3 research outputs found

    Potential Enterotoxicity of Phylogenetically Diverse Bacillus cereus Sensu Lato Soil Isolates from Different Geographical Locations

    Get PDF
    Bacillus cereus sensu lato comprises Gram-positive spore-forming bacteria producing toxins associated with foodborne diseases. Three pore-forming enterotoxins, nonhemolytic enterotoxin (Nhe), hemolysin BL (Hbl), and cytotoxin K (CytK), are considered the primary factors in B. cereus sensu lato diarrhea. The aim of this study was to determine the potential risk of enterotoxicity among soil B. cereus sensu lato isolates representing diverse phylogroups and originated from different geographic locations with various climates (Burkina Faso, Kenya, Argentina, Kazakhstan, and Poland). While nheA- and hblA-positive isolates were present among all B. cereus sensu lato populations and distributed across all phylogenetic groups, cytK-2-positive strains predominated in geographic regions with an arid hot climate (Africa) and clustered together on a phylogenetic tree mainly within mesophilic groups III and IV. The highest in vitro cytotoxicity to Caco-2 and HeLa cells was demonstrated by the strains clustered within phylogroups II and IV. Overall, our results suggest that B. cereus sensu lato pathogenicity is a comprehensive process conditioned by many intracellular factors and diverse environmental conditions.Izabela ÅšwiÄ™cicka - [email protected] Drewnowska - Department of Microbiology, Faculty of Biology, University of Bialystok, Bialystok, PolandNatalia StefaÅ„ska - Department of Microbiology, Faculty of Biology, University of Bialystok, Bialystok, PolandMagdalena Czerniecka - Department of Cytobiochemistry, Faculty of Biology, University of Bialystok, Bialystok, Poland; Laboratory of Tissue Culture, Faculty of Biology, University of Bialystok, Bialystok, PolandGrzegorz Zambrowski - Laboratory of Applied Microbiology, University of Bialystok, Bialystok, PolandIzabela ÅšwiÄ™cicka - Department of Microbiology, Faculty of Biology, University of Bialystok, Bialystok, Poland; Laboratory of Applied Microbiology, University of Bialystok, Bialystok, PolandMock M, Fouet A. 2001. Anthrax. Annu Rev Microbiol 55:647–671. https://doi.org/10.1146/annurev.micro.55.1.647Murawska E, Fiedoruk K, Swiecicka I. 2014. Modular genetic architecture of the toxigenic plasmid pIS56-63 harboring cry1Ab21 in Bacillus thuringiensis subsp. thuringiensis strain IS5056. Pol J Microbiol 63:147–156. https://doi.org/10.33073/pjm-2014-020.Stenfors Arnesen LP, Fagerlund A, Granum PE. 2008. From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol Rev 32: 579 – 606. https://doi.org/10.1111/j.1574-6976.2008.00112.x.Dierick K, Van Coillie E, Swiecicka I, Meyfroidt G, Devlieger H, Meulemans A, Hoedemaekers G, Fourie L, Heyndrickx M, Mahillon J. 2005. Fatal family outbreak of Bacillus cereus-associated food poisoning. J Clin Microbiol 43:4277– 4279. https://doi.org/10.1128/JCM.43.8.4277-4279.2005.Swiecicka I, Bideshi DK, Federici BA. 2008. Novel isolate of Bacillus thuringiensis subsp. thuringiensis that produces a quasi-cuboidal crystal of Cry1Ab21 toxic to larvae of Trichoplusia ni. Appl Environ Microbiol 74:923–930. https://doi.org/10.1128/AEM.01955-07.Guinebretiere M-H, Auger S, Galleron N, Contzen M, De Sarrau B, De Buyser M-L, Lamberet G, Fagerlund A, Granum PE, Lereclus D, De Vos P, Nguyen-The C, Sorokin A. 2013. Bacillus cytotoxicus sp. nov. is a novel thermotolerant species of the Bacillus cereus group occasionally associated with food poisoning. Int J Syst Evol Micriobiol 63:31– 40. https://doi.org/10.1099/ijs.0.030627-0.Miller R, Beno SM, Kent DJ, Carroll LM, Martin NM, Boor KJ, Kovac J. 2016. Bacillus wiedmannii sp. nov., a psychrotolerant and cytotoxic Bacillus cereus group species isolated from dairy foods and dairy environments. Int J Syst Evol Microbiol 66:4744 – 4753. https://doi.org/10.1099/ijsem.0.001421.Jiménez G, Blanch AR, Tamames J, Rosselló-Mora R. 2013. Complete genome sequence of Bacillus toyonnsis BCT-7112T, the active ingredient of the feed additive preparation Toyocerin. Genome Announc 1:e01080-13. https://doi.org/10.1128/genomeA.01080-13.Lechner S, Mayr R, Francis KP, Prüss BM, Kaplan T, Wiessner-Gunkel E, Stewart GS, Scherer S. 1998. Bacillus weihenstephanensis sp. nov. is a new psychrotolerant species of the Bacillus cereus group. Int J Syst Evol Microbiol 48:1373–1382. https://doi.org/10.1099/00207713-48-4-1373.Nakamura LK. 1998. Bacillus pseudomycoides sp. nov. Int J Syst Evol Microbiol 48:1031–1035. https://doi.org/10.1099/00207713-48-3-1031.Liu Y, Lai Q, Shao Z. 2018. Genome analysis-based reclassification of Bacillus weihenstephanensis as a later heterotypic synonym of Bacillus mycoides. Int J Syst Evol Microbiol 68:106 –112. https://doi.org/10.1099/ijsem.0.002466.Thorsen L, Hansen BM, Nielsen KF, Hendriksen NB, Phipps RK, Budde BB. 2006. Characterization of emetic Bacillus weihenstephanensis, a new cereulide-producing bacterium. Appl Environ Microbiol 72:5118 –5121.https://doi.org/10.1128/AEM.00170-06.Jung MY, Kim JS, Paek WK, Lim J, Lee H, Kim PI, Ma JY, Kim W, Chan YH. 2011. Bacillus manliponensis sp. nov., a new member of the Bacillus cereus group isolated from foreshore tidal flat sediment. J Microbiol 49:1027–1032. https://doi.org/10.1007/s12275-011-1049-6.Jung MY, Paek WK, Park IS, Han JR, Sin Y, Paek J, Rhee MS, Kim H, Song HS, Chang YH. 2010. Bacillus gaemokensis sp. nov., isolated from foreshore tidal flat sediment from the Yellow Sea. J Microbiol 48:867– 871. https://doi.org/10.1007/s12275-010-0148-0.Cheng T, Lin P, Jin S, Wu Y, Fu B, Long R, Liu D, Guo Y, Peng L, Xia Q. 2014. Complete genome sequence of Bacillus bombysepticus, a pathogen leading to Bombyx mori Black Chest Septicemia. Genome Announc 2:e00312-14. https://doi.org/10.1128/genomeA.00312-14.Liu B, Liu GH, Hu GP, Sengonca C, Lin NQ, Tang JY, Tang WQ, Lin YZ. 2014. Bacillus bingmayongensis sp. nov., isolated from the pit soil of Emperor Qin’s terra-cotta warriors in China. Antonie Van Leeuwenhoek 105:995. https://doi.org/10.1007/s10482-014-0150-3.Liu Y, Du J, Lai Q, Zeng R, Ye D, Xu J, Shao Z. 2017. Proposal of nine novel species of the Bacillus cereus group. Int J Syst Evol Microbiol 67:2499 –2508. https://doi.org/10.1099/ijsem.0.001821.Castiaux V, Laloux L, Schneider YJ, Mahillon J. 2016. Screening of cytotoxic B. cereus on differentiated Caco-2 cells and in co-culture with mucus-secreting (HT29-MTX) cells. Toxins 8:320. https://doi.org/10.3390/toxins8110320.Jessberger N, Krey VM, Rademacher C, Böhm ME, Mohr AK, Ehling-Schulz M, Scherer S, Märtlbauer E. 2015. From genome to toxicity: a combinatory approach highlights the complexity of enterotoxin production in Bacillus cereus. Front Microbiol 6:560. https://doi.org/10.3389/fmicb.2015.00560.Wijnands LM, Dufrenne JB, Rombouts FM, In ’t Veld PH, van Leusden FM. 2006. Prevalence of potentially pathogenic Bacillus cereus in food commodities in the Netherlands. J Food Prot 69:2587–2594. https://doi.org/10.4315/0362-028X-69.11.2587.Miller RA, Jian J, Beno SM, Wiedmann M, Kovac J. 2018. Intraclade variability in toxin production and cytotoxicity of Bacillus cereus group type strains and dairy-associated isolates. Appl Environ Microbiol 84:e02479-17. https://doi.org/10.1128/AEM.02479-17.Drewnowska JM, Swiecicka I. 2013. Eco-genetic structure of Bacillus cereus sensu lato populations from