Journal Home > Volume 13 , Issue 1

Weizmannia coagulans (formerly Bacillus coagulans) is a spore-forming and lactic acid-producing bacterium. It has recently attracted much attention from researchers and food manufacturers due to its probiotic functions and stability in processing and storage. W. coagulans is capable of improving gut health through the regulation of gut microbiota, modulation of immunity, and improving digestibility and metabolism. Spores, germinated cells and metabolites of W. coagulans modulate the gut micro-environment and further affect other organs. W. coagulans is an environment-friendly probiotic since it can contribute to the host by reconstructing the balance of gut microbiota and only temporarily resides in the intestine after administration. W. coagulans has been generally recognized as safe (GRAS) by the US Food and Drug Administration (FDA), thus it is an ideal probiotic for improving gut health. The merit of its stability in processing and storage provides W. coagulans spores many possibilities for its use in various types of functional foods. This review presents an overview of the characteristics of W. coagulans that make it an ideal probiotic candidate and highlights the proposed health benefits with scientific evidence conferred by the administration of W. coagulans.


menu
Abstract
Full text
Outline
About this article

Weizmannia coagulans: an ideal probiotic for gut health

Show Author's information Shiqi Zhanga,bPinglan Lia,cSuwon LeebYu WangaChunming Tana,cNan Shangc,d,( )
Key Laboratory of Functional Dairy, Ministry of Education, College of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100083, China
Coree Beijing Co., Ltd., Beijing 101312, China
Key Laboratory of Precision Nutrition and Food Quality, Department of Nutrition and Health, China Agricultural University, Beijing 100083, China
College of Engineering, China Agricultural University, Beijing 100083, China

Peer review under responsibility of Tsinghua University Press.

Abstract

Weizmannia coagulans (formerly Bacillus coagulans) is a spore-forming and lactic acid-producing bacterium. It has recently attracted much attention from researchers and food manufacturers due to its probiotic functions and stability in processing and storage. W. coagulans is capable of improving gut health through the regulation of gut microbiota, modulation of immunity, and improving digestibility and metabolism. Spores, germinated cells and metabolites of W. coagulans modulate the gut micro-environment and further affect other organs. W. coagulans is an environment-friendly probiotic since it can contribute to the host by reconstructing the balance of gut microbiota and only temporarily resides in the intestine after administration. W. coagulans has been generally recognized as safe (GRAS) by the US Food and Drug Administration (FDA), thus it is an ideal probiotic for improving gut health. The merit of its stability in processing and storage provides W. coagulans spores many possibilities for its use in various types of functional foods. This review presents an overview of the characteristics of W. coagulans that make it an ideal probiotic candidate and highlights the proposed health benefits with scientific evidence conferred by the administration of W. coagulans.

Keywords: Microbiota, Probiotics, Spore former, Gut disorders, Weizmannia coagulans

References(123)

[1]

FAO/WHO, Working group report on drafting guidelines for the evaluation of probiotics in food, World Health Organization and Food and Agriculture Organization of the United Nations (2002) Ontario: London.

[2]

F.M.F. Elshaghabee, N. Rokana, R.D. Gulhane, et al., Bacillus as potential probiotics: status, concerns, and future perspectives, Front. Microbiol. 8(2017) 1490. https://doi.org/10.3389/fmicb.2017.01490.

[3]

P. Shokryazdan, M. Faseleh Jahromi, J.B. Liang, et al., Probiotics: from isolation to application, J. Am. Coll. Nutr. 36 (2017) 666-676. https://doi.org/10.1080/07315724.2017.1337529.

[4]

A. Velayati, I. Kareem, M. Sedaghat, et al., Does symbiotic supplementation which contains Bacillus coagulans, Lactobacillus rhamnosus, Lactobacillus acidophilus and fructooligosaccharide has favourite effects in patients with type-2 diabetes? A randomised, doubleblind, placebo-controlled trial, Arch. Physiol. Biochem. (2021) 1-8. https://doi.org/10.1080/13813455.2021.1928225.

[5]

T. Takimoto, M. Hatanaka, T. Hoshino, et al., Effect of Bacillus subtilis C-3102 on bone mineral density in healthy postmenopausal Japanese women: a randomized, placebo-controlled, double-blind clinical trial, Biosci. Microb. Food H. 37 (2018) 87-96. https://doi.org/10.12938/bmfh.18-006.

[6]

J. Heo, S.K. Kim, K.S. Park, et al., A double-blind, randomized, active drug comparative, parallel-group, multi-center clinical study to evaluate the safety and efficacy of probiotics (Bacillus licheniformis, Zhengchangsheng(R)capsule) in patients with diarrhea, Intest. Res. 12 (2014) 236-44. https://doi.org/10.5217/ir.2014.12.3.236.

[7]

B.W. Hammer, Bacteriological studies on the coagulation of evaporated milk, Research Bulletin (Iowa Agriculture and Home Economics Experiment Station) 2 (1918) 119-132.

