Lichenysin is produced by most Bacillus licheniformis strains

Journal of Applied Microbiology

Volumn 115, Issue 4, 2013, Pages 1068-1080

  Madslien, E H ^a,b   Ronning H T ^b   Lindback T ^b   Hassel, B ^a   Andersson, M A ^c   Granum, P E ^b  

^a NORWEGIAN DEFENCE RESEARCH ESTABLISHMENT FFI   (Norway)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Bacillus; Cytotoxicity; Food safety; Genotyping

Indexed keywords

BACTERIOLOGY; FOOD SAFETY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; POLYMERASE CHAIN REACTION; RISK ASSESSMENT;

BACILLUS LICHENIFORMIS; FOOD-SAFETY; GENE FRAGMENTS; GENOTYPING; LC-MS-MS; LICHENYSIN; LIQUID CHROMATOGRAPHY-TANDEM MASS SPECTROMETRY; LIQUID CHROMATOGRAPHY/TANDEM MASS SPECTROMETRY; MASS SPECTROMETRY ANALYSIS; ORDERS OF MAGNITUDE;

CYTOTOXICITY;

BACTERIAL PROTEIN; CELL EXTRACT; LICHENYSIN; UNCLASSIFIED DRUG;

BACTERIUM; FOOD SAFETY; GENE; GENOTYPE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; POLYMERASE CHAIN REACTION; TOXICITY;

ANIMAL CELL; ARTICLE; BACILLUS LICHENIFORMIS; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL STRAIN; CONTROLLED STUDY; CYTOTOXICITY; ERYTHROCYTE; GENOTYPE; HEMOLYSIS; LCHAA BACTERIAL GENE; LIQUID CHROMATOGRAPHY; MOLECULAR WEIGHT; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN ANALYSIS; SPERMATOZOON; TANDEM MASS SPECTROMETRY; VERO CELL;

BACILLUS LICHENIFORMIS;

BACILLUS; CYTOTOXICITY; FOOD SAFETY; GENOTYPING;

ANIMALS; BACILLUS; CERCOPITHECUS AETHIOPS; HEMOLYSIS; LIGASES; LIPOPROTEINS; PEPTIDES, CYCLIC; TANDEM MASS SPECTROMETRY; VERO CELLS;

EID: 84884974392     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12299     Document Type: Article

References (56)

1. Agerholm, J.S., Krogh, H.V. and Jensen, H.E. (1995) A retrospective study of bovine abortions associated with Bacillus licheniformis. J Vet Med Ser B 42, 225-234.
2. Agerholm, J.S., Jensen, N.E., Dantzer, V., Jensen, H.E. and Aarestrup, F.M. (1999) Experimental infection of pregnant cows with Bacillus licheniformis bacteria. Vet Pathol 36, 191-201.
3. Andersson, M.A., Mikkola, R., Helin, J., Andersson, M.C. and Salkinoja-Salonen, M. (1998) A novel sensitive bioassay for detection of Bacillus cereus emetic toxin and related depsipeptide ionophores. Appl Environ Microbiol 64, 1338-1343.
4. Apetroaie-Constantin, C., Mikkola, R., Andersson, M.A., Teplova, V., Suominen, I., Johansson, T. and Salkinoja-Salonen, M. (2009) Bacillus subtilis and B mojavensis strains connected to food poisoning produce the heat stable toxin amylosin. J Appl Microbiol 106, 1976-1985.
5. Arima, K., Kakinuma, A. and Tamura, G. (1968) Surfactin, a crystalline peptidelipid surfactant produced by Bacillus subtilis: isolation, characterization and its inhibition of fibrin clot formation. Biochem Biophys Res Commun 31, 488.
6. Cutting, S.M. (2011) Bacillus probiotics. Food Microbiol 28, 214-220.
7. Fagerlund, A., Lindbäck, T., Storset, A.K., Granum, P.E. and Hardy, S.P. (2008) Bacillus cereus Nhe is a pore-forming toxin with structural and functional properties similar to the ClyA (HlyE, SheA) family of haemolysins, able to induce osmotic lysis in epithelia. Microbiology 154, 693-704.
8. From, C., Pukall, R., Schumann, P., Hormazábal, V. and Granum, P.E. (2005) Toxin-producing ability among Bacillus spp. outside the Bacillus cereus group. Appl Environ Microbiol 71, 1178-1183.
9. From, C., Hormazabal, V., Hardy, S.P. and Granum, P.E. (2007) Cytotoxicity in Bacillus mojavensis is abolished following loss of surfactin synthesis: implications for assessment of toxicity and food poisoning potential. Int J Food Microbiol 117, 43-49.
10. Grangemard, I., Bonmatin, J.M., Bernillon, J., Das, B.C. and Peypoux, F. (1999) Lichenysins G, a novel family of lipopeptide biosurfactants from Bacillus licheniformis IM 1307: production, isolation and structural evaluation by NMR and mass spectrometry. J Antibiot 52, 363.
11. Hoornstra, D., Andersson, M.A., Mikkola, R. and Salkinoja-Salonen, M.S. (2003) A new method for in vitro detection of microbially produced mitochondrial toxins. Toxicol In Vitro 17, 745-751.
12. Hsieh, F.C., Li, M.C., Lin, T.C. and Kao, S.S. (2004) Rapid detection and characterization of surfactin-producing Bacillus subtilis and closely related species based on PCR. Curr Microbiol 49, 186-191.
13. Hwang, Y.-H., Kim, M.-S., Song, I.-B., Park, B.-K., Lim, J.G.-H., Park, S.-C. and Yun, H.-I. (2009) Subacute (28 day) toxicity of surfactin C, a lipopeptide produced by Bacillus subtilis, in rats. J Health Sci 55, 351-355.
14. Ishihara, H., Takoh, M., Nishibayashi, R. and Sato, A. (2002) Distribution and variation of bacitracin synthetase gene sequences in laboratory stock strains of Bacillus licheniformis. Curr Microbiol 45, 18-23.
15. Jacques, P. (2011) Surfactin and other lipopeptides from Bacillus spp. In Biosurfactants: From Genes to Applications ed. Steinbüchel, A. and Soberón-Chávez, G. pp. 57-93. New York: Springer.
16. Jolley, K.A., Feil, E.J., Chan, M.S. and Maiden, M.C. (2001) Sequence type analysis and recombinational tests (START). Bioinformatics 17, 1230-1231.
17. Joshi, S., Yadav, S. and Desai, A.J. (2008) Application of response-surface methodology to evaluate the optimum medium components for the enhanced production of lichenysin by Bacillus licheniformis R2. Biochem Eng J 41, 122-127.
18. Kramer, J.M. and Gilbert, R.J. (1989) Bacillus cereus and other Bacillus species. In Foodborne Bacterial Pathogens ed. Doyle, M.P. pp. 21-70. New York Marcel Dekker, Inc.
19. Kramer, J.M., Turnbull, P.C.B., Munshi, G. and Gilbert, R.J. (1982) Identification and characterization of Bacillus cereus and other Bacillus species associated with food poisoning. In Isolation and Identification Methods for Food Poisoning Organisms ed. Corry, J.E.L., Roberts, D. and Skinner, F.A. pp. 261-286. London: Society for applied bacteriology technical series.
20. Logan, N.A. (1988) Bacillus species of medical and veterinary importance. J Med Microbiol 25, 157-165.
21. Logan, N.A. (2012) Bacillus and relatives in foodborne illness. J Appl Microbiol 112, 417-429.
22. Logan, N.A. and De Vos, P. (2009) Genus I. Bacillus. In Bergey's Manual of Systematic Bacteriology ed. De Vos, P., Garrity, G.M., Jones, D., Krieg, N.R., Ludwig, W., Rainey, F.A., Schleifer, K. and Whitman, W.B. pp. 21-128. New York: Springer.
23. Madslien, E.H., Olsen, J.S., Granum, P.E. and Blatny, J.M. (2012) Genotyping of B. licheniformis based on a novel multi-locus sequence typing (MLST) scheme. BMC Microbiol 12, 230.
24. Maughan, H. and Nicholson, W.L. (2011) Increased fitness and alteration of metabolic pathways during Bacillus subtilis evolution in the laboratory. Appl Environ Microbiol 77, 4105-4118.
25. Mikkola, R., Saris, N.-E.L., Grigoriev, P.A., Andersson, M.A. and Salkinoja-Salonen, M.S. (1999) Ionophoretic properties and mitochondrial effects of cereulide. Eur J Biochem 263, 112-117.
26. Mikkola, R., Kolari, M., Andersson, M.A., Helin, J. and Salkinoja-Salonen, M.S. (2000) Toxic lactonic lipopeptide from food poisoning isolates of Bacillus licheniformis. Eur J Biochem 267, 4068-4074.
27. Morikawa, M., Hirata, Y. and Imanaka, T. (2000) A study on the structure-function relationship of lipopeptide biosurfactants. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of. Lipids 1488, 211-218.
28. Naruse, N., Tenmyo, O., Kobaru, S., Kamei, H., Miyaki, T., Konishi, M. and Oki, T. (1990) Pumilacidin, a complex of new antiviral antibiotics. Production, isolation, chemical properties, structure and biological activity. J Antibiot 43, 267.
29. Nei, M. and Gojobori, T. (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3, 418-426.
30. Nicholson, W.L., Munakata, N., Horneck, G., Melosh, H.J. and Setlow, P. (2000) Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol Rev 64, 548-572.
31. Nieminen, T., Rintaluoma, N., Andersson, M., Taimisto, A.M., Ali-Vehmas, T., Seppälä, A., Priha, O. and Salkinoja-Salonen, M. (2007) Toxinogenic Bacillus pumilus and Bacillus licheniformis from mastitic milk. Vet Microbiol 124, 329-339.
32. Park, B.K., Lim, J.H., Hwang, Y.H., Kim, M.S., Song, I.B., Lee, H.G., Han, S.J., Hwang, M.H. et al. (2006) Acute oral toxicity of surfactin C in mice. J Toxicol Public Health 22, 405-408.
33. Rey, M.W., Ramaiya, P., Nelson, B.A., Brody-Karpin, S.D., Zaretsky, E.J., Tang, M., Lopez de Leon, A., Xiang, H. et al. (2004) Complete genome sequence of the industrial bacterium Bacillus licheniformis and comparisons with closely related Bacillus species. Genome Biol 5, r77.
34. Rozen, S. and Skaletsky, H. (1999) Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics Methods and Protocols ed. Misener, S. and Kravetz, S.A. pp.365-386. Totowa: Humana Press Inc.
35. Saitou, N. and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406-425.
36. Salkinoja-Salonen, M.S., Vuorio, R., Andersson, M.A., Kampfer, P., Andersson, M.C., Honkanen-Buzalski, T. and Scoging, A.C. (1999) Toxigenic strains of Bacillus licheniformis related to food poisoning. Appl Environ Microbiol 65, 4637-4645.
37. Sandvig, K. and Olsnes, S. (1982) Entry of the toxic proteins abrin, modeccin, ricin, and diphtheria toxin into cells. I. Requirement for calcium. J Biol Chem 257, 7495-7503.
38. Santini, F., Borghetti, V., Amalfitano, G. and Mazzucco, A. (1995) Bacillus licheniformis prosthetic aortic valve endocarditis. J Clin Microbiol 33, 3070-3073.
39. Schallmey, M., Singh, A. and Ward, O.P. (2004) Developments in the use of Bacillus species for industrial production. Can J Microbiol 50, 1-17.
40. Shaligram, N.S. and Singhal, R.S. (2010) Surfactin- A Review on Biosynthesis, Fermentation, Purification and Applications. Food Technol Biotechnol 48, 119-134.
41. Sheppard, J.D., Jumarie, C., Cooper, D.G. and Laprade, R. (1991) Ionic channels induced by surfactin in planar lipid bilayer membranes. Biochim Biophys Acta 1064, 13-23.
42. Stachelhaus, T. and Marahiel, M.A. (2006) Modular structure of genes encoding multifunctional peptide synthetases required for non-ribosomal peptide synthesis. FEMS Microbiol Lett 125, 3-14.
43. Stachelhaus, T., Mootz, H.D., Bergendahl, V. and Marahiel, M.A. (1998) Peptide bond formation in nonribosomal peptide biosynthesis: catalytic role of the condensation domain. J Biol Chem 273, 22773-22781.
44. Staden, R. (1996) The staden sequence analysis package. Mol Biotechnol 5, 233-241.
45. Stenfors Arnesen, L.P., Fagerlund, A. and Granum, P.E. (2008) From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol Rev 32, 579-606.
46. Sugar, A.M. and McCloskey, R.V. (1977) Bacillus licheniformis sepsis. JAMA 238, 1180.
47. Syrjälä, P., Anttila, M., Dillard, K., Fossi, M., Collin, K., Nylund, M. and Autio, T. (2007) Causes of bovine abortion, stillbirth and neonatal death in Finland. Acta Vet Scand 49, S3.
48. Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24, 1596-1599.
49. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28, 2731-2739.
50. Tapi, A., Chollet-Imbert, M., Scherens, B. and Jaques, P. (2009) New approach for detection of non-ribosomal peptide synthetase genes in Bacillus strains by polymerase chain reaction. Appl Microbiol Biotechnol 85, 1521-1531.
51. Taylor, J.M.W., Sutherland, A.D., Aidoo, K.E. and Logan, N.A. (2005) Heat-stable toxin production by strains of Bacillus cereus, Bacillus firmus, Bacillus megaterium, Bacillus simplex and Bacillus licheniformis. FEMS Microbiol Lett 242, 313-317.
52. Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680.
53. Turgay, K. and Marahiel, M.A. (1994) A general approach for identifying and cloning peptide synthetase genes. Pept Res 7, 238-241.
54. Yakimov, M.M., Timmis, K.N., Wray, V. and Fredrickson, H.L. (1995) Characterization of a new lipopeptide surfactant produced by thermotolerant and halotolerant subsurface Bacillus licheniformis BAS50. Appl Environ Microbiol 61, 1706-1713.
55. Yakimov, M.M., Abraham, W.R., Meyer, H., Laura, G. and Golyshin, P.N. (1999) Structural characterization of lichenysin A components by fast atom bombardment tandem mass spectrometry. Biochimica et Biophysica Acta (BBA)- Molecular and Cell Biology of. Lipids 1438, 273-280.
56. Youssef, N.H., Duncan, K.E., Nagle, D.P., Savage, K.N., Knapp, R.M. and McInerney, M.J. (2004) Comparison of methods to detect biosurfactant production by diverse microorganisms. J Microbiol Methods 56, 339-347.