different environments in northeastern Poland. PLoS One 8:e80175. https://doi.org/10.1371/journal.pone.0080175.Bartoszewicz M, CzyzË™ewska U. 2017. Spores and vegetative cells of phenotypically and genetically diverse Bacillus cereus sensu lato are common bacteria in fresh water of northeastern Poland. Can J Microbiol 63:939 –950. https://doi.org/10.1139/cjm-2017-0337.Da Riol C, Dietrich R, Märtlbauer E, Jessberger N. 2018. Consumed foodstuffs have a crucial impact on the toxic activity of enteropathogenic Bacillus cereus. Front Microbiol 9:1946. https://doi.org/10.3389/fmicb.2018.01946.Tewari A, Abdullah S. 2015. Bacillus cereus food poisoning: international and Indian perspective. J Food Sci Technol 52:2500 –2511. https://doi.org/10.1007/s13197-014-1344-4.Kroten´ MA, Bartoszewicz M, S´wieË›cicka I. 2010. Cereulide and valinomycin, two import ant natural dodecadepsipeptides with ionophoretic activities. Pol J Microbiol 59:3–10. https://doi.org/10.33073/pjm-2010-001.European Food Safety Authority, European Centre for Disease Prevention and Control. 2018. The European Union summary report on trends and sources of zoonoses, zoonotic agents and foodborne outbreaks 2017. EFSA J 16:e05500.Lund T, De Buyser ML, Granum PE. 2000. A new cytotoxin from Bacillus cereus that may cause necrotic enteritis. Mol Microbiol 38:254 –261. https://doi.org/10.1046/j.1365-2958.2000.02147.xFagerlund A, Ween O, Lund T, Hardy SP, Granum PE. 2004. Genetic and functional analysis of the cytK family of genes in Bacillus cereus. Microbiology 150:2689 –2697. https://doi.org/10.1099/mic.0.26975-0Gohar M, Faegri K, Perchat S, Ravnum S, Økstad OA, Gominet M, Kolstø AB, Lereclus D. 2008. The PlcR virulence regulon of Bacillus cereus. PLoS One 3:e2793. https://doi.org/10.1371/journal.pone.0002793Grenha R, Slamti L, Nicaise M, Refes Y, Lereclus D, Nessler S. 2013. Structural basis for the activation mechanism of the PlcR virulence regulator by the quorum-sensing signal peptide PapR. Proc Natl Acad Sci U S A 110:1047–1052. https://doi.org/10.1073/pnas.1213770110.Böhm ME, Huptas C, Krey VM, Scherer S. 2015. Massive horizontal gene transfer, strictly vertical inheritance and ancient duplications differentially shape the evolution of Bacillus cereus enterotoxin operons hbl,cytK and nhe. BMC Evol Biol 15:246. https://doi.org/10.1186/s12862-015-0529-4.Kaminska PS, Yernazarova A, Murawska E, Swiecicki J, Fiedoruk K, Bideshi DK, Swiecicka I. 2014. Comparative analysis of quantitative reverse transcription real-time PCR and commercial enzyme immunoassays for detection of enterotoxigenic Bacillus thuringiensis isolates. FEMS Microbiol Lett 357:34 –39. https://doi.org/10.1111/1574-6968.12503.Swiecicka I, Bartoszewicz M, Kasulyte-Creasey D, Drewnowska JM, Murawska E, Yernazarova A, Lukaszuk E, Mahillon J. 2013. Diversity of thermal ecotypes and potential pathotypes of Bacillus thuringiensis soil isolates. FEMS Microbiol Ecol 85:262–272. https://doi.org/10.1111/1574-6941.12116.Cohan FM. 2017. Transmission in the origins of bacterial diversity, from ecotypes to phyla. Microbiol Spectr 5:MTBP-0014-2016. https://doi.org/10.1128/microbiolspec.MTBP-0014-2016Guinebretière MH, Thompson FL, Sorokin A, Normand P, Dawyndt P, Ehling-Schulz M, Svensson B, Sanchis V, Nguyen-The C, Heyndrickx M,De Vos P. 2008. Ecological diversification in the Bacillus cereus group.Environ Microbiol 10:851– 865. https://doi.org/10.1111/j.1462-2920.2007.01495.xFiedoruk K, Drewnowska JM, Daniluk T, Leszczynska K, Iwaniuk P, Swiecicka I. 2017. Ribosomal background of the Bacillus cereus group thermotypes. SciRep 7:46430. https://doi.org/10.1038/srep46430.Guinebretière MH, Velge P, Couvert O, Carlin F, Debuyser ML, Nguyen-The C. 2010. Ability to Bacillus cereus group strains to cause food poisoning varies according to phylogenetic affiliation (group I to VII) rather than species affiliation. J Clin Microbiol 48:3388 –3391. https://doi.org/10.1128/JCM.00921-10.Peel MC, Finlayson BL, McMahon TA. 2007. Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644. https://doi.org/10.5194/hess-11-1633-2007.Slamti L, Lereclus D. 2005. Specificity and polymorphism of the PlcRPapR quorum-sensing system in the Bacillus cereus group. J Bacteriol 187:1182–1187. https://doi.org/10.1128/JB.187.3.1182-1187.2005.Kaminska PS, Yernazarova A, Drewnowska JM, Zambrowski G, Swiecicka I. 2015. The worldwide distribution of genetically and phylogenetically diverse Bacillus cereus isolates harbouring Bacillus anthracis-like plasmids. Environ Microbiol Rep 7:738 –745. https://doi.org/10.1111/1758-2229.12305.Hendriksen NB, Hansen BM, Johansen JE. 2006. Occurrence and pathogenic potential of Bacillus cereus group bacteria in a sandy loam. Antonie Van Leeuwenhoek 89:239 –249. https://doi.org/10.1007/s10482-005-9025-y.Collier FA, Elliot SL, Ellis RJ. 2005. Spatial variation in Bacillus thuringiensis/cereus populations within the phyllosphere of broad-leaved dock (Rumex obtusifolius) and surrounding habitats. FEMS Microbiol Ecol 54:417–425.https://doi.org/10.1016/j.femsec.2005.05.005.Shah N, DuPont HL, Ramsey DJ. 2009. Global etiology of travelers’diarrhea: systematic review from 1973 to the present. Am J Trop Med Hyg 80:609 – 614. https://doi.org/10.4269/ajtmh.2009.80.609.Cohan FM, Perry EB. 2007. A systematic for discovering the fundamental units of bacterial diversity. Curr Biol 17:R373–R386. https://doi.org/10.1016/j.cub.2007.03.032.Slamti L, Lemy C, Henry C, Guillot A, Huillet E, Lereclus D. 2016. CodY regulates the activity of the virulence quorum-sensor PlcR by controlling the import of the signaling peptide PapR in Bacillus thuringiensis. Front Microbiol 6:1501. https://doi.org/10.3389/fmicb.2015.01501.Fagerlund A, Lindbäck T, Granum PE. 2010. Bacillus cereus cytotoxins Hbl, Nhe and CytK are secreted via the Sec translocation pathway. BMC Microbiol 10:304. https://doi.org/10.1186/1471-2180-10-304.Castiaux V, Liu X, Delbrassinne L, Mahillon J. 2015. Is cytotoxin K from Bacillus cereus a bona fide enterotoxin? Int J Food Microbiol 211:79 – 85. https://doi.org/10.1016/j.ijfoodmicro.2015.06.020.Jessberger N, Rademacher C, Krey VM, Dietrich R, Mohr AK, Böhm ME, Scherer S, Ehling-Schulz M, Märtlbauer E. 2017. Simulating intestinal growth conditions enhances toxin production of entheropathogenic Bacillus cereus. Front Microbiol 8:627. https://doi.org/10.3389/fmicb.2017.00627.Bartoszewicz M, Bideshi D, Kraszewska A, Modzelewska E, Swiecicka I. 2009. Natural isolates of Bacillus thuringiensis display genetic and psychrotrophic properties characteristic of Bacillus weihenstephanensis. J Appl Microbiol 106:1967–1975. https://doi.org/10.1111/j.1365-2672.2009.04166.x.Guinebretière MH, Fagerlund A, Granum PE, Nguyen-The C. 2006. Rapid discrimination of cytK-1 and cytK-2 genes in Bacillus cereus strains by a novel duplex PCR system. FEMS Microbiol Lett 259:74 – 80. https://doi.org/10.1111/j.1574-6968.2006.00247.x.Prüß BM, Dietrich R, Nibler B, MäRtlbauer E, Scherer S, 1999. The hemolytic enterotoxin HBL is broadly distributed among species of the Bacillus cereus group. Appl Environ Microbiol 65:5436 –5442. https://doi.org/10.1128/AEM.65.12.5436-5442.1999.Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870 –1874. https://doi.org/10.1093/molbev/msw054.Francisco AP, Vaz C, Monteiro PT, Melo-Cristino J, Ramirez M, Carriço JA. 2012. PHYLOViZ: phylogenetic inference and data visualization for sequence based typing methods. BMC Bioinformatics 13:87. https://doi.org/10.1186/1471-2105-13-87.Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG. 2004. eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol 186:1518 –1530. https://doi.org/10.1128/JB.186.5.1518-1530.2004.Drewnowska JM, Fiodor A, Barboza-Corona JE, Swiecicka I. 4 March 2020. Chitinolytic activity of phylogenetically diverse Bacillus cereus sensu lato from natural environments. Syst Appl Microbiol https://doi.org/10.1016/j.syapm.2020.126075.Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389 –3402. https://doi.org/10.1093/nar/25.17.3389.Reiter L, Kolstø A-B, Piehler AP. 2011. Reference genes for quantitative, reverse-transcription PCR in Bacillus cereus group strains throughout the bacterial life cycle. J Microbiol Methods 86:210 –217. https://doi.org/10.1016/j.mimet.2011.05.006.Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45. https://doi.org/10.1093/nar/29.9.e45.Plumb JA, Milroy R, Kaye SB. 1989. Effects of the pH dependence of 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyl-tetrazolium bromide-formazan absorption on chemosensitivity determined by a novel tetrazoliumbased assay. Cancer Res 49:4435– 4440.Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA, Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam AR, Xia F, Stevens R. 2014. The SEED and the Rapid Annotation of microbial genomes using Subsystem Technology (RAST). Nucleic Acids Res 42:D206 –D214. https://doi.org/10.1093/nar/gkt1226.861111

    New Steroidal Selenides as Proapoptotic Factors

    No full text
    Cytostatic and pro-apoptotic effects of selenium steroid derivatives against HeLa cells were determined. The highest cytostatic activity was shown by derivative 4 (GI50 25.0 µM, almost complete growth inhibition after three days of culture, and over 97% of apoptotic and dead cells at 200 µM). The results of our study (cell number measurements, apoptosis profile, relative expression of apoptosis-related APAF1, BID, and mevalonate pathway-involved HMGCR, SQLE, CYP51A1, and PDHB genes, and computational chemistry data) support the hypothesis that tested selenosteroids induce the extrinsic pathway of apoptosis by affecting the cell membrane as cholesterol antimetabolites. An additional mechanism of action is possible through a direct action of derivative 4 to inhibit PDHB expression in a way similar to steroid hormones

    Structural and Thermomagnetic Properties of Gallium Nanoferrites and Their Influence on Cells In Vitro

    No full text
    Magnetite and gallium substituted cuboferrites with a composition of GaxFe3−xO4 (0 ≤ x ≤ 1.4) were fabricated by thermal decomposition from acetylacetonate salts. The effect of Ga3+ cation substitution on the structural and thermomagnetic behavior of 4–12 nm sized core-shell particles was explored by X-ray and neutron diffraction, small angle neutron scattering, transmission electron microscopy, Mössbauer spectroscopy, and calorimetric measurements. Superparamagnetic (SPM) behavior and thermal capacity against increasing gallium concentration in nanoferrites were revealed. The highest heat capacity typical for [email protected] and Ga0.6Fe2.4O4@Fe3O4 is accompanied by a slight stimulation of fibroblast culture growth and inhibition of HeLa cell growth. The observed effect is concentration dependent in the range of 0.01–0.1 mg/mL and particles of Ga0.6Fe2.4O4@Fe3O4 design have a greater effect on cells. Observed magnetic heat properties, as well as interactions with tumor and healthy cells, provide a basis for further biomedical research to use the proposed nanoparticle systems in cancer thermotherapy (magnetic hyperthermia)
    corecore