A novel salt-tolerant chitobiosidase discovered by genetic screening of a metagenomic library derived from chitin-amended agricultural soil

Applied Microbiology and Biotechnology

Volumn 99, Issue 19, 2015, Pages 8199-8215

  Cretoiu, Mariana Silvia ^a,b   Berini, Francesca ^c   Kielak, Anna Maria ^d   Marinelli, Flavia ^c   van Elsas, Jan Dirk ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

^c UNIVERSITY OF INSUBRIA   (Italy)

^d NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

Author keywords

Chitinolytic enzymes; Fosmid library; Functional metagenomics; Suppressive soil

Indexed keywords

AGRICULTURE; BIOLOGY; CHITIN; CLONING; DIAGNOSIS; ENCODING (SYMBOLS); ENZYMES; ESCHERICHIA COLI; GENE EXPRESSION; POLYMERASE CHAIN REACTION; PROTEINS; SOILS;

AGRICULTURAL SOILS; CHITIN DEACETYLASE; CHITINOLYTIC ENZYMES; DEGENERATE PRIMERS; METAGENOMIC LIBRARIES; METAGENOMICS; OPEN READING FRAME; STENOTROPHOMONAS MALTOPHILIA;

GENES;

BACTERIAL DNA; CHITIN; CHITOBIOSIDASE; ENZYME; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CHITINASE; SODIUM CHLORIDE; SOIL;

AGRICULTURAL SOIL; BACTERIUM; CHITIN; COLIFORM BACTERIUM; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC MARKER; PROTEIN; SALINITY TOLERANCE; SOIL MICROORGANISM;

ACIDOBACTERIUM; AEROMONAS VERONII; AGRICULTURAL SOIL; ARTICLE; BURKHOLDERIA; CHLOROFLEXI; ESCHERICHIA COLI; GENETIC SCREENING; KTEDONOBACTER RACEMIFER; METAGENOMICS; NITROLANCETUS HOLLANDICUS; NONHUMAN; SOIL; STENOTROPHOMONAS MALTOPHILIA; BACTERIUM; CHEMISTRY; ENZYME STABILITY; ENZYMOLOGY; GENE LIBRARY; GENETICS; METABOLISM; MICROBIOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PH; PHYLOGENY;

ACIDOBACTERIUM; AEROMONAS VERONII; BACTERIA (MICROORGANISMS); BURKHOLDERIA SP.; CHLOROFLEXI; CHLOROFLEXI (CLASS); ESCHERICHIA COLI; STENOTROPHOMONAS MALTOPHILIA;

BACTERIA; BACTERIAL PROTEINS; BASE SEQUENCE; CHITIN; CHITINASES; CLONING, MOLECULAR; ENZYME STABILITY; GENE LIBRARY; HYDROGEN-ION CONCENTRATION; METAGENOMICS; MOLECULAR SEQUENCE DATA; PHYLOGENY; SODIUM CHLORIDE; SOIL; SOIL MICROBIOLOGY;

EID: 84941191901     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-015-6639-5     Document Type: Article

References (71)

