The promises and risks of probiotic Bacillus species
Abstract
Supplementing the human microbiome with probiotic microorganisms is a proposed solution for civilization syndromes such as dysbiosis and gastrointestinal tract (GIT) disorders. Bimodal probiotic strains of the Bacillus genus constitute the microbiota of the human environment, and are typically found in soil, water, a number of non-dairy fermented foods, as well as in human and animal GIT. Probiotic Bacillus sp. are Gram positive rods, with the ability of sporulation to survive environmental stress and preparation conditions. In vitro models of the human stomach and human studies with probiotic Bacillus reveal the mechanisms of its life cycle and sporulation. The Bacillus sp. probiotic biofilm introduces biochemical effects such as antimicrobial and enzymatic activity, thus contributing to protection from GIT and other infections. Despite the beneficial activity of Bacillus strains belonging to the safety group 1, a number of strains can pose a substantial health risk, carrying genes for various toxins or antibiotic resistance. Commercially available Bacillus probiotic preparations include strains from the subtilis and other closely related phylogenetic clades. Those intended for oral administration in humans, often encapsulated with appropriate supporting materials, still tend to be mislabeled or poorly characterized. Bacillus sp. MALDI-TOF analysis, combined with sequencing of characteristic 16S rRNA or enzyme coding genes, may provide accurate identification. A promising future application of the probiotic Bacillus sp. might be the microflora biocontrol in the human body and the closest human environment. Environmental probiotic Bacillus species display the potential to support human microflora, however controversies regarding the safety of certain strains is a key factor in their still limited application.
References
REFERENCES
Abreo A, Gebretsadik T, Stone CA, Hartert TV (2018) The impact of modifiable risk factor reduction on childhood asthma development. Clin Transl Med 7(1): 15. http://doi: 10.1186/s40169-018-0195-4.
Araya M, Gopal P, Lindgren SE, Lodi R, Oliver G, Saxelin ML, Servin AL, Stanton C, Gilliland SE, Morelli L, Reid G, Pineiro M, Schlundt J (2001) Joint FAO/WHO Expert Consultation on Evaluation of Health and Nutritional Properties of Probiotics in Food including Powder Milk with Live Lactic Acid Bacteria. In Probiotics in food. Health and Nutritional properties and guidelines for evaluation, FAO Food and Nutrition paper 85. http://www.fao.org/3/a-a0512e.pdf
Ashe S, Maji UJ, Sen R, Mohanty S, Maiti NK (2014) Specific oligonucleotide primers for detection of endoglucanase positive Bacillus subtilis by PCR. 3 Biotech 4(5): 461-465. http://doi:10.1007/s13205-013-0177-6.
Azarko J., Wendt U. (2011) Identification of microorganisms – comparision of biochemical and mass spectrometry method. Diagn Lab, 47 (4), 409-417.
Banaszczyk J, Jędrzejczak G, Zarzeczańska D, Ramotowska S, Fiutak M, Skowron M, Ossowski T, Skowron P, Jeżewska-Frąckowiak J (2017) Probiotic Bacillus sp. environmental strains as a component of improved dishwasher cleaning product. W Sci News 72: 141-149
Ben-Dov E (2014) Bacillus thuringiensis subsp. israelensis and its dipteran-specific toxins. Toxins. 6(4): 1222-1243. http://doi:10.3390/toxins6041222.
