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Open Access

Alleviative effects of Bacillus coagulans strains on irritable bowel syndrome-unraveling strain specificity through physiological and genomic analysis

Jiang Caoa,b, Leilei Yua,b, Jianