Psychrotolerant Paenibacillus tundrae isolates from barley grains produce new cereulide-like depsipeptides (Paenilide and Homopaenilide) that are highly toxic to mammalian cells

Applied and Environmental Microbiology

Volumn 78, Issue 10, 2012, Pages 3732-3743

  Rasimus, Stiina ^a   Mikkola, Raimo ^a   Andersson, Maria A ^a   Teplova, Vera V ^a,b   Venediktova, Natalia ^b   Ek Kommonen, Christine ^c   Salkinoja Salonen, Mirja ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b INSTITUTE OF THEORETICAL AND EXPERIMENTAL BIOPHYSICS   (Russian Federation)

^c NATL VET AND FOOD RES INSTITUTE   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

CATIONIC COMPOUNDS; DEPSIPEPTIDES; ELECTROCONDUCTIVE; GLUCOSE CONSUMPTION; LIPID MEMBRANES; LIPOPHILICITY; MAMMALIAN CELLS; METABOLIC ACIDOSIS; MITOCHONDRIAL MEMBRANE POTENTIAL; NANOMOLAR CONCENTRATION; PCR ASSAY; PEPTIDE TOXIN; POTASSIUM IONS; PSYCHROTOLERANT; RAT LIVER MITOCHONDRIA; RESPIRATORY CONTROL; STRUCTURAL DIFFERENCES; TANDEM MASS SPECTRA; TOXIC EFFECT; TWO-COMPONENT; WET WEIGHT;

BACILLUS CEREUS; BIOCHEMISTRY; ELECTRIC CONDUCTIVITY; GENE ENCODING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; POLYMERASE CHAIN REACTION; RAT CONTROL;

MITOCHONDRIA;

BACTERIAL DNA; CEREULIDE; DEPSIPEPTIDE; RIBOSOME DNA; RNA 16S;

BACTERIUM; BARLEY; COLONIZATION; FOOD POISONING; INHIBITION; LIQUID CHROMATOGRAPHY; MEMBRANE; MOTILITY; PEPTIDE; TOXIN;

ANIMAL; ARTICLE; BACILLUS CEREUS; CHEMISTRY; CLASSIFICATION; COLD; DNA SEQUENCE; DRUG EFFECT; ENZYMOLOGY; EPITHELIUM CELL; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HORDEUM; ISOLATION AND PURIFICATION; MALE; MASS SPECTROMETRY; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MOLECULAR WEIGHT; MOUSE; NUCLEOTIDE SEQUENCE; PAENIBACILLUS; RAT; SPERMATOZOON; SWINE;

ANIMALS; BACILLUS CEREUS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COLD TEMPERATURE; DEPSIPEPTIDES; DNA, BACTERIAL; DNA, RIBOSOMAL; EPITHELIAL CELLS; HORDEUM; MALE; MASS SPECTROMETRY; MICE; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; PAENIBACILLUS; RATS; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SPERMATOZOA; SWINE;

BACILLUS CEREUS; HORDEUM; MAMMALIA; MURINAE; PAENIBACILLUS; RATTUS; SUS;

EID: 84861162325     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00049-12     Document Type: Article

References (67)