[8]

L. Drago, E. De Vecchi, Should Lactobacillus sporogenes and Bacillus coagulans have a future?, J. Chemotherapy 21 (2009) 371-377. https://doi.org/10.1179/joc.2009.21.4.371.

[9]

E.P. Nyangale, S. Farmer, H.A. Cash, et al., Bacillus coagulans GBI-30,6086 modulates faecalibacterium prausnitzii in older men and women, J. Nutr. 145 (2015) 1446-52. https://doi.org/10.3945/jn.114.199802.

[10]

S. Zhao, X. Peng, Q.Y. Zhou, et al., Bacillus coagulans 13002 and fructooligosaccharides improve the immunity of mice with immunosuppression induced by cyclophosphamide through modulating intestinal-derived and fecal microbiota, Food Res. Int. 140 (2021) 109793. https://doi.org/10.1016/j.foodres.2020.109793.

[11]

A.K. Gupta, C. Maity, Efficacy and safety of Bacillus coagulans LBSC in irritable bowel syndrome: a prospective, interventional, randomized, doubleblind, placebo-controlled clinical study, Medicine (Baltimore) 100 (2021) e23641. https://doi.org/10.1097/MD.0000000000023641.

[12]

P. Kundu, E. Blacher, E. Elinav, et al., Our gut microbiome: the evolving inner self, Cell 171 (2017) 1481-1493. https://doi.org/https://doi.org/10.1016/j.cell.2017.11.024.

[13]

W.A. Walker, The importance of appropriate initial bacterial colonization of the intestine in newborn, child, and adult health, Pediatr. Res. 82 (2017) 387-395. https://doi.org/10.1038/pr.2017.111.

[14]

A. Andremont, J. Cervesi, P.A. Bandinelli, et al., Spare and repair the gut microbiota from antibiotic-induced dysbiosis: state-of-the-art, Drug Discov. Today (2021). https://doi.org/10.1016/j.drudis.2021.02.022.

[15]

K. Parkin, C.T. Christophersen, V. Verhasselt, et al., Risk factors for gut dysbiosis in early life, Microorganisms 9 (2021). https://doi.org/10.3390/microorganisms9102066.

[16]

M. Aguilera, M. Cerda-Cuellar, V. Martinez, Antibiotic-induced dysbiosis alters host-bacterial interactions and leads to colonic sensory and motor changes in mice, Gut Microbes 6 (2015) 10-23. https://doi.org/10.4161/19490976.2014.990790.

[17]

R. Maslennikov, V. Ivashkin, I. Efremova, et al., Gut dysbiosis and small intestinal bacterial overgrowth as independent forms of gut microbiota disorders in cirrhosis, World J. Gastroenterol 28 (2022) 1067-1077. https://doi.org/10.3748/wjg.v28.i10.1067.

[18]

B. Fairfield, B. Schnabl, Gut dysbiosis as a driver in alcohol-induced liver injury, JHEP Rep. 3 (2021) 100220. https://doi.org/10.1016/j.jhepr.2020.100220.

[19]

T. Hrncir, Gut microbiota dysbiosis: triggers, consequences, diagnostic and therapeutic options, Microorganisms 10 (2022). https://doi.org/10.3390/microorganisms10030578.

[20]

C. Duvallet, S.M. Gibbons, T. Gurry, et al., Meta-analysis of gut microbiome studies identifies disease-specific and shared responses, Nat. Commun. 8(2017) 1784. https://doi.org/10.1038/s41467-017-01973-8.

[21]

H. Duan, L. Yu, F. Tian, et al., Antibiotic-induced gut dysbiosis and barrier disruption and the potential protective strategies, Crit. Rev. Food. Sci. Nutr. (2020) 1-26. https://doi.org/10.1080/10408398.2020.1843396.

[22]

K. Abhari, S.S. Shekarforoush, J. Sajedianfard, et al., The effects of probiotic, prebiotic and synbiotic diets containing Bacillus coagulans and inulin on rat intestinal microbiota, Iran J. Vet. Res. 16 (2015) 267-73.

[23]

A. Adami, V. Cavazzoni, Occurrence of selected bacterial groups in the faeces of piglets fed with Bacillus coagulans as probiotic, J. Basic Microbio. 39 (1999) 3-9. https://doi.org/10.1002/(SICI)1521-4028(199903)39:1<3::AID-JOBM3>3.0.CO;2-O.

[24]

M.E. Sanders, D.J. Merenstein, G. Reid, et al., Probiotics and prebiotics in intestinal health and disease: from biology to the clinic, Nat. Rev. Gastroenterol. Hepatol. 16 (2019) 605-616. https://doi.org/10.1038/s41575-019-0173-3.

[25]

E.B. Daliri, B.H. Lee, New perspectives on probiotics in health and disease, Food SCI. Hum. Well. 4 (2015) 56-65. https://doi.org/10.1016/j.fshw.2015.06.002.