1. Adrangi S, Faramarzi MA (2013) From bacteria to humans: a journey into the world of chitinases. Biotechnol Adv 31:1786–1795
2. Anthon GE, Barrett DM (2002) Determination of reducing sugars with 3-methyl-2-benzothiazolinonehydrazone. Anal Biochem 305:287–289
3. Aunpad R, Rice DW, Sedelnikova S, Panbangred W (2007) Biochemical characterisation of two forms of halo- and thermo-tolerant chitinase C of Salinivibrio costicola expressed in Escherichia coli. Ann Microbiol 57:249–257
4. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST Server: rapid annotations using subsystems technology. BMC Bioinforma 9:386
5. Beier S, Bertilsson S (2013) Bacterial chitin degradation—mechanisms and ecophysiological strategies. Front Microbiol 4:1–10. doi:10.3389/fmicb.2013.00149
6. Bolhuis A, Kwan D, Thomas JR (2008) Halophilic adaptations of proteins. In: Siddiqui KS, Thomas T (ed) Protein adaptation in extremophiles. Noval Science Publisher Inc., pp 71-104
7. Bonfante P, Anca IA (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu Rev Microbiol 63:363–383
8. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:D233–D238
9. Cretoiu MS, Kielak AM, Abu Al-Soud W, Sørensen SJ, van Elsas JD (2012) Mining of unexplored habitats for novel chitinases–chiA as a helper gene proxy in metagenomics. Appl Microbiol Biotechnol 94:1347–1358
10. Cretoiu MS, Korthals GW, Visser JHM, van Elsas JD (2013) Chitin amendment increases soil suppressiveness toward plant pathogens and modulates the actinobacterial and oxalobacteriaceal communities in an experimental agricultural field. Appl Environ Microbiol 79:1–11
11. Darling AE, Mau B, Perna NT (2010) ProgressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5(6):e11147
12. Delcher AL, Harmon D, Kasif S, White O, Salzberg SL (1999) Improved microbial gene identification with GLIMMER. Nucleic Acids Res 27:4636–4641
13. Delpin M, Goodman AE (2009) Nutrient regime regulates complex transcriptional start site usage within a Pseudoalteromonas chitinase gene cluster. ISME J 3:1053–1063
14. Eijsink V, Hoell I, Vaaje-Kolstad G (2010) Structure and function of enzymes acting on chitin and chitosan. Biotechnol Genet Eng Rev 27:331–366
15. Ekkers DM, Cretoiu MS, Kielak AM, van Elsas JD (2012) The great screen anomaly—a new frontier in product discovery through functional metagenomics. Appl Microbiol Biotechnol 93:1005–1020
16. Ferrer M, Martínez-Abarca F, Golyshin PN (2005) Mining genomes and ‘metagenomes’ for novel catalysts. Curr Opin Biotechnol 16:588–593
17. Field D, Tiwari B, Booth T, Houten S, Swan D, Bertrand N, Thurston M (2006) Open Software for biologists: from famine to feast. Nat Biotechnol 24:801–803
18. Francetic O, Belin D, Badaut C, Pugsley A (2000a) Expression of the endogenous type II secretion pathway in Eschericha coli leads to chitinase secretion. EMBO J 19:6697–6703
19. Francetic O, Badaut C, Rimsky S, Pugsley A (2000b) The ChiA (YheB) protein of Escherichia coli K-12 is an endochitinase whose gene is negatively controlled by the nucleoid-structuring protein H-NS. Mol Microbiol 35:1506–1517
20. Garcia-Fraga B, da Silva AF, Lòpez-Sejias J, Sieiro C (2014) Functional expression and characterization of a chitinase from the marine archaeon Halobacterium salinarum CECT 395 in Escherichia coli. Appl Microbiol Biotechnol 95:2133–2143
21. Gomes J, Steiner W (2004) The biocatalytic potential of extremophiles and extremozymes. Food Technol Biotechnol 42:223–235
22. Gooday GW (1990) Physiology of microbial degradation of chitin and chitosan. Biodegradation 1:177–190
23. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
24. Hardeman F, Sjoling 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
25. Hjort K, Presti I, Elvang A, Marinelli F, Sjoling S (2014) Bacterial chitinase with phytopathogen control capacity from suppressive soil revealed by functional metagenomics. Appl Microbiol Biotechnol 98:2819–2828
26. Horn SJ, Vaaje-Kolstad G, Westereng B, Eijsink VGH (2012) Novel enzymes for the degradation of cellulose. Biotechnol Biofuels 5:45
