Background and objective: Growth of beneficial probiotics is attributed to their tolerance to stress factors while most probiotics have a relatively short and unstable shelf life. Bacillus coagulans, an economically important spore-forming species, is becoming increasingly remarkable in field of probiotics for the decrease of harmful effects of processing and environment conditions on the survival of bacterial cells and to assure their functionality in the human body. The aim of this review was to explore scientific research on therapeutic, functional and biosafety properties of Bacillus coagulans as a novel probiotic.
Results and conclusion: Many scientific literatures have been published on the use of health promoting Bacillus spores in foods. Bacillus coagulans mostly includes several health benefits of non-spore forming probiotics and is able to tolerate heat and stressful requirements of food processing as well as gastrointestinal tract conditions. Considering specific characteristics of spore-forming probiotics, Bacillus coagulans demonstrates a promising potential in production of probiotic foods.
Conflict of interest: The authors declare no conflict of interest.
Kanmani P, Satish Kumar R, Yuvaraj N, Paari KA, Pattukumar V, Arul V. Probiotics and Its Functionally Valuable Products—A Review. Crit Rev Food Sci Nutr. 2013; 53: 641-658. doi.org/10.1080/10408398.2011.5537522.
Jose NM, Bunt CR, Hussain MA. Comparison of microbiological and probiotic characteristics of lactobacilli isolates from dairy food products and animal rumen contents. Microorganisms. 2015; 3(2): 198-212. doi:10.3390/microorganisms3020198.
Forssten SD, Sindelar CW, Ouwehand AC. Probiotics from an industrial perspective. Anaerobe. 2011; 17(6): 410-413. doi: 10.1016/j.anaerobe.2011.04.014. Epub 2011 Apr 29.
Cutting SM. Bacillus probiotics. Food microbiol. 2011; 28: 214-220. doi.org/10.1016/j.fm.2010.03.007
Graff S, Chaumeil JC, Boy P, Lai-Kuen R, Charrueau C. Formulations for protecting the probiotic Saccharomyces boulardii from degradation in acidic condition. Biol Pharm Bull. 2008; 31(2): 266-272.
Sanders ME, Morelli L, Tompkins TA. Sporeformers as human probiotics: Bacillus, Sporolactobacillus, and Brevibacillus. Compr Rev Food Sci Food Saf. 2003; 2: 101-110. doi.org/10.1111/j.1541-4337.2003.tb00017.x
Elshaghabee FMF, Rokana N, Gulhane RD, Sharma C, Panwar H. Bacillus As Potential Probiotics: Status, Concerns, and Future Perspectives. Front Microbiol. 2017; 8: 1490. doi.org/10.3389/fmicb.2017.01490
Talebi S, Makhdoumi A, Bahreini M, Matin MM, Moradi HS. Three novel Bacillus strains from a traditional lacto‐fermented pickle as potential probiotics. J Appl Microbiol. 2018; 888-896. doi: 10.1111/jam.13901. Epub 2018 Jun 26.
Ghelardi E, Celandroni F, Salvetti S, Gueye SA, Lupetti A, Senesi S. Survival and persistence of Bacillus clausii in the human gastrointestinal tract following oral administration as spore‐based probiotic formulation. J Appl Microbiol. 2015; 119: 552-559. doi.org/10.1111/jam.12848
Nyangale EP, Farmer S, Keller D, Chernoff D, Gibson GR. Effect of prebiotics on the fecal microbiota of elderly volunteers after dietary supplementation of Bacillus coagulans GBI-30, 6086. Anaerobe. 2014; 30: 75-81. doi.org/10.1016/j.anaerobe.2014.09.002
Mazza P. The use of Bacillus subtilis as an antidiarrhoeal microorganism. Boll. Chim. Farm. 1994; 133: 3-18. PMID:8166962
Hong HA, Huang JM, Khaneja R, Hiep LV, Urdaci MC, Cutting, SM. The safety of Bacillus subtilis and Bacillus indicus as food probiotics. J Appl Microbiol. 2008; 105: 510-520. doi.org/10.1111/j.1365-2672.2008.03773.x
Hong H, Le Hong Duc A, Cutting SM. The use of bacterial spore formers as probiotics. FEMS Microbiol Rev. 2005; 29: 813-835. doi.org/10.1016/j.femsre.2004.12.001
La MR, Bottaro G, Gulino N, Gambuzza F, Di Forti F, Inì G, Tornambè E. Prevention of antibiotic-associated diarrhea with Lactobacillus sporogens and fructo-oligosaccharides in children. A multicentric double-blind vs placebo study. Minerva pediatrica. 2003; 55(5): 447-452.