[26]

L.M. Rocha-Ramirez, U. Hernandez-Chinas, S.S. Moreno-Guerrero, et al., Probiotic properties and immunomodulatory activity of Lactobacillus strains isolated from dairy products, Microorganisms 9 (2021). https://doi.org/10.3390/microorganisms9040825.

[27]

W. Holzapfel, A. Arini, M. Aeschbacher, et al., Enterococcus faecium SF68 as a model for efficacy and safety evaluation of pharmaceutical probiotics, Benef. Microbes 9 (2018) 375-388. https://doi.org/10.3920/BM2017.0148.

[28]

T. Didari, S. Solki, S. Mozaffari, et al., A systematic review of the safety of probiotics, Expert Opin. Drug. Saf. 13 (2014) 227-39. https://doi.org/10.1517/14740338.2014.872627.

[29]

K. Abdhul, M. Ganesh, S. Shanmughapriya, et al., Bacteriocinogenic potential of a probiotic strain Bacillus coagulans [BDU3] from Ngari, Int. J. Biol. Macromol. 79 (2015) 800-806. https://doi.org/10.1016/j.ijbiomac.2015.06.005.

[30]

Y. Yu, X. Yu, J. Ouyang, et al., Complete genome sequence of Bacillus coagulans BC01, a promising human probiotic strain isolated from thick broad bean sauce, Microbiol. Resour. Announc. 10 (2021). https://doi.org/10.1128/MRA.00392-21.

[31]

G. Konuray, Z. Erginkaya, Potential use of Bacillus coagulans in the food industry, Foods 7 (2018) 1-10. https://doi.org/10.3390/foods7060092.

[32]

M. Koopaie, M. Fatahzadeh, S. Jahangir, et al., Comparison of the effect of regular and probiotic cake (Bacillus coagulans) on salivary pH and Streptococcus mutans count, Dent. Med. Probl. 56 (2019) 33-38. https://doi.org/10.17219/dmp/99757.

[33]

R.S. Gupta, S. Patel, N. Saini, et al., Robust demarcation of 17 distinct Bacillus species clades, proposed as novel Bacillaceae genera, by phylogenomics and comparative genomic analyses: description of Robertmurraya kyonggiensis sp. nov. and proposal for an emended genus Bacillus limiting it only to the members of the Subtilis and Cereus clades of species, Int. J. Syst. Evol. Microbiol. 70 (2020) 5753-5798. https://doi.org/10.1099/ijsem.0.004475.

[34]

W.Y. Bang, O.H. Ban, B.S. Lee, et al., Genomic-, phenotypic-, and toxicitybased safety assessment and probiotic potency of Bacillus coagulans IDCC 1201 isolated from green malt, J. Ind. Microbiol. Biotechnol. 48 (2021). https://doi.org/10.1093/jimb/kuab026.

[35]

W.B. Sarles, B.W. Hammer, Observations on Bacillus coagulans, J. Bacteriol. 23 (1932) 301-14. https://doi.org/10.1128/jb.23.4.301-314.1932.

[36]

M. Majeed, S. Majeed, S. Arumugam, et al., Comparative evaluation for thermostability and gastrointestinal survival of probiotic Bacillus coagulans MTCC 5856, Biosci. Biotechnol. Biochem. 85 (2021) 962-971. https://doi.org/10.1093/bbb/zbaa116.

[37]

C. Gonzalez-Ferrero, J.M. Irache, C.J. Gonzalez-Navarro, Soybean proteinbased microparticles for oral delivery of probiotics with improved stability during storage and gut resistance, Food Chem. 239 (2018) 879-888. https://doi.org/10.1016/j.foodchem.2017.07.022.

[38]

Y. Mu, Y. Cong, Bacillus coagulans and its applications in medicine, Benef. Microbes 10 (2019) 679-688. https://doi.org/10.3920/BM2018.0016.

[39]

D. Keller, S. Verbruggen, H. Cash, et al., Spores of Bacillus coagulans GBI-30,6086 show high germination, survival and enzyme activity in a dynamic, computer-controlled in vitro model of the gastrointestinal tract, Benef. Microbes 10 (2019) 77-87. https://doi.org/10.3920/BM2018.0037.

[40]

N.K. Tam, N.Q. Uyen, H.A. Hong, et al., The intestinal life cycle of Bacillus subtilis and close relatives, J. Bacteriol. 188 (2006) 2692-2700. https://doi.org/10.1128/JB.188.7.2692-2700.2006.

[41]

C. Gusils, S. Cuozzo, F. Sesma, et al., Examination of adhesive determinants in three species of Lactobacillus isolated from chicken, Can. J. Microbiol. 48(2002) 34-42. https://doi.org/10.1139/w01-122.

[42]

T. Wakai, C. Kano, H. Karsens, et al., Functional role of surface layer proteins of Lactobacillus acidophilus L-92 in stress tolerance and binding to host cell proteins, Biosci. Microbiota Food Health 40 (2021) 33-42. https://doi.org/10.12938/bmfh.2020-005.