1. Andersson MA, et al. 2004. Sperm bioassay for rapid detection of cereulide-producing Bacillus cereus in food and related environments. Int. J. Food Microbiol. 94:175-183. doi:10.1016/j.ijfoodmicro.2004.01.018.
2. Andersson MA, et al. 2010. Boar spermatozoa as a biosensor for detecting toxic substances in indoor dust and aerosols. Toxicol. In Vitro 24:2041-2052. doi:10.1016/j.tiv.2010.08.011.
3. Antunez K, Anido M, Evans JD, Zunino P. 2010. Secreted and immunogenic proteins produced by the honeybee bacterial pathogen, Paenibacillus larvae. Vet. Microbiol. 141:385-389. doi:10.1016/j.vetmic.2009.09.006.
4. Apetroaie-Constantin C, et al. 2009. Bacillus subtilis and B. mojavensis strains connected to food poisoning produce the heat stable toxin amylosin. J. Appl. Microbiol. 106:1976-1985. doi:10.1111/j.1365-2672.2009.04167.x.
5. Apetroaie-Constantin C, et al. 2008. Environment driven cereulide production by emetic strains of Bacillus cereus. Int. J. Food Microbiol. 127: 60-67. doi:10.1016/j.ijfoodmicro.2008.06.006.
6. Ash C, Priest FG, Collins MD. 1993. Molecular identification of rRNA group 3 bacilli (Ash, Farrow, Wallbanks and Collins) using a PCR probe test. Proposal for the creation of a new genus Paenibacillus. Antonie Van Leeuwenhoek 64:253-260.
7. Atlas RM. 1993. Handbook of microbiological media. CRC Press, Boca Raton, FL.
8. Carlin F, et al. 2000. Spore-forming bacteria in commercial cooked, pasteurised and chilled vegetable purees. Food Microbiol. 17:153-165. doi:10.1006/fmic.1999.0299.
9. Chan QW, Melathopoulos AP, Pernal SF, Foster LJ. 2009. The innate immune and systemic response in honey bees to a bacterial pathogen, Paenibacillus larvae. BMC Genomics 10:387. doi:10.1186/1471-2164-10-387.
10. De Jonghe V, et al. 2010. Toxinogenic and spoilage potential of aerobic spore-formers isolated from raw milk. Int. J. Food Microbiol. 136:318-325. doi:10.1016/j.ijfoodmicro.2009.11.007.
11. Delbrassinne L, et al. 2011. Follow-up of the Bacillus cereus emetic toxin production in penne pasta under household conditions using liquid chromatography coupled with mass spectrometry. Food Microbiol. 28:1105-1109. doi:10.1016/j.fm.2011.02.014.
12. Deng Y, et al. 2011. Isolation and characterization of peptide antibiotics LI-F04 and polymyxin B(6) produced by Paenibacillus polymyxa strain JSa-9. Peptides 32:1917-1923. doi:10.1016/j.peptides.2011.08.004.
13. Dierick K, et al. 2005. Fatal family outbreak of Bacillus cereus-associated food poisoning. J. Clin. Microbiol. 43:4277-4279. doi:10.1128/JCM.43.8.4277-4279.2005.
14. Echard G. 1974. Chromosomal banding patterns and karyotype evolution in three pig kidney cell strains (PK15, F and RP). Chromosoma 45:133-149.
15. Edwards U, Rogall T, Blocker H, Emde M, Bottger EC. 1989. Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res. 17: 7843-7853.
16. Ehling-Schulz M, et al. 2006. Cereulide synthetase gene cluster from emetic Bacillus cereus: structure and location on a mega virulence plasmid related to Bacillus anthracis toxin plasmid pXOI. BMC Microbiol. 6:20. doi:10.1186/1471-2180-6-20.
17. Ehling-Schulz M, Fricker M, Scherer S. 2004. Identification of emetic toxin producing Bacillus cereus strains by a novel molecular assay. FEMS Microbiol. Lett. 232:189-195. doi:10.1016/S0378-1097(04)00066-7.
18. Elo S, Maunuksela L, Salkinoja-Salonen M, Smolander A, Haahtela K. 2000. Humus bacteria of Norway spruce stands: plant growth promoting properties and birch, red fescue and alder colonizing capacity. FEMS Microbiol. Ecol. 31:143-152.
19. Fangio MF, Roura SI, Fritz R. 2010. Isolation and identification of Bacillus spp. and related genera from different starchy foods. J. Food Sci. 75:M218-M221. doi:10.1111/j.1750-3841.2010.01566.x.
20. Fricker M, Reissbrodt R, Ehling-Schulz M. 2008. Evaluation of standard and new chromogenic selective plating media for isolation and identification of Bacillus cereus. Int. J. Food Microbiol. 121:27-34. doi:10.1016/ j.ijfoodmicro.2007.10.012.
21. Fromm HI, Boor KJ. 2004. Characterization of pasteurized fluid milk shelf-life attributes. J. Food Sci. 69:M207-M214.
22. Girardin H, Albagnac C, Dargaignaratz C, Nguyen-The C, Carlin F. 2002. Antimicrobial activity of foodborne Paenibacillus and Bacillus spp. against Clostridium botulinum. J. Food Prot. 65:806-813.
23. Guinebretiere MH, et al. 2001. Identification of bacteria in pasteurized zucchini purees stored at different temperatures and comparison with those found in other pasteurized vegetable purees. Appl. Environ. Microbiol. 67:4520-4530.
24. Häggblom MM, Apetroaie C, Andersson MA, Salkinoja-Salonen MS. 2002. Quantitative analysis of cereulide, the emetic toxin of Bacillus cereus, produced under various conditions. Appl. Environ. Microbiol. 68:2479-2483. doi:10.1128/AEM.68.5.2479-2483.2002.
25. Hansen BM, Leser TD, Hendriksen NB. 2001. Polymerase chain reaction assay for the detection of Bacillus cereus group cells. FEMS Microbiol. Lett. 202:209-213.
26. He Z, et al. 2007. Isolation and identification of a Paenibacillus polymyxa strain that coproduces a novel lantibiotic and polymyxin. Appl. Environ. Microbiol. 73:168-178. doi:10.1128/AEM.02023-06.
27. Hoornstra D, Andersson MA, Mikkola R, Salkinoja-Salonen MS. 2003. A new method for in vitro detection of microbially produced mitochondrial toxins. Toxicol. In Vitro 17:745-751.
28. Hoton FM, Andrup L, Swiecicka I, Mahillon J. 2005. The cereulide genetic determinants of emetic Bacillus cereus are plasmid-borne. Microbiology 151:2121-2124. doi:10.1099/mic.0.28069-0.
29. Hoton FM, et al. 2009. Family portrait of Bacillus cereus and Bacillus weihenstephanensis cereulide-producing strains. Environ. Microbiol. Rep. 1:177-183. doi:10.1111/j.1758-2229.2009.00028.x.
30. Huck JR, Sonnen M, Boor KJ. 2008. Tracking heat-resistant, coldthriving fluid milk spoilage bacteria from farm to packaged product. J. Dairy Sci. 91:1218-1228. doi:10.3168/jds.2007-0697.
31. Huck JR, Woodcock NH, Ralyea RD, Boor KJ. 2007. Molecular subtyping and characterization of psychrotolerant endospore-forming bacteria in two New York State fluid milk processing systems. J. Food Prot. 70: 2354-2364.
32. Hunt ME, Rice EW. 2005. Microbiological examination, p 9-35-9-52. In Eaton AD, Clesceri LS, Rice EW, Greenberg AE (ed), Standard methods for the examination of water and wastewater, 21st ed. Port City Press, Baltimore, MD.
33. Ichikawa K, et al. 2010. Acute encephalopathy of Bacillus cereus mimicking Reye syndrome. Brain Dev. 32:688-690. doi:10.1016/j.braindev.2009.09.004.
34. Izumi H, Anderson IC, Killham K, Moore ERB. 2008. Diversity of predominant endophytic bacteria in European deciduous and coniferous trees. Can. J. Microbiol. 54:173-179. doi:10.1139/W07-134.
35. Jääskeläinen EL, et al. 2003. In vitro assay for human toxicity of cereulide, the emetic mitochondrial toxin produced by food poisoning Bacillus cereus. Toxicol. In Vitro 17:737-744.
36. Jestoi M, et al. 2004. Presence and concentrations of the Fusarium-related mycotoxins beauvericin, enniatins and moniliformin in Finnish grain samples. Food Addit. Contam. 21:794-802. doi:10.1080/02652030410001713906.
37. Johnson D, Lardy H. 1967. Isolation of liver or kidney mitochondria. Methods Enzymol. 10:94-96.
38. Kamo N, Muratsugu M, Hongoh R, Kobatake Y. 1979. Membrane potential of mitochondria measured with an electrode sensitive to tetraphenyl phosphonium and relationship between proton electrochemical potential and phosphorylation potential in steady state. J. Membr. Biol. 49:105-121.
39. Lal S, Tabacchioni S. 2009. Ecology and biotechnological potential of Paenibacillus polymyxa: a minireview. Indian J. Microbiol. 49:2-10. doi: 10.1007/s12088-009-0008-y.
40. Logan NA, et al. 2004. Paenibacillus cineris sp. nov. and Paenibacillus cookii sp. nov., from Antarctic volcanic soils and a gelatin-processing plant. Int. J. Syst. Evol. Microbiol. 54:1071-1076. doi:10.1099/ijs.0.02967-0.
41. Ma M, et al. 2011. Complete genome sequence of Paenibacillus polymyxa SC2, a strain of plant growth-promoting rhizobacterium with broadspectrum antimicrobial activity. J. Bacteriol. 193:311-312. doi:10.1128/JB.01234-10.
42. Mageshwaran V, Walia S, Govindasamy V, Annapurna K. 2011. Antibacterial activity of metabolite produced by Paenibacillus polymyxa strain HKA-15 against Xanthomonas campestris pv. phaseoli. Indian J. Exp. Biol. 49:229-233.
43. Mahler H, et al. 1997. Fulminant liver failure in association with the emetic toxin of Bacillus cereus. N. Engl. J. Med. 336:1142-1148. doi: 10.1056/NEJM199704173361604.
44. McFaddin JF. 2000. Biochemical tests for identification of medical bacteria. Lippincott Williams & Wilkins, Philadelphia, PA.
45. Mehta R, Chan K, Lee O, Tafazoli S, O'Brien PJ. 2008. Drugassociated mitochondrial toxicity, p 71-126. In Dykens JA, Will Y (ed), Drug-induced mitochondrial dysfunction. John Wiley & Sons Inc, Hoboken, NJ.
46. Mikkola R, Saris NE, Grigoriev PA, Andersson MA, Salkinoja-Salonen MS. 1999. Ionophoretic properties and mitochondrial effects of cereulide- the emetic toxin of B. cereus. Eur. J. Biochem. 263:112-117.
47. Naghmouchi K, et al. 2011. Paenibacillus polymyxa JB05-01-1 and its perspectives for food conservation and medical applications. Arch. Microbiol. 193:169-177. doi:10.1007/s00203-010-0654-9.
48. Naranjo M, et al. 2011. Sudden death of a young adult associated with Bacillus cereus food poisoning. J. Clin. Microbiol. 49:4379-4381. doi: 10.1128/JCM.05129-11.
49. Nelson DM, Glawe AJ, Labeda DP, Cann IK, Mackie RI. 2009. Paenibacillus tundrae sp. nov. and Paenibacillus xylanexedens sp. nov., psychrotolerant, xylan-degrading bacteria from Alaskan tundra. Int. J. Syst. Evol. Microbiol. 59:1708-1714. doi:10.1099/ijs.0.004572-0.
50. Ouyang J, et al. 2008. Paenibacillus thiaminolyticus: a new cause of human infection, inducing bacteremia in a patient on hemodialysis. Ann. Clin. Lab. Sci. 38:393-400.
51. Pettit GR, et al. 2009. Antineoplastic agents. 570. Isolation and structure elucidation of bacillistatins 1 and 2 from a marine Bacillus silvestris. J. Nat. Prod. 72:366-371. doi:10.1021/np800603u.
52. Pitchayawasin S, et al. 2004. Molecular diversity of cereulide detected by means of nano-HPLC-ESI-Q-TOF-MS. Int. J. Mass Spectrom. 235:123-129. doi:10.1016/j.ijms.2004.04.007.
53. Pósfay-Barbe KM, et al. 2008. Food poisoning as a cause of acute liver failure. Pediatr. Infect. Dis. J. 27:846-847. doi:10.1097/INF.0b013e318170f2ae.
54. Rasimus S, Kolari M, Rita H, Hoornstra D, Salkinoja-Salonen M. 2011. Biofilm-forming bacteria with varying tolerance to peracetic acid from a paper machine. J. Ind. Microbiol. Biotechnol. 38:1379-1390. doi:10.1007/s10295-010-0921-4.
55. Rasko DA, et al. 2007. Complete sequence analysis of novel plasmids from emetic and periodontal Bacillus cereus isolates reveals a common evolutionary history among the B. cereus-group plasmids, including Bacillus anthracis pXO1. J. Bacteriol. 189:52-64. doi:10.1128/JB.01313-06.
56. Roux V, Raoult D. 2004. Paenibacillus massiliensis sp. nov., Paenibacillus sanguinis sp. nov. and Paenibacillus timonensis sp. nov., isolated from blood cultures. Int. J. Syst. Evol. Microbiol. 54:1049-1054. doi:10.1099/ijs.0.02954-0.
57. Shiota M, et al. 2010. Rapid detoxification of cereulide in Bacillus cereus food poisoning. Pediatrics 125:e951-e955. doi:10.1542/peds.2009-2319.
58. Sirota-Madi A, et al. 2010. Genome sequence of the pattern forming Paenibacillus vortex bacterium reveals potential for thriving in complex environments. BMC Genomics 11:710. doi:10.1186/1471-2164-11-710.
59. Teplova VV, Mikkola R, Tonshin AA, Saris NE, Salkinoja-Salonen MS. 2006. The higher toxicity of cereulide relative to valinomycin is due to its higher affinity for potassium at physiological plasma concentration. Toxicol. Appl. Pharmacol. 210:39-46. doi:10.1016/j.taap.2005.06.012.
60. Teplova VV, Tonshin AA, Grigoriev PA, Saris NE, Salkinoja-Salonen MS. 2007. Bafilomycin A1 is a potassium ionophore that impairs mitochondrial functions. J. Bioenerg. Biomembr. 39:321-329. doi:10.1007/s10863-007-9095-9.
61. Thorsen L, Budde BB, Henrichsen L, Martinussen T, Jakobsen M. 2009. Cereulide formation by Bacillus weihenstephanensis and mesophilic emetic Bacillus cereus at temperature abuse depends on pre-incubation conditions. Int. J. Food Microbiol. 134:133-139. doi:10.1016/j.ijfoodmicro.2009.03.023.
62. Thorsen L, et al. 2006. Characterization of emetic Bacillus weihenstephanensis, a new cereulide-producing bacterium. Appl. Environ. Microbiol. 72:5118-5121. doi:10.1128/AEM.00170-06.
63. Trivedi P, Spann T, Wang N. 2011. Isolation and characterization of beneficial bacteria associated with citrus roots in Florida. Microb. Ecol. 62:324-336. doi:10.1007/s00248-011-9822-y.
64. Tupinamba G, et al. 2008. Antimicrobial activity of Paenibacillus polymyxa SCE2 against some mycotoxin-producing fungi. J. Appl. Microbiol. 105:1044-1053. doi:10.1111/j.1365-2672.2008.03844.x.
65. Wang GYS, Kuramoto M, Yamada K, Yazawa K, Uemura D. 1995. Homocereulide, an extremely potent cytotoxic depsipeptide from the marine bacterium Bacillus cereus. Chem. Lett. 24:791-792. doi:10.1246/cl.1995.791.
66. Wu XC, et al. 2011. Paenimacrolidin, a novel macrolide antibiotic from Paenibacillus sp. F6-B70 active against methicillin-resistant Staphylococcus aureus. Microb. Biotechnol. 4:491-502. doi:10.1111/j.1751-7915.2010.00201.x.
67. Wu XC, et al. 2010. Isolation and partial characterization of antibiotics produced by Paenibacillus elgii B69. FEMS Microbiol. Lett. 310:32-38. doi:10.1111/j.1574-6968.2010.02040.x.