Berkeley RM, Heyndrickx NL, De Vos P (2008) Applications and systematics of Bacillus and relatives. Wiley-Blackwell. Oxford
Billings N, Birjiniuk A, Samad TS, Doyle PS, Ribbeck K (2015) Material properties of biofilms – key methods for understanding permeability and mechanics. Rep Prog Phys 78(3): 036601. http://doi: 10.1088/0034-4885/78/3/036601
Björkstén B, Naaber P, Sepp E, Mikelsaar M (1999) The intestinal microflora in allergic Estonian and Swedish 2-year-old children. Clin Exp Allergy 29(3): 342-346. erratum in Clin Exp Allergy 30(7): 1047. https://doi.org/10.1046/j.1365-2222.1999.00560.x
Björkstén B. (1994) Risk factors in early childhood for the development of atopic diseases. Allergy 49(6): 400-407. https://doi.org/10.1111/j.1398-9995.1994.tb00831.x
Bloomfield SF, Stanwell-Smith R, Crevel RWR, Pickup J (2006) Too clean, or not too clean: the Hygiene Hypothesis and home hygiene. Clin Exp Allergy 36(4): 402–425. http://doi: 10.1111/j.1365-2222.2006.02463.x
Both E, Gyenge L, Bodor Z, Gyorgy E, Lanyi S, Abraham B (2012) Intensification of probiotic microorganisms viability by microencapsulation using ultrasonic atomizer. UPB Buletin Scientific Series B: Chem Mater Sc. ;74(1):27–32
Castellazzi AM, Valsecchi C, Caimmi S, Licari A, Marseglia A, Leoni MC, Caimmi D, del Giudice MM, Leonardi S, La Rosa M, Marseglia GL (2013) Probiotics and food allergy. Ital J Pediatr 39: 47. http://doi: 10.1186/1824-7288-39-47
Chávarri M, Marañón I, Villarán MC (2012) Encapsulation Technology to Protect Probiotic Bacteria. In Probiotics. Ch23 pp 501-540. InTech, Rijeka, Rigobelo. http://dx.doi.org/10.5772/50046
Ciałowicz KM (2017) New discoveries at Tell el-Farkha and the beginnings of the Egyptian state. Étud Trav XXX: 231–250. http://dx.doi.org/10.12775/EtudTrav.30.011
Cutting SM (2011) Bacillus probiotics. Food Microbiol 28: 214-220. http://doi: 10.1016/j.fm.2010.03.007
Dimkic´ I, Stankovic´ S, Nišavic´ M, Petkovic´ M, Ristivojevic´ P, Fira D, Beric´ T (2017) The profile and antimicrobial activity of Bacillus lipopeptide extracts of five potential biocontrol strains. Front Microbiol 8: 925. https://doi.org/10.3389/fmicb.2017.00925
Djenane Z, Nateche F, Amziane M, Gomis-Cebolla J, El-Aichar F, Khorf H, Ferré J (2017) Assessment of the antimicrobial activity and the entomocidal potential of Bacillus thuringiensis isolates from Algeria. Ed. Vernon L. Tesh. Toxins 9(4): 139. http://doi:10.3390/toxins9040139
Earl AM, Eppinger M, Fricke WF, Rosovitz MJ, Rasko DA, Daugherty S, Losick R, Kolter R, Ravel J (2012) Whole-genome sequences of Bacillus subtilis and close relatives. J Bacteriol 194: 2378-2379. http://dx.doi.org/10.1128/JB.05675-11
Elshaghabee FMF, Rokana N, Gulhane RD, Sharma C, Panwar H (2017) Bacillus as potential probiotics: status, concerns, and future perspectives. Front Microbiol 8: 1490. http://doi:10.3389/fmicb.2017.01490
Emese B, László G, Zsolt B, György É, Szabolcs Lanyi, Ábrahám B (2012) Intensification of probiotic microorganisms viability by microencapsulation using ultrasonic atomizer. UPB Scientific Bulletin, Series B: Chemistry and Materials Science. 74
Franklin MJ, Chang C, Akiyama T, Bothner B (2015) New technologies for studying biofilms. Microbiol. Spectr 3(4). http://doi:10.1128/microbiolspec.MB-0016-2014
Gehrman SH, Porubcan RS (1985) Stabilized liquid bacterial suspension for oral administration to animals. US Patent 4,518,696
Giaouris E, Heir E, Desvaux M, Hébraud M, Møretrø T, Langsrud S, Doulgeraki A, Nychas G-J, Kacániová M, Czaczyk K, Ölmez H, Simões M (2015) Intra- and inter-species interactions within biofilms of important foodborne bacterial pathogens. Front Microbiol 6: 841. http://doi: 10.3389/fmicb. 2015.00841
Goderska K (2012) Different methods of probiotics stabilization. In Probiotics. Ch24 pp 541-550. InTech, Rijeka, Rigobelo. http://dx.doi.org/10.5772/50313
Havenaar R, Huis In’t Veld JHJ (1992) Probiotics: a general view. In The Lactic Acid Bacteria in Health and Disease. Elsevier Science Publishers, pp 151-170. London and New York
Hoa NT, Baccigalupi L, Huxham A, Smertenko A, Van PH, Ammendola S, Ricca E, Cutting SM (2000) Characterization of Bacillus species used for oral bacteriotherapy and bacterioprophylaxis of gastrointestinal disorders. Appl Environ Microbiol 66(12): 5241–5247. PMCID: PMC92451
Hong HA, Duc Le H, Cutting SM (2005) The use of bacterial spore formers as probiotics, FEMS Microbiology Reviews 29(4): 813–835, https://doi.org/10.1016/j.femsre.2004.12.001
Hong HA, Khaneja R, Tam NMK, Cazzato A, Tan S, Urdaci M, Brisson A, Gasbarrini A, Barnes A, Cutting SM (2009) Bacillus subtilis isolated from the human gastrointestinal tract. Res Microbiol 160: 134-143. http://doi: 10.1016/j.resmic.2008.11.002
Hu Y, Liu Y, Yang W, Liu Y, Zhang Y, Yin J (2016) Preparation method for Bacillus coagulans bacterial suspension. Nanjing Tech University, WO/2016/150152
Jeżewska-Frąckowiak J, Seroczynska K, Banaszczyk J, Wozniak D, Skowron M, Ozog A, Żylicz-Stachula A, Ossowski T, Skowron P (2017) Detection of endospore producing Bacillus species from commercial probiotics and their preliminary microbiological characterization. J Environ Biol 38: 1435-1440. http://doi: 10.22438/jeb/38/6/MRN-478
Joshi VK, Singh RS (2012) Food Biotechnology. Principles and practices. IK International Publishing House Pvt. Ltd, New Delhi
Kadaikunnan S, Rejiniemon TS, Khaled JM, Alharbi NS, Mothana R (2015) In-vitro antibacterial, antifungal, antioxidant and functional properties of Bacillus amyloliquefaciens Ann Clin Microbiol Antimicrob 14: 9. https://doi.org/10.1186/s12941-015-0069-1
Kearns DB, Losick R. (2005) Cell population heterogeneity during growth of Bacillus subtilis. Genes Dev 19(24): 3083-3094. http://doi:10.1101/gad.1373905
Kirejevas V, Kazarjan A (2012) Probiotic oil suspension and use thereof. BACTERFIELD Gmbh, WO/2010/122107A1; EP2421384A1
Kosikowska U, Stępień-Pyśniak D, Pietras-Ożga D, Andrzejczuk S, Juda M, Malm A (2015) Application of MALDI-TOF MS for identification of clinical isolates of bacteria from humans and animals. Diagn Lab 51(1): 23-30
La Ragione RM, Casula G, Cutting SM, Woodward MJ (2001) Bacillus subtilis spores competitively exclude Escherichia coli O78:K80 in poultry. Vet Microbiol 79: 133-142. https://doi.org/10.1016/S0378-1135(00)00350-3
La Ragione RM, Woodward MJ (2001) Competitive exclusion by Bacillus subtilis spores of Salmonella enterica serotype Enteritidis and Clostridium perfringens in young chickens. Vet Microbiol 94: 245-256. https://doi.org/10.1016/S0378-1135(03)00077-4
