-2776 (Pubitemid 40647026)
19. Horn SJ, Sørbotten A, Synstad B, Sikorski P, Sørlie M, Vårum KM, Eijsink VG (2006) Endo/exo mechanism and processivity of family 18 chitinases produced by Serratia marcescens. FEBS J 273:491-503
20. Hoster F, Schmitz JE, Daniel R (2005) Enrichment of chitinolytic microorganisms: isolation and characterization of a chitinase exhibiting antifungal activity against phytopathogenic fungi from a novel Streptomyces strain. Appl Microbiol Biotechnol 66:434-442 (Pubitemid 40110150)
21. Howard MB, Nathan A, Ronald M, Weiner E, Steven WH (2003) Detection and characterization of chitinases and other chitin-modifying enzymes. J Ind Microbiol Biot 30:627-635 (Pubitemid 38067779)
22. Huang C, Lin H, Yang X (2012) Industrial production of recombinant therapeutics in Escherichia coli and its recent advancements. J Ind Microbiol Biot 39:383-399
23. Hurtado-Guerrero R, van Aalten DMF (2007) Structure of Saccharomyces cerevisiae chitinase 1 and screening based discovery of potent inhibitors. Chem Biol 14:589-599 (Pubitemid 46765151)
24. Ikeda S, Ytow N, Ezura H, Minamisawa K, Miyashita K, Fujimura T (2007) Analysis of molecular diversity of bacterial chitinase genes in the maize rhizosphere using culture-independent methods. Microbes Environ 22:71-77
25. Karlsson M, Stenlid J (2009) Evolution of family 18 glycoside hydrolases: diversity, domain structures and phylogenetic relationships. J Mol Microbiol Biotechnol 16:208-223
26. Kawase T, Yokokawa S, Saito A, Fujii T, Nikaidou N, Miyashita K, Watanabe T (2006) Comparison of enzymatic and antifungal properties between family 18 and 19 chitinases from S. coelicolor A3(2). Biosci Biotech Bioch 70:988-998
27. Keyhani NO, Roseman S (1999) Physiological aspects of chitin catabolism in marine bacteria. Biochim Biophys Acta 1473:108-122
28. Laemmli UK (1970) Cleavage of structural proteins during the assemblage of the head of bacteriophage T4. Nature 277:680-685
29. LeCleir GR, Buchan A, Hollibaugh JT (2004) Chitinase gene sequences retrieved from diverse aquatic habitats reveal environment-specific distributions. Appl Environ Microb 70:6977-6983 (Pubitemid 39643758)
30. LeCleir GR, Buchan A, Maurer J, Moran MA, Hollibaugh JT (2007) Comparison of chitinolytic enzymes from an alkaline, hypersaline lake and an estuary. Environ Microbiol 9:197-205 (Pubitemid 46059010)
31. Lee YS, Park IH, Yoo JS, Chung SY, Lee YC, Cho YS, Ahn SC, Kim CM, Choi YL (2007) Cloning, purification, and characterization of chitinase from Bacillus sp. DAU101. Biores Technol 98:2734-2741
32. 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
33. Makrides SC (1996) Strategies for achieving high-level expression of genes in Escherichia coli. Microbiol Rev 90:512-538
34. McCreath KJ, Gooday GW (1992) A rapid and sensitive microassay for determination of chitinolytic activity. J Microbiol Meth 14:229-237
35. Metcalfe AC, Krsek M, Gooday GW, Prosser JI, Wellington EM (2002) Molecular analysis of a bacterial chitinolytic community in an upland pasture. Appl Environ Microb 68:5042-5050 (Pubitemid 35154816)
36. Mukherjee G, Sen SK (2006) Purification, characterization and antifungal activity of chitinase from Streptomyces venezuelae P10. Curr Microbiol 53:265-269 (Pubitemid 44454968)
37. Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R (2010) High levels of miticides and agrochemicals in north american apiaries: implications for honey bee health. PLoS ONE 5:e9754
38. Neeraja C, Anil K, Purushotham P, Suma K, Sarma PVSRN, Moerschbacher BM, Podile AR (2010) Biotechnological approaches to develop bacterial chitinases as a bioshield against fungal diseases of plants. Crit Rev Biotechnol 30:231-241