27. Hsu SC, Lockwood JL (1975) Powdered chitin agar as a selective medium for enumeration of actinomycetes in water and soil. Appl Microbiol 29:422–426
28. Ichikawa N, Oguchi A, Ikeda H, Ishikawa J, Kitani S, Watanabe Y, Nakamura S, Katano Y, Kishi E, Sasagawa M, Ankai A, Fukui S, Hashimoto Y, Kamata S, Otoguro M, Tanikawa S, Nihira T, Horinouchi S, Ohnishi Y, Hayakawa M, Kuzuyama T, Arisawa A, Nomoto F, Miura H, Takahashi Y, Fujita N (2010) Genome sequence of Kitasatospora setae NBRC 14216T: an evolutionary snapshot of the family Streptomycetaceae. DNA Res 17:393–406
29. Israel DI (1993) A PCR-based method for high stringency screening of DNA libraries. Nucleic Acids Res 21:2627–2631
30. 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
31. Kharade SS, McBride MJ (2015) Flavobacterium johnsoniae PorV is required for secretion of a subset of proteins targeted to the type IX secretion system. J Bacteriol 197. Doi 10.1128/JB.02085-14
32. Khmel IA, Ovadis MI, Mayatskaya AV, Veselovskii AM, Bass IA, Lipasova VA, Bolshoy A, Chet I, Chernin LS (2005) Activity of Serratia plymuthica IC1270 gene chiA promoter region in Escherichia coli mutants deficient in global regulators of transcription. J Basic Microbiol 45:426–437
33. Kielak AM, Cretoiu MS, Semenov AV, Sørensen SJ, van Elsas JD (2013) Bacterial chitinolytic communities respond to chitin and pH alteration in soil. Appl Environ Microbiol 79:263–272
34. Konagaya Y, Tsuchiva C, Sugita H (2006) Purification and characterization of chitinases from Clostridium sp. E-16 isolated from the intestinal tract of the South American sea lion (Otaria flavescens). Lett Appl Microbiol 43:187–193
35. Korthals GW, de Boer M, Visser JHM, Molendijk LPG (2010) Bodemgezondheid binnen bedrijfssytemen. Mededelingenblad van de Koninklijke Nederlandse Plantenziektekundige Vereniging 41:281-284
36. LeClair 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
37. 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
38. Litchfield CD (2011) Potential for industrial products from the halophilic Archaea. J Ind Microbiol Biotechnol 38:1635–1647
39. Lobo MD, Silva FD, Landim PG, da Cruz PR, de Brito TL, de Medeiros SC, Oliveira JT, Vasconcelos IM, Pepreira HD, Grangeiro TB (2013) Expression and efficient secretion of a functional chitinase from Chromobacterium violaceum in Escherichia coli. BMC Biotechnol 13:46
40. Manucharova NA, Vlasenko AN, Stepanov AL (2007) Temperature as an autoecological factor of chitinolytic microbial complex formation in soils. Biol Bull 34:163–169
41. Metcalfe AC, Krsek M, Gooday GW, Prosser JI, Wellington EMH (2002) Molecular analysis of a bacterial chitinolytic community in an upland pasture. Appl Environ Microbiol 68:5042–5050
42. Nacke H, Will C, Herzog S, Nowka B, Engelhaupt M, Daniel R (2011) Identification of novel lipolytic genes and gene families by screening of metagenomic libraries derived from soil samples of the German Biodiversity Exploratories. FEMS Microbiol Ecol 78:188–201
43. Nakamoto T (2009) Evolution and the universality of the mechanism of initiation of protein synthesis. Gene 432:1–6
44. Noguchi H, Park J, Takagi T (2006) MetaGene: prokaryotic gene finding from environmental genome shotgun sequences. Nucleic Acids Res 34:5623–5630
45. Oren A, Mana L (2002) Amino acid composition of bulk protein and salt relationships of selected enzymes of Salinibacter ruber, an extremely halophilic bacterium. Extremophiles 6:217–223
46. Park BH, Karpinets TV, Syed MH, Leuze MR, Uberbacher EC (2010) CAZymes Analysis Toolkit (CAT): web service for searching and analyzing carbohydrate-active enzymes in a newly sequenced organism using CAZy database. Glycobiology 20:1574–1584
47. Payne CM, Baban J, Horn SJ, Backe PH, Arvai AS, Dalhus B, Bjørås M, Eijsink VG, Sørlie M, Beckham GT, Vaaje-Kolstad G (2012) Hallmarks of processivity in glycoside hydrolases from crystallographic and computational studies of the Serratia marcescens chitinases. J Biol Chem 287:36322–36330