Shahcheraghi SH, Ayatollahi J, Lotfi M. Applications of Bacillus subtilis as an important bacterium in medical sciences and human life. Tropical Journal of Medical Research. 2015; 18: 1-4. doi.org/10.4103/1119-0388.152530
Hosseini Nezhad M, Hussain MA, Britz ML. Stress responses in probiotic Lactobacillus casei. Crit Rev Food Sci Nutr. 2015; 55(6): 740-749. doi:10.1080/10408398.2012.675601.
Hussain MA, Hosseini Nezhad M, Sheng Y, Amoafo O. Proteomics and the stressful life of lactobacilli. FEMS Microbiol Lett. 2013; 349(1): 1-8. doi: 10.1111/1574-6968.12274.
Nicholson WL, Munakata N, Horneck G, Melosh HJ, Setlow P. 2000 Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol Rev. 2000; 64: 548-572. doi.org/10.1128/MMBR.64.3.548-572.2000
Jurenka JS. Bacillus coagulans: monograph. Altern Med Rev. 2012; 17: 76-81.
Darjani P, Hosseini Nezhad M, Kadkhodaee R, Milani E. Influence of prebiotic and coating materials on morphology and survival of a probiotic strain of Lactobacillus casei exposed to simulated gastrointestinal conditions. LWT-Food Sci Technol. 2016; 73: 162-167. doi.org/10.1016/j.lwt.2016.05.032
Gangwar AS, Bhardwaj A, Sharma V. Fermentation of tender coconut water by probiotic bacteria Bacillus coagulans. IJFS. 2018; 7 (1). doi.org/10.7455/ijfs/7.1.2018.a9
Majeed M, Nagabhushanam K, Arumugam S, Natarajan S, Majeed S, Pande A, Beede K, Ali F. Cranberry seed fibre: a promising prebiotic fibre and its fermentation by the probiotic Bacillus coagulans MTCC 5856. IJFST. 2018. doi.org/10.1111/ijfs.13747
Postollec F, Mathot AG, Bernard M, Divanac'h ML, Pavan S, Sohier D. Tracking spore-forming bacteria in food: from natural biodiversity to selection by processes. Int J Food Microbiol. 2012; 158: 1-8. doi.org/10.1016/j.ijfoodmicro.2012.03.004
Barbosa TM, Serra CR, La Ragione RM, Woodward MJ, Henriques AO. Screening for Bacillus isolates in the broiler gastrointestinal tract. Appl Environ Microbiol. 2005; 71: 968-978. doi.org/10.1128/AEM.71.2.968-978.200519
Spinosa MR, Braccini T, Ricca E, De Felice M, Morelli L, Pozzi G, Oggioni MR. On the fate of ingested Bacillus spores. Res Microbiol. 2000; 151: 361-368. doi.org/10.1016/S0923-2508(00)00159-5
Tuohy KM, Pinart‐Gilberga M, Jones M, Hoyles L, McCartney AL, Gibson GR. Survivability of a probiotic Lactobacillus casei in the gastrointestinal tract of healthy human volunteers and its impact on the faecal microflora. J Appl Microbiol. 2007; 102: 1026-1032. doi.org/10.1111/j.1365-2672.2006.03154.x
Cutting SM, Ricca E. 2014; Bacterial spore-formers: friends and foes. Blackwell Publishing Ltd Oxford, UK. 2014. doi.org/10.1111/1574-6968.12572
Ramirez-Peralta A, Zhang P, Li Y, Setlow P. Effects of sporulation conditions on the germination and germination protein levels of Bacillus subtilis spores. Appl. Environ. Microbiol. 2012; 78: 2689-2697. doi.org/10.1128/AEM.07908-11
Moir A. How do spores germinate? J Appl Microbiol. 2006; 101: 526-530. doi.org/10.1111/j.1365-2672.2006.02885.x
Sanders ME, Morelli L, Bush S. Lactobacillus sporogenes is not a Lactobacillus probiotic. ASM News. 2001; 67: 385-386.