39. Pearse AGE (1980) Histochemistry: theoretical and applied, 4th edn. Churchill-Livingstone, London
40. Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785-786
41. 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
42. Ramaiah N, Hill RT, Chun J, Ravel J, Matte MH, Straube WL, Colwell RR (2000) Use of a chiA probe for detection of chitinase genes in bacteria from the Chesapeake Bay1. FEMS Microbiol Ecol 34:63-71
43. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
44. Schmeisser C, Steele H, Streit WR (2007) Metagenomics, biotechnology with non-culturable microbes. Appl Microbiol Biot 75:955-962 (Pubitemid 46944554)
45. Sigrist CJA, Cerutti L, de Castro E, Langendijk-Genevaux PS, Bulliard V, Bairoch A, Hulo N (2010) PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Res 38:161-166
46. Singh A, Kirubakaran SI, Sakthivel N (2007) Heterologous expression of new antifungal chitinase from wheat. Protein Express Purif 56:100-109 (Pubitemid 47499092)
47. Sjöling S, Stafford W, Cowan DA (2007) Soil metagenomics: Exploring and exploiting the soil microbial gene pool. In: van Elsas JD, Jansson J, Trevors JT (eds) Modern soil microbiology, 2nd edn. CRC Press, Boca Raton, pp 409-434
48. Steinberg C, Edel-Hermann V, Alabouvette C, Lemanceau P (2007) Soil suppressiveness to plant diseases. In: van Elsas JD, Jansson J, Trevors JT (eds) Modern soil microbiology, 2nd edn. CRC Press, Boca Raton, pp 455-501
49. Suzuki K, Sugawara N, Suzuki M, Uchiyama T, Katouno F, Nikaidou N, Watanabe T (2002) Chitinases A, B, and C1 of Serratia marcescens 2170 produced by recombinant Escherichia coli: enzymatic properties and synergismon chitin degradation. Biosci Biotech Bioch 66:1075-1083 (Pubitemid 39251304)
50. Terahara T, Ikeda S, Noritake C, Minamisawa K, Ando K, Tsuneda S, Harayama S (2009) Molecular diversity of bacterial chitinases in arable soils and the effects of environmental factors on the chitinolytic bacterial community. Soil Biol Biochem 41:473-480
51. Tsujibu H, Okamoto T, Hatano N, Miyamoto K, Watanabe T, Mitsutomi M, Inamuri Y (2000) Family 19 chitinases from Streptomyces thermoviolaceus OPC-520: molecular cloning and characterization. Biosci Biotechnol Biochem 64:2445-2453
52. Uchiyama T, Watanabe K (2006) Improved inverse PCR scheme for metagenome walking. Biotechniques 41:183-188 (Pubitemid 46542602)
53. Wang S, Shao B, Fu H, Rao P (2009) Isolation of thermostable legume chitinase and study on the antifungal activity. Appl Microbiol Biot 85:313-321
54. Worku Y, Gerhardson B (1996) Suppressiveness to clubroot, pea root and Fusarium wilt in Swedish soils. J Phytopathol 144:143-146
55. Xiao L, Xie CC, Cai J, Zj L, Chen YH (2009) Identification and characterization of a chitinase produced bacillus showing significant antifungal activity. Curr Microbiol 58:528-533
56. Yan R, Hou J, Ding D, Guan W, Wang C, Wu Z, Li M (2008) In vitro antifungal activity and mechanism of action of chitinase against four plant pathogenic fungi. J Basic Microbiol 48:293-301
57. Zdobnov EM, Apweiler R (2001) InterProScan - an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17:847-848 (Pubitemid 32970486)
58. Zees AC, Pyrpassopoulos S, Vorgias CE (2009) Insights into the role of the (α+β) insertion in the TIM-barrel catalytic domain, regarding the stability and the enzymatic activity of Chitinase A from Serratia marcescens. Biochim Biophys Acta 1794:23-31
59. Zhang Z, Yuen GY, Sarath G, Penheiter AR (2001) Chitinases from the plant disease biocontrol agent, Stenotrophomonas maltophilia C3. Phytopathol 91:204-211 (Pubitemid 32106561)