48. Peterson DG, Tomkins JP, Frisch DA, Wing RA, Paterson AH (2002) Construction of plant bacterial artificial chromosome (BAC) libraries: an illustrated guide (http:www.mgel.msstate.edu/newbac.htm)
49. Poulsen PH, Moller J, Magid J (2008) Determination of a relationship between chitinase activity and microbial diversity in chitin amended compost. Bioresour Technol 99:4355–4359
50. Qing G, Ma LC, Khorchid A, Swapna GVT, Mal TK, Takayama MM, Xia B, Phadtare S, Ke H, Acton T, Montelione GT, Ikura M, Inouye M (2004) Cold-shock induced high-yield protein production in Escherichia coli. Nat Biotechnol 22:877–882
51. Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R (2005) InterProScan: protein domains identifier. Nucleic Acids Res 33(Web Server issue):W116–W120
52. Raes J, Korbel JO, Lercher MJ, von Mering C, Bork P (2007) Prediction of effective genome size in metagenomic samples. Genome Biol 8:R10
53. Raghava GP, Barton GJ (2006) Quantification of the variation in percentage identity for protein sequence alignments. BMC Bioinforma 7:415
54. Reed CJ, Lewis H, Treio E, Winston V, Evilia C (2013) Protein adaptations in archaeal extremophiles. Archaea 2013:373275
55. Rost B (1999) Twilight zone of protein sequence alignments. Protein Eng 12:85–94
56. Roy A, Kucukural A, Zhang Y (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5:725–738
57. Salis HM, Mirsky EA, Voigt CA (2009) Automated design of synthetic ribosome binding sites to control protein expression. Nat Biotechnol 27:946–950
58. Schagger H, van Jagow G (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166:368–379
59. Shultzaberger RK, Bucheimer RE, Rudd KE, Schneider TD (2001) Anatomy of Escherichia coli ribosome binding sites. J Mol Biol 313:215–228
60. Simon C, Daniel R (2009) Achievements and new knowledge unraveled by metagenomic approaches. Appl Microbiol Biotechnol 85:265–276
61. Sorokin DY, Lucker S, Vejmelkova D, Kostrikina NA, Kleerebezem R, Rijpstra WI, Damste JS, Le Paslier D, Muyzer G, Wagner M, van Loosdrecht MC, Daims H (2012) Nitrification expanded: discovery, physiology and genomics of a nitrite-oxidizing bacterium from the phylum Chloroflexi. ISME J 6:2245–2256
62. Stewart CR, Gaslightwala I, Hinata K, Krolikowski KA, Needleman DS, Peng AS, Peterman MA, Tobias A, Wei P (1998) Genes and regulatory sites of the “host-takeover module” in the terminal redundancy of Bacillus subtilis bacteriophage SPO1. Virology 246:329–340
63. Suzuki K, Taivoji M, Sugawara N, Nikaidou N, Henrissat B, Watanabe T (1999) The third chitinase gene (chiC) of Serratia marcescens 2170 and the relationship of its product to other bacterial chitinases. Biochemistry 343:587–596
64. Tikole S, Sankararamakrishnan R (2006) A survey of mRNA sequences with a non-AUG start codon in RefSeq database. J Biomol Struct Dyn 24:33–42
65. Toratani T, Kezuka Y, Nonaka T, Hiragi Y, Watanabe T (2006) Structure of full-length bacterial chitinase containing two fibronectin type III domains revealed by small angle X-ray scattering. Biochem Biophys Res Commun 348:814–818
66. Vaaje-Kolstad G, Horn SJ, Sørlie M, Eijsink VG (2013) The chitinolytic machinery of Serratia marcescens—a model system for enzymatic degradation of recalcitrant polysaccharides. FEBS J 280:3028–3049
67. Van Elsas JD, Speksnijder AJ, van Overbeek LS (2008) A procedure for the metagenomics exploration of disease-suppressive soils. J Microbiol Methods 75:515–522
68. Watanabe T, Kobori K, Miyashita K, Fujii T, Sakai H, Uchida M, Tanaka H (1993) Identification of glutamic acid 204 and aspartic acid 200 in chitinase A1 of Bacillus circulans WL-12 as essential residues for chitinase activity. J Biol Chem 268:18567–18572
69. Williamson N, Brian P, Wellington EM (2000) Molecular detection of bacterial and streptomycete chitinase in the environment. Antonie Van Leeuwenhoek 78(3-4):315–321
70. Zees AC, Pyrpassopoulos S, Vorgias CE (2009) Insights into the role of the (alpha + beta) 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
71. Zhang G, Ge H (2013) Protein hypersaline adaptation: insight from amino acids with machine learning algorithms. Protein J 32:239–245