Jafari M, Mortazavian AM, Hosseini H. Effect of household cooking methods on the viability of Bacillus probiotics supplemented in cooked sausage. NFSR. 2017; 4: 47-56. doi.org/10.18869/acadpub.nfsr.4.1.47
Wells-Bennik MHJ, Eijlander RT, Den Besten Erwin HMW, Berendsen M, Warda AK, Krawczyk AO, Nierop Groot MN, Xiao Y, Zwietering MH, Kuipers OP. Bacterial spores in food: survival, emergence, and outgrowth. Annu RevFood Sci Technol. 2016; 7: 457-482. doi.org/10.1146/annurev-food-041715-033144
Jafari M, Alebouyeh M, Mortazavian AM, Ghanati K, Amiri Z, Zali MR. Influence of heat shock temperatures and fast freezing on viability of probiotic sporeformers and the issue of spore plate count versus true numbers. NFSR. 2016; 3: 35-42. doi.org/10.18869/acadpub.nfsr.3.1.35
Majeed M, Majeed S, Nagabhushanam K, Natarajan S, Sivakumar A, Ali F. Evaluation of the stability of Bacillus coagulans MTCC 5856 during processing and storage of functional foods. IJFST. 2016; 51: 894-901. doi.org/10.1111/ijfs.13044
Inooka S, Uehara S, Kimura M. The effect of Bacillus natto on the T and B. lymphocytes from spleens of feeding chickens. Poult Sci. 1986; 65: 1217-1219. doi.org/10.3382/ps.0651217
Tsukamoto Y, Kasai M, Kakuda H. Construction of a Bacillus subtilis (natto) with high productivity of vitamin K2 (menaquinone-7) by analog resistance. Biosci Biotechnol Biochem. 2001; 65: 2007-2015. doi.org/10.1271/bbb.65.2007
Hosoi T, Ametani A, Kiuchi K, Kaminogawa S. Changes in fecal microflora induced by intubation of mice with Bacillus subtilis (natto) spores are dependent upon dietary components. Can J Microbiol. 1999; 45: 59-66.
Hosoi T, Ametani A, Kiuchi K, Kaminogawa S. Improved growth and viability of lactobacilli in the presence of Bacillus subtilis (natto), catalase, or subtilisin. Can J Microbiol. 2000; 46: 892-897. doi.org/10.1139/w00-070
Jäger R, Purpura M, Farmer S, Cash HA, Keller D. Probiotic Bacillus coagulans GBI-30, 6086 Improves Protein Absorption and Utilization. Probiotics Antimicrob Proteins. 2017; 10(4): 611-615. doi.org/10.1007/s12602-017-9354-y
Jäger R, Shields KA, Lowery RP, De Souza EO, Partl JM, Hollmer C, Purpura M, Wilson JM. Probiotic Bacillus coagulans GBI-30, 6086 reduces exercise-induced muscle damage and increases recovery. Peer J. 2016; 4: 2276. doi.org/10.7717/peerj.2276
Lakshmi SG, Jayanthi N, Saravanan M, Sudha Ratna M. Safety assesment of Bacillus clausii UBBC07, a spore forming probiotic. Toxicol rep. 2017; 4: 62-71. doi.org/10.1016/j.toxrep.2016.12.004
Horowitz-Wlassowa LM, Nowotelnow NW. Über eine sporogene Milchsäurebakterienart, Lactobacillus sporogenes n. sp. Cent F Bak, II Abt. 1932; 87: 331.
Bergey DH, Breed RS, Murray EJD. Sergey's Manual of Determinative Bacteriology. A Key for the Identification of Organisms of the Class Schizomycetes. 1939; 48 LWW.
Hyronimus B, Le Marrec C, Urdaci MC. Coagulin, a bacteriocin-like-inhibitory substance produced by Bacillus coagulans I. J Appl Microbiol. 1998; 85: 42-50.
Meroni PL, Palmieri R, Barcellini W. Effect of long-term treatment with Bacillus subtilis on the frequency of urinary tract infections in older patients. Chemioterapia. 1983; 2: 142-144.
Abdhul K, Ganesh M, Shanmughapriya S, Vanithamani S, Kanagavel M, Anbarasu K, Natarajaseenivasan K. Bacteriocinogenic potential of a probiotic strain Bacillus coagulans [BDU3] from Ngari. Int J Biol Macromol. 2015; 79: 800-806. doi.org/10.1016/j.ijbiomac.2015.06.005
Su F, Tao F, Tang H, Xu P. Genome sequence of the thermophile Bacillus coagulans Hammer, the type strain of the species. Journal of bacteriology. 2012; 194(22): 6294-6295. doi.org/10.1128/JB.01380-12
Qin J, Zhao B, Wang X, Wang L, Yu B, Ma Y, Ma C, Tang H, Sun J, Xu P. Non-sterilized fermentative production of polymer-grade L-lactic acid by a newly isolated thermophilic strain Bacillus sp. 2–6. PLoS One. 2009; 4(2): 4359. doi: 10.1371/journal.pone.0004359.
De Vecchi E, Drago L. Lactobacillus sporogenes or Bacillus coagulans: misidentification or mislabelling? Int J Probiotics Prebiotics. 2006; 1: 3-10.
Madempudi RS, Kalle AM. Antiproliferative Effects of Bacillus coagulans Unique IS2 in Colon Cancer Cells. Nutr Cancer. 2017; 69: 1062-1068. doi.org/10.1080/01635581.2017.1359317
Konuray G, Erginkaya Z. Potential Use of Bacillus coagulans in the Food Industry. Foods. 2018; 7(6): 92. doi: 10.3390/foods7060092.
Sudha RM, Sunita M, Sekhar BM. Safety studies of Bacillus coagulans Unique IS-2 in rats: morphological, biochemical and clinical evaluations. Int J Probiotics Prebiotics. 2016; 11 (1) 43.
Keller D, Van Dinter R, Cash H, Farmer S, Venema K. Bacillus coagulans GBI-30, 6086 increases plant protein digestion in a dynamic, computer-controlled in vitro model of the small intestine (TIM-1). Benef Microbes. 2017; 8: 491-496. doi.org/10.3920/BM2016.0196
Majeed M, Prakash L. Lactospore®: The Effective Probiotic. Piscataway, NJ: NutriScience Publishers, Inc. ISBN 0-9647856-4-1. 1998.
Sudha MR, Radkar N, Maurya A. Effect of supplementation of probiotic Bacillus coagulans unique IS-2 (ATCC PAT-11748) on hypercholesterolemic subjects: a clinical study. Int J Probiotics Prebiotics. 2011; 6: 89.
Upadrasta A, Madempudi RS. Probiotics and blood pressure: current insights. Integr. Blood Press. Control. 2016; 9: 33-42. doi.org/10.2147/IBPC.S73246
Sudha MR, Yelikar KA, Deshpande S. Clinical study of Bacillus coagulans unique IS-2 (ATCC PTA-11748) in the treatment of patients with bacterial vaginosis. Indian J Microbiol. 2012; 52: 396-399. doi.org/10.1007/s12088-011-0233-z
Sudha RM, Bhonagiri S. Efficacy of bacillus coagulans strain Unique IS-2 in the treatment of patients with acute diarrhea. Int J Probiotics Prebiotics. 2012; 7: 33-37.
Haldar L, Gandhi DN. Effect of oral administration of Bacillus coagulans B37 and Bacillus pumilus B9 strains on fecal coliforms, Lactobacillus and Bacillus spp. in rat animal model. Veterinary World. 2016; 9: 766-772. doi.org/10.14202/vetworld.2016.766-772
Hun L. Original Research: Bacillus coagulans Significantly Improved Abdominal Pain and Bloating in Patients with IBS. J Postgrad Med. 2009; 121: 119-124. doi.org/10.3810/pgm.2009.03.1984
Nyangale EP, Farmer S, Cash HA, Keller D, Chernoff D, Gibson GR. Bacillus coagulans GBI-30, 6086 Modulates Faecalibacterium prausnitzii in Older Men and Women. Int J Nutr. 2015; 145: 1446-1452. doi.org/10.3945/jn.114.199802
Adami A, Cavazzoni V. Occurrence of selected bacterial groups in the faeces of piglets fed with Bacillus coagulans as probiotic. J Basic Microbiol. 1999; 39: 3-9.
Donskey C, Hoyen CK, Das SM, Farmer S, Dery M, Bonomo RA. Effect of oral Bacillus coagulans administration on the density of vancomycin‐resistant enterococci in the stool of colonized mice. Lett Appl Microbiol. 2001; 33: 84-88. PMID: 11442822
Endres JR, Clewell A, Jade KA, Farber T, Hauswirth J, Schauss AG. Safety assessment of a proprietary preparation of a novel Probiotic, Bacillus coagulans, as a food ingredient. Food Chem Toxicol. 2009; 47: 1231-1238. doi.org/10.1016/j.fct.2009.02.018
Endres JR, Qureshi I, Farber T, Hauswirth J, Hirka G, Pasics I, Schauss AG. One-year chronic oral toxicity with combined reproduction toxicity study of a novel probiotic, Bacillus coagulans, as a food ingredient. Food Chem Toxicol. 2011; 49: 1174-1182. doi.org/10.1016/j.fct.2011.02.012
Khatri I, Sharma S, Ramya TNC, Subramanian S. Complete genomes of Bacillus coagulans S-lac and Bacillus subtilis TO-A JPC, two phylogenetically distinct probiotics. PloS ONE. 2016; 11: 0156745. doi.org/10.1371/journal.pone.0156745
Rhee MS, Moritz BE, Xie G, Del Rio TG, Dalin E, Tice H, Bruce D, Goodwin L, Chertkov O, Brettin T. Complete genome sequence of a thermotolerant sporogenic lactic acid bacterium, Bacillus coagulans strain 36D1. Stand Genomic Sci. 2011; 5: 331. doi.org/10.4056/sigs.2365342.
Yao G, Gao P, Zhang W. Complete genome sequence of probiotic Bacillus coagulans HM-08: A potential lactic acid producer. J Biotechnol. 2016; 228: 71-72. doi.org/10.1016/j.jbiotec.2016.04.045.