Lane N (2015) The unseen world: reflections on Leeuwenhoek (1677) “Concerning little animals.” Phil. Trans. R. Soc. B 370: 20140344. http://dx.doi.org/10.1098/rstb.2014.0344
LaSarre B, Federle MJ (2013) Exploiting quorum sensing to confuse bacterial pathogens. MMBR 77(1): 73-111. http://doi:10.1128/MMBR.00046-12
Leuschner R (2006) CRL, Evaluation report on the analytical methods submitted in connection with Section II, 2.5, (Control Methods) of the Application for authorisation as a feed additive according to Regulation (EC) No 1831/2003 , BioPlus 2B (for turkeys for fattening), Active agents: Bacillus subtilis DSM 5750, Bacillus licheniformis, DSM 5749, European Comission Joint Research Centre, Institute for Reference Materials and Measurements, Community Reference Laboratory, Feed Additives Authorisation D08-FSQ(2006)D/15068
Leuschner R (2008) CRL Evaluation report on the analytical methods submitted in connection with Section II, 2.5 (Control Methods) of the Application for authorisation as a Feed Additive according to Regulation (EC) No 1831/2003, BioPlus 2B® for rabbits, Active Agent(s): Bacillus subtilis DSM 5750 and Bacillus licheniformis DSM 5749, European Comission Joint Research Centre, Institute for Reference Materials and Measurements, Community Reference Laboratory, Feed Additives Authorisation D08/FSQ/CVH/RL/D(2008)16171
Lewis ZT, Shani G, Masarweh CF, Popovic M, Frese SA, Sela DA, Underwood MA, Mills DA (2016) Validating bifidobacterial species and subspecies identity in commercial probiotic products. Pediatr Res 79(3): 445-452. http://doi:10.1038/pr.2015.244
Lyons NA, Kolter R (2017) Bacillus subtilis protects public goods by extending kin discrimination to closely related species. MBio 8(4). pii: e00723-17. doi: 10.1128/mBio.00723-17
Mah TF, O’Toole GA (2001) Mechanism of biofilm resistance to antimicrobial agents. Trends Microbiol 9 (1): 34-39. https://doi.org/10.1016/S0966-842X(00)01913-2
Mahidsanan T, Gasaluck P, Eumkeb G (2017) A novel soybean flour as a cryoprotectant in freeze-dried Bacillus subtilis SB-MYP-1. LWT Food Science and Technology 77: 152-159. https://doi.org/10.1016/j.lwt.2016.11.015
Mantzouridou F, Spanou A, Kiosseoglou V (2012) An inulin-based dressing emulsion as a potential probiotic food carrier. Food Res Int 46(1): 260–269. https://doi.org/10.1016/j.foodres.2011.12.016
Martín MJ, Lara-Villoslada F, Ruiz MA, Morales ME (2015) Microencapsulation of bacteria: A review of different technologies and their impact on the probiotic effects. Innov Food Sci Emerg Technol 27: 15-25, https://doi.org/10.1016/j.ifset.2014.09.010
Meroni PL, Palmieri R, Barcellini W, De Bartolo G, Zanussi C (1983) Effect of long term-treatment with B. subtilis on the frequency of urinary tract infections in older patients. Chemiotherapia, 2(2): 142-144
Metchnikoff E (1907) Prolongation of life. Optimistic studies. Paris, Eng transl. Mitchell PC, 1908, GP Putnam’s Sons, New York and London, The Knickerbocker Press
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(6): e02479-17. http://doi:10.1128/AEM.02479-17
Myszka K., Czaczyk K. (2007) Mechanisms determining bacterial biofilm resistance to antimicrobial factors. Biotechnology, 1: 40-52.
Noorashikin MN, Li LY, Karim M, Daud HM, Natrah FMI (2016) Screening and identification of quorum sensing degraders from live feed Artemia. J Environ Biol 37(4): 811-6. PMID: 28779741
Olmos J, Paniagua-Michel J (2014) Bacillus subtilis A potential probiotic bacterium to formulate functional feeds for aquaculture. J Microb Biochem Technol 6: 361-365. http://doi: 10.4172/1948-5948.1000169
Papadimitriou K, Zoumpopoulou G, Foligné B, Alexandraki V, Kazou M, Pot B, Tsakalidou E (2015) Discovering probiotic microorganisms: in vitro, in vivo, genetic and omics approaches. Front Microbiol 6: 58. http://doi: 10.3389/fmicb.2015.00058
Pérez-Gutiérrez R-A, López-Ramírez V, Islas Á, Alcaraz LD, Hernández-González I, Olivera BC, Santillán M, Eguiarte LE, Souza V, Travisano M, Olmedo-Alvarez G (2013) Antagonism influences assembly of a Bacillus guild in a local community and is depicted as a food-chain network. ISME J 7(3): 487-497. doi:10.1038/ismej.2012.119
Plaza-Diaz J, Gomez-Llorente C, Fontana L, Gil A (2014) Modulation of immunity and inflammatory gene expression in the gut, in inflammatory diseases of the gut and in the liver by probiotics. World J Gastroenterol 20: 15632-15649. http://doi: 10.3748/wjg.v20.i42.15632
Porubcan RS, Sellars RL (1978) Preparation of culture concentrates for direct vat set cheese production. US Patent 4,115,199
Quigley EMM (2010) Prebiotics and probiotics; modifying and mining the microbiota. Pharmacol Res 61(3): 213-8. http://doi: 10.1016/j.phrs.2010.01.004
Ravel J, Blaser MJ, Braun J, Brown E, Bushman FD, Chang EB, Davies J, Dewey KG, Dinan T, Dominguez-Bello M, Erdman SE, Finlay BB, Garrett WS, Huffnagle GB, Huttenhower C, Jansson J, Jeffery IB, Jobin C, Khoruts A, Kong HH, Lampe JW, Ley RE, Littman DR, Mazmanian SK, Mills DA, Neish AS, Petrof E, Relman DA, Rhodes R, Turnbaugh PJ, Young WB, Knight R, White O (2014) Human microbiome science: vision for the future. Microbiome 2:16. http://doi.org/10.1186/2049-2618-2-16
Reid G, Hammond JA (2005) Probiotics: Some evidence of their effectiveness. Can Fam Physician 51(11): 1487–1493. PMCID: PMC1479479
Riedel S. (2005) Anthrax: a continuing concern in the era of bioterrorism. Proc (Bayl Univ Med Cent) 18(3): 234–243. PMID: 16200179
Roberts MS, Nakamura LK, Cohan FM (1994) Bacillus mojavensis sp. nov., distinguishable from Bacillus subtilis by sexual isolation, divergence in DNA sequence, and differences in fatty acid composition. Int J Syst Bacteriol 44(2): 256-264
Roberts MS, Nakamura LK, Cohan FM (1996) Bacillus vallismortis sp. nov., a Close Relative of Bacillus subtilis, Isolated from Soil in Death Valley, California. Int J Syst Bacteriol 46(2): 470-475
Safitri R, Priadie B, Miranti M, Astuti AW (2015) Ability of bacterial consortium: Bacillus coagulans, Bacilus licheniformis, Bacillus pumilus, Bacillus subtilis, Nitrosomonas sp. and Pseudomonas putida in bioremediation of waste water in Cisirung waste water treatment plant. AgroLife Sci J 4(1): 146-152
Sanders ME, Akkermans LM, Haller D, Hammerman C, Heimbach J, Hörmannsperger G, Huys G, Levy DD, Lutgendorff F, Mack D, Phothirath P, Solano-Aguilar G, Vaughan E (2010) Safety assessment of probiotics for human use. Gut Microbes 1(3): 164-85. http://doi: 10.4161/gmic.1.3.12127
Schmalstieg FC, Goldman AS (2008) Ilya Ilich Metchnikoff (1845-1915) and Paul Ehrlich (1854-1915): the centennial of the 1908 Nobel Prize in Physiology or Medicine. J Med Biogr 16: 96-103. http://doi: 10.1258/jmb.2008.008006
Schnorr SL, Sankaranarayanan K, Lewis CM, Warinner C (2016) Insights into human evolution from ancient and contemporary microbiome studies. Curr Opin Genet Dev 41:14-26. https://doi.org/10.1016/j.gde.2016.07.003
Seroczyńska K, Bystrzycki R, Banaszczyk J, Woźniak D, Jędrzejczak G, Partryka T, Skowron P, Jeżewska-Frąckowiak J (2016) Self-soluble capsule for the preparation of washing solutions. GRUPA INCO S.A., Patent app. EP16207662.4
Sornplang P, Piyadeatsoontorn S (2016) Probiotic isolates from unconventional sources: a review. J Anim Sci Technol 58: 26. http://doi:10.1186/s40781-016-0108-2
Standards Unit, PHE, Microbiology Services, Public Health England, UK (2015) Standards for microbiology investigations. Identification of Bacillus species. In Bacteriology – Identification 9(3): 1 -27
Standards Unit, PHE, Microbiology Services, Public Health England, UK (2018) Standards for microbiology investigations. Identification of Bacillus species. In Bacteriology – Identification 9(3.1): 1 -27
Strachan DP (1989) Hay fever, hygiene and household size. B M J 299: 1259-60. PMC1838109
Thirabunyanon M, Thongwittaya N (2011) Protection activity of a novel probiotic strain of Bacillus subtilis against Salmonella enteritidis infection. Res Vet Sci 93: 74-81. https://doi.org/10.1016/j.rvsc.2011.08.008
Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett C, Knight R, Gordon JI.(2007) The human microbiome project: exploring the microbial part of ourselves in a changing world. Nature 449(7164): 804–810. https://doi:10.1038/nature06244
Urgesi R, Casale C, Pistelli R, Rapaccini GL, de Vitis I (2013) A randomized double-blind placebo-controlled clinical trial on efficacy and safety of association of simethicone and Bacillus coagulans (Colinox®) in patients with irritable bowel syndrome. Eur Rev Med Pharmacol Sci 18: 1344-1353
Vandini A, Temmerman R, Frabetti A, Caselli E, Antonioli P, Balboni PG, Platano D, Branchini D, Mazzacane S (2014) Hard surface biocontrol in hospitals using microbial-based cleaning products. PLoS ONE 9(9): e108598. http://doi:10.1371/journal.pone.0108598
Verschuere L, Rombaut G, Sorgeloos P, Verstraete W (2000) Probiotic bacteria as biological control agents in aquaculture. Microbiol Mol Biol Rev 64(4): 655-671. PMCID: PMC99008
Waligora-Dupriet AJ, Butel MJ (2012). Microbiota and allergy: Dysbiosis to probiotics. In Allergic Diseases - Highlights in the Clinic, Mechanisms and Treatment. http://doi: 10.5772/26234
Wattiau P, Renard M-E, Ledent P, Debois V, Blackman G, Agathos S (2001) A PCR test to identify Bacillus subtilis and closely related species and its application to the monitoring of wastewater biotreatment. Appl Microbiol Biotechnol 56: 816. https://doi.org/10.1007/s002530100691
West CE, Dzidic M, Prescott SL, Jenmalm MC (2017) Bugging allergy; role of pre-, pro- and synbiotics in allergy prevention. Allergol Int 66(4): 529-538. http://doi: 10.1016/j.alit.2017.08.001. Epub 2017 Sep 1
Yasin IM, Razak NF, Natrah FMI, Harmin SA (2016) Selection and evaluation of Malaysian Bacillus spp. strains as potential probiotics in cultured tiger grouper (Epinephelus fuscoguttatus). J Environ Biol 37: 791-800. PMID: 28779739
Żakowska D, Bartoszcze M, Niemcewicz M, Bielawska-Drózd A, Kocik J (2012) New aspects of the infection mechanisms of B. anthracis. Ann Agric Environ Med 19(4): 613-618
Zupančič J, Novak Babič M, Zalar P, Gunde-Cimerman N (2016) The Black Yeast Exophiala dermatitidis and Other Selected Opportunistic Human Fungal Pathogens Spread from Dishwashers to Kitchens. PLoS ONE 11(2): e0148166. http://doi:10.1371/journal.pone.0148166
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