[43]

C.E. O'Brien, A.K. Meier, K. Cernioglo, et al., Early probiotic supplementation with B. infantis in breastfed infants leads to persistent colonization at 1 year, Pediatr. Res. 91 (2022) 627-636. https://doi.org/10.1038/s41390-020-01350-0.

[44]

S. Roy Sarkar, P. Mitra Mazumder, S. Banerjee, Probiotics protect against gut dysbiosis associated decline in learning and memory, J. Neuroimmunol. 348 (2020) 577390. https://doi.org/10.1016/j.jneuroim.2020.577390.

[45]

P. Louis, H.J. Flint, Formation of propionate and butyrate by the human colonic microbiota, Environ. Microbiol. 19 (2017) 29-41. https://doi.org/10.1111/1462-2920.13589.

[46]

K.C.K. Poelaert, J. Van Cleemput, K. Laval, et al., Beyond gut instinct: metabolic short-chain fatty acids moderate the pathogenesis of alphaherpesviruses, Front. Microbiol. 10 (2019) 723. https://doi.org/10.3389/fmicb.2019.00723.

[47]

S.A. Mekonnen, D. Merenstein, C.M. Fraser, et al., Molecular mechanisms of probiotic prevention of antibiotic-associated diarrhea, Curr. Opin. Biotechnol. 61(2020) 226-234. https://doi.org/10.1016/j.copbio.2020.01.005.

[48]

Z. Zheng, C. Ma, C. Gao, et al., Efficient conversion of phenylpyruvic acid to phenyllactic acid by using whole cells of Bacillus coagulans SDM, PLoS One 6 (2011) e19030. https://doi.org/10.1371/journal.pone.0019030.

[49]

S.C. Xing, J.D. Mi, J.Y. Chen, et al., Metabolic activity of Bacillus coagulans R11 and the health benefits of and potential pathogen inhibition by this species in the intestines of laying hens under lead exposure, Sci. Total Environ. 709 (2020) 134507. https://doi.org/10.1016/j.scitotenv.2019.134507.

[50]

C.Y. Saw, T.J. Chang, P.Y. Chen, et al., Presence of Bacillus coagulans spores and vegetative cells in rat intestine and feces and their physiological effects, Biosci. Biotechnol. Biochem. 83 (2019) 2327-2333. https://doi.org/1 0.1080/09168451.2019.1651628.

[51]

K. Sasaki, D. Sasaki, J. Inoue, et al., Bacillus coagulans SANK 70258 suppresses Enterobacteriaceae in the microbiota of ulcerative colitis in vitro and enhances butyrogenesis in healthy microbiota, Appl. Microbiol. Biotechnol. 104(2020) 3859-3867. https://doi.org/10.1007/s00253-020-10506-1.

[52]

R. Sulthana, A.C. Archer, Bacteriocin nanoconjugates: boon to medical and food industry, J. Appl. Microbiol. 131 (2021) 1056-1071. https://doi.org/10.1111/jam.14982.

[53]

A. Fernandes, R. Jobby, Bacteriocins from lactic acid bacteria and their potential clinical applications, Appl. Biochem. Biotechnol. (2022). https://doi.org/10.1007/s12010-022-03870-3.

[54]

V. Sharma, K. Harjai, G. Shukla, Effect of bacteriocin and exopolysaccharides isolated from probiotic on P. aeruginosa PAO1 biofilm, Folia. Microbiol. (Praha) 63 (2018) 181-190. https://doi.org/10.1007/s12223-017-0545-4.

[55]

C. Le Marrec, B. Hyronimus, P. Bressollier, et al., Biochemical and genetic characterization of coagulin, a new antilisterial bacteriocin in the pediocin family of bacteriocins, produced by Bacillus coagulans I(4), Appl. Environ. Microbiol. 66 (2000) 5213-5220. https://doi.org/10.1128/AEM.66.12.5213-5220.2000.

[56]

L. Fu, C. Wang, X. Ruan, et al., Preservation of large yellow croaker (Pseudosciaena crocea) by Coagulin L1208, a novel bacteriocin produced by Bacillus coagulans L1208, Int. J. Food Microbiol. 266 (2018) 60-68. https://doi.org/10.1016/j.ijfoodmicro.2017.11.012.

[57]

E. Huszcza, B. Burczyk, Surfactin isoforms from Bacillus coagulans, Z. Naturforsch C.J. Biosci. 61 (2006) 727-733. https://doi.org/10.1515/znc-2006-9-1020.

[58]

S. Riazi, R.E. Wirawan, V. Badmaev, et al., Characterization of lactosporin, a novel antimicrobial protein produced by Bacillus coagulans ATCC 7050, J. Appl. Microbiol. 106 (2009) 1370-1377. https://doi.org/10.1111/j.1365-2672.2008.04105.x.

[59]

E.A.E. Abada, Isolation and characterization of a antimicrobial compound from Bacillus coagulans, Anim. Cells Syst. 12 (2008) 41-46. https://doi.org/10.1080/19768354.2008.9647152.

[60]

A. Ouwehand, E. Isolauri, S. Salminen, The role of the intestinal microflora for the development of the immune system in early childhood, Eur. J. Nutr. 41 (2002) 32-37. https://doi.org/10.1007/s00394-002-1105-4.

[61]

A. Ancona, C. Petito, I. Iavarone, et al., The gut-brain axis in irritable bowel syndrome and inflammatory bowel disease, Dig. Liver Dis. 53 (2021) 298-305. https://doi.org/10.1016/j.dld.2020.11.026.

[62]

E.R. Guzman-Bautista, K. Suzuki, S. Asami, et al., Bacteria-immune cells dialog and the homeostasis of the systems, Curr. Opin. Immunol. 66 (2020) 82-89. https://doi.org/10.1016/j.coi.2020.05.010.

[63]

R. Frei, M. Akdis, L. O'Mahony, Prebiotics, probiotics, synbiotics, and the immune system: experimental data and clinical evidence, Curr. Opin. Gastroenterol. 31 (2015) 153-158. https://doi.org/10.1097/MOG.0000000000000151.

[64]

S. Hougee, A.J. Vriesema, S.C. Wijering, et al., Oral treatment with probiotics reduces allergic symptoms in ovalbumin-sensitized mice: a bacterial strain comparative study, Int. Arch. Allergy Immunol. 151 (2010) 107-117. https://doi.org/10.1159/000236000.

[65]

H. Szajewska, A. Skorka, M. Ruszczynski, et al., Meta-analysis: Lactobacillus GG for treating acute gastroenteritis in children--updated analysis of randomised controlled trials, Aliment Pharmacol. Ther. 38 (2013) 467-476. https://doi.org/10.1111/apt.12403.

[66]

Y. Liu, J. Wang, C. Wu, Modulation of gut microbiota and immune system by probiotics, pre-biotics, and post-biotics, Front. Nutr. 8 (2021) 634897. https://doi.org/10.3389/fnut.2021.634897.

[67]

M. Kalliomaki, S. Salminen, H. Arvilommi, et al., Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial, Lancet 357 (2001) 1076-1079. https://doi.org/10.1016/S0140-6736(00)04259-8.

[68]

C. Gruber, M. Wendt, C. Sulser, et al., Randomized, placebo-controlled trial of Lactobacillus rhamnosus GG as treatment of atopic dermatitis in infancy, Allergy 62 (2007) 1270-1276. https://doi.org/10.1111/j.1398-9995.2007.01543.x.

[69]

T.V. Bomko, T.N. Nosalskaya, T.V. Kabluchko, et al., Immunotropic aspect of the Bacillus coagulans probiotic action, J. Pharm. Pharmacol. 69 (2017) 1033-1040. https://doi.org/10.1111/jphp.12726.

[70]

T. Shinde, A.P. Perera, R. Vemuri, et al., Synbiotic supplementation with prebiotic green banana resistant starch and probiotic Bacillus coagulans spores ameliorates gut inflammation in mouse model of inflammatory bowel diseases, Eur. J. Nutr. 59 (2020) 3669-3689. https://doi.org/10.1007/s00394-020-02200-9.

[71]

L.R. Fitzpatrick, J.S. Small, W.H. Greene, et al., Bacillus coagulans GBI-30(BC30) improves indices of Clostridium difficile-induced colitis in mice, Gut Pathog. 3 (2011) 16. https://doi.org/10.1186/1757-4749-3-16.

[72]

L.R. Fitzpatrick, J.S. Small, W.H. Greene, et al., Bacillus coagulans GBI-30,6086 limits the recurrence of Clostridium difficile-induced colitis following vancomycin withdrawal in mice, Gut Pathog. 4 (2012) 13. https://doi.org/10.1186/1757-4749-4-13.

[73]

K. Abhari, S.S. Shekarforoush, S. Hosseinzadeh, et al., The effects of orally administered Bacillus coagulans and inulin on prevention and progression of rheumatoid arthritis in rats, Food Nutr. Res. 60 (2016) 30876. https://doi.org/10.3402/fnr.v60.30876.

[74]

Y. Wang, J. Lin, Z. Cheng, et al., Bacillus coagulans TL3 inhibits LPSinduced caecum damage in rat by regulating the TLR4/MyD88/NF-kappaB and Nrf2 signal pathways and modulating intestinal microflora, Oxid Med. Cell Longev. 2022 (2022) 5463290. https://doi.org/10.1155/2022/5463290.

[75]

M. Pyclik, D. Srutkova, M. Schwarzer, et al., Bifidobacteria cell wallderived exo-polysaccharides, lipoteichoic acids, peptidoglycans, polar lipids and proteins -their chemical structure and biological attributes, Int. J. Biol. Macromol. 147 (2020) 333-349. https://doi.org/10.1016/j.ijbiomac.2019.12.227.

[76]

S.S. Kang, J.R. Sim, C.H. Yun, et al., Lipoteichoic acids as a major virulence factor causing inflammatory responses via Toll-like receptor 2, Arch. Pharm. Res. 39 (2016) 1519-1529. https://doi.org/10.1007/s12272-016-0804-y.

[77]

A.D. Friedrich, J. Leoni, M.L. Paz, et al., Lipoteichoic acid from Lacticaseibacillus rhamnosus GG modulates dendritic cells and T cells in the gut, Nutrients 14 (2022) 1-15. https://doi.org/10.3390/nu14030723.

[78]

W.J. Kim, J.H. Hyun, N.K. Lee, et al., Protective effects of a novel Lactobacillus brevis strain with probiotic characteristics against staphylococcus aureus lipoteichoic acid-induced intestinal inflammatory response, J. Microbiol. Biotechnol. 32 (2022) 205-211. https://doi.org/10.4014/jmb.2110.10034.

[79]

G.S. Jensen, K.F. Benson, S.G. Carter, et al., GanedenBC30 cell wall and metabolites: anti-inflammatory and immune modulating effects in vitro, BMC Immunology 11 (2010) 1-14. https://doi.org/10.1186/1471-2172-11-15.

[80]

N.K. Lee, W.S. Kim, H.D. Paik, Bacillus strains as human probiotics: characterization, safety, microbiome, and probiotic carrier, Food Sci. Biotechnol. 28 (2019) 1297-1305. https://doi.org/10.1007/s10068-019-00691-9.

[81]

M.H. Foley, S. O'Flaherty, G. Allen, et al., Lactobacillus bile salt hydrolase substrate specificity governs bacterial fitness and host colonization, Proc. Natl. Acad. Sci. U.S.A. 118 (2021). https://doi.org/10.1073/pnas.2017709118.

[82]

Y. Hao, P. Zhou, Y.J. Zhu, et al., Gut microbbiota dysbiosis and altered bile acid catabolism lead to metabolic disorder in psoriasis mice, Front. Microbiol. 13 (2022) 853566. https://doi.org/10.3389/fmicb.2022.853566.

[83]

N. Batra, J. Singh, U.C. Banerjee, et al., Production and characterization of a thermostable beta-galactosidase from Bacillus coagulans RCS3, Biotechnol. Appl. Biochem. 36 (2002) 1-6. https://doi.org/10.1042/ba20010091.

[84]

P. Liu, J. Xie, J. Liu, et al., A novel thermostable beta-galactosidase from Bacillus coagulans with excellent hydrolysis ability for lactose in whey, J. Dairy. Sci. 102 (2019) 9740-9748. https://doi.org/10.3168/jds.2019-16654.

[85]

M. Aulitto, A. Strazzulli, F. Sansone, et al., Prebiotic properties of Bacillus coagulans MA-13: production of galactoside hydrolyzing enzymes and characterization of the transglycosylation properties of a GH42 betagalactosidase, Microb. Cell Fact. 20 (2021) 71. https://doi.org/10.1186/s12934-021-01553-y.

[86]

H. Alkan, Z. Baysal, F. Uyar, et al., Production of lipase by a newly isolated Bacillus coagulans under solid-state fermentation using melon wastes, Appl. Biochem. Biotechnol. 136 (2007) 183-192. https://doi.org/10.1007/BF02686016.

[87]

B. Zhang, H. Zhang, Y. Yu, et al., Effects of Bacillus coagulans on growth performance, antioxidant capacity, immunity function, and gut health in broilers, Poultry Science 100 (2021) 1-10. https://doi.org/10.1016/j.psj.2021.101168.

[88]

R. Horne, J.A. Foster, Metabolic and microbiota measures as peripheral biomarkers in major depressive disorder, Front. Psychiatry. 9 (2018) 513. https://doi.org/10.3389/fpsyt.2018.00513.

[89]

S.M. Jandhyala, R. Talukdar, C. Subramanyam, et al., Role of the normal gut microbiota, World J. Gastroenterol. 21 (2015) 8787-8803. https://doi.org/10.3748/wjg.v21.i29.8787.

[90]

C. Osinski, D. Moret, K. Clement, et al., Enteroendocrine system and gut barrier in metabolic disorders, Int. J. Mol. Sci. 23 (2022). https://doi.org/10.3390/ijms23073732.

[91]

L. Bordalo Tonucci, K.M. Dos Santos, C.L. De Luces Fortes Ferreira, et al., Gut microbiota and probiotics: Focus on diabetes mellitus, Crit. Rev. Food. Sci. Nutr. 57 (2017) 2296-2309. https://doi.org/10.1080/10408398.2014.934438.

[92]

M. Kriss, K.Z. Hazleton, N.M. Nusbacher, et al., Low diversity gut microbiota dysbiosis: drivers, functional implications and recovery, Curr. Opin. Microbiol. 44 (2018) 34-40. https://doi.org/10.1016/j.mib.2018.07.003.

[93]

C.N. Almada-Erix, C.N. Almada, L. Cabral, et al., Orange juice and yogurt carrying probiotic Bacillus coagulans GBI-306086: impact of intake on Wistar male rats health parameters and gut bacterial diversity, Front. Microbiol. 12 (2021) 623951. https://doi.org/10.3389/fmicb.2021.623951.

[94]

R. Urtasun, J. Diaz-Gomez, M. Arana, et al., A combination of apple vinegar drink with Bacillus coagulans ameliorates high fat diet-induced body weight gain, insulin resistance and hepatic steatosis, Nutrients 12 (2020). https://doi.org/10.3390/nu12092504.

[95]

Y. Lee, R. Yoshitsugu, K. Kikuchi, et al., Combination of soya pulp and Bacillus coagulans lilac-01 improves intestinal bile acid metabolism without impairing the effects of prebiotics in rats fed a cholic acid-supplemented diet, Br. J. Nutr. 116 (2016) 603-610. https://doi.org/10.1017/S0007114516002270.

[96]

S. Kang, M.Y. Park, I. Brooks, et al., Spore-forming Bacillus coagulans SNZ 1969 improved intestinal motility and constipation perception mediated by microbial alterations in healthy adults with mild intermittent constipation: A randomized controlled trial, Food Res. Int. 146 (2021) 110428. https://doi.org/10.1016/j.foodres.2021.110428.

[97]

K. Minamida, M. Nishimura, K. Miwa, et al., Effects of dietary fiber with Bacillus coagulans lilac-01 on bowel movement and fecal properties of healthy volunteers with a tendency for constipation, Biosci. Biotechnol. Biochem. 79 (2015) 300-306. https://doi.org/10.1080/09168451.2014.972331.

[98]

C. Maity, A.K. Gupta, A prospective, interventional, randomized, doubleblind, placebo-controlled clinical study to evaluate the efficacy and safety of Bacillus coagulans LBSC in the treatment of acute diarrhea with abdominal discomfort, Eur. J. Clin. Pharmacol. 75 (2019) 21-31. https://doi.org/10.1007/s00228-018-2562-x.

[99]

M.R. Sudha, N. Jayanthi, M. Aasin, et al., Efficacy of Bacillus coagulans Unique IS2 in treatment of irritable bowel syndrome in children: a double blind, randomised placebo controlled study, Benef. Microbes 9 (2018) 563-572. https://doi.org/10.3920/BM2017.0129.

[100]

M. Majeed, K. Nagabhushanam, S. Natarajan, et al., Bacillus coagulans MTCC 5856 supplementation in the management of diarrhea predominant irritable bowel syndrome: a double blind randomized placebo controlled pilot clinical study, Nutr. J. 15 (2016) 21. https://doi.org/10.1186/s12937-016-0140-6.

[101]

L. Hun, Bacillus coagulans significantly improved abdominal pain and bloating in patients with IBS, Postgrad. Med. 121 (2009) 119-124. https://doi.org/10.3810/pgm.2009.03.1984.

[102]

K. Abhari, S. Saadati, F. Hosseini-Oskouiee, et al., Is Bacillus coagulans supplementation plus low FODMAP diet superior to low FODMAP diet in irritable bowel syndrome management?, Eur. J. Nutr. 59 (2020) 2111-2117. https://doi.org/10.1007/s00394-019-02060-y.

[103]

B.J. Dolin, Effects of a proprietary Bacillus coagulans preparation on symptoms of diarrhea-predominant irritable bowel syndrome, Methods Find Exp. Clin. Pharmacol. 31 (2009) 655-659. https://doi.org/10.1358/mf.2009.31.10.1441078.

[104]

K. Abhari, S. Saadati, Z. Yari, et al., The effects of Bacillus coagulans supplementation in patients with non-alcoholic fatty liver disease: a randomized, placebo-controlled, clinical trial, Clin. Nutr. ESPEN 39 (2020) 53-60. https://doi.org/10.1016/j.clnesp.2020.06.020.

[105]

D.R. Mandel, K. Eichas, J. Holmes, Bacillus coagulans: a viable adjunct therapy for relieving symptoms of rheumatoid arthritis according to a randomized, controlled trial, BMC Complem. Altern. M. 10 (2010) 1-7. https://doi.org/10.1186/1472-6882-10-1.

[106]

M. Tarik, L. Ramakrishnan, N. Bhatia, et al., The effect of Bacillus coagulans Unique IS-2 supplementation on plasma amino acid levels and muscle strength in resistance trained males consuming whey protein: a double-blind, placebo-controlled study, Eur. J. Nutr. (2022). https://doi.org/10.1007/s00394-022-02844-9.

[107]

R.A. Stecker, J.M. Moon, T.J. Russo, et al., Bacillus coagulans GBI-30,6086 improves amino acid absorption from milk protein, Nutr. Metab. (Lond) 17 (2020) 93. https://doi.org/10.1186/s12986-020-00515-2.

[108]

V.V. Kumar, K.M. Sudha, S. Bennur, et al., A prospective, randomized, open-label, placebo-controlled comparative study of Bacillus coagulans GBI-30,6086 with digestive enzymes in improving indigestion in geriatric population, J. Family Med. Prim. Care 9 (2020) 1108-1112. https://doi.org/10.4103/jfmpc.jfmpc_922_19.

[109]

M.A. Anaya-Loyola, J.A. Enciso-Moreno, J.E. Lopez-Ramos, et al., Bacillus coagulans GBI-30,6068 decreases upper respiratory and gastrointestinal tract symptoms in healthy Mexican scholar-aged children by modulating immune-related proteins, Food Res. Int. 125 (2019) 108567. https://doi.org/10.1016/j.foodres.2019.108567.

[110]

M. Baron, A patented strain of Bacillus coagulans increased immune response to viral challenge, Postgrad. Med. 121 (2009) 114-118. https://doi.org/10.3810/pgm.2009.03.1971.

[111]

R.S. Madempudi, J. Neelamraju, J.J. Ahire, et al., Bacillus coagulans Unique IS2 in constipation: a double-blind, placebo-controlled study, Probiotics Antimicrob. 12 (2020) 335-342. https://doi.org/10.1007/s12602-019-09542-9.

[112]

M.R. Sudha, S. Bhonagiri, Efficacy of Bacillus coagulans strain Unique IS2 in the treatment of patients with acute diarrhea, Int. J. Probiotics Prebiotics 31 (2012) 33-37.

[113]

R.K. Chandra, Effect of Lactobacillus on the incidence and severity of acute rotavirus diarrhoea in infants. A prospective placebo-controlled double-blind study, Nutr. Res. 22 (2002) 65-69. https://doi.org/10.1016/s0271-5317(01)00367-0.

[114]

M. Daniali, S. Nikfar, M. Abdollahi, Antibiotic resistance propagation through probiotics, Expert Opin. Drug. Metab. Toxicol. 16 (2020) 1207-1215. https://doi.org/10.1080/17425255.2020.1825682.

[115]

A.S. Metlakunta, R.J. Soman, Safety evaluation of Bacillus coagulans SNZ 1969 in Wistar rats, Regul. Toxicol. Pharmacol. 110 (2020) 104538. https://doi.org/10.1016/j.yrtph.2019.104538.

[116]

J.R. Endres, I. Qureshi, T. Farber, et al., One-year chronic oral toxicity with combined reproduction toxicity study of a novel probiotic, Bacillus coagulans, as a food ingredient, Food Chem. Toxicol. 49 (2011) 1174-1182. https://doi.org/10.1016/j.fct.2011.02.012.

[117]

L. Orru, E. Salvetti, L. Cattivelli, et al., Draft genome sequence of Bacillus coagulans GBI-30,6086, a widely used spore-forming probiotic strain, Genome Announc. 2 (2014). https://doi.org/10.1128/genomeA.01080-14.

[118]

S. Soldi, S.C. Tagliacarne, C. Valsecchi, et al., Effect of a multistrain probiotic (Lactoflorene((R)) Plus) on inflammatory parameters and microbiota composition in subjects with stress-related symptoms, Neurobiol. Stress 10 (2019) 100138. https://doi.org/10.1016/j.ynstr.2018.11.001.

[119]

A. Upadrasta, S. Pitta, R.S. Madempudi, Draft genome sequence of the spore-forming probiotic strain Bacillus coagulans Unique IS-2, Genome Announc. 4 (2016). https://doi.org/10.1128/genomeA.00225-16.

[120]

M. Majeed, K. Nagabhushanam, S. Natarajan, et al., Evaluation of genetic and phenotypic consistency of Bacillus coagulans MTCC 5856: a commercial probiotic strain, World J. Microbiol. Biotechnol. 32 (2016) 60. https://doi.org/10.1007/s11274-016-2027-2.

[121]

R. Urgesi, C. Casale, R. Pistelli, et al., A randomized double-blind placebocontrolled clinical trial on efficacy and safety of association of simethicone and Bacillus coagulans (Colinox(R)) in patients with irritable bowel syndrome, Eur. Rev. Med. Pharmacol. Sci. 18 (2014) 1344-1353.

[122]

J. Zhang, J. Guo, D. Li, et al., The efficacy and safety of Clostridium butyricum and Bacillus coagulans in Helicobacter pylori eradication treatment: An open-label, single-arm pilot study, Medicine (Baltimore) 99(2020) e22976. https://doi.org/10.1097/MD.0000000000022976.

[123]

L.I. Ouoba, B. Diawara, N.T. Annan, et al., Volatile compounds of Soumbala, a fermented African locust bean (Parkia biglobosa) food condiment, J. Appl. Microbiol. 99 (2005) 1413-1421. https://doi.org/10.1111/j.1365-2672.2005.02722.x.

Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 25 July 2022
Revised: 26 August 2022
Accepted: 22 September 2022
Published: 01 June 2023
Issue date: January 2024

Copyright

© 2024 Beijing Academy of Food Sciences. Publishing services by Tsinghua University Press.

Acknowledgements

Acknowledgement

This work was supported by National Natural Science Foundation of China (32172172, 32201994) and the Foreign Expert Collaboration Project (G2021108010L).

Rights and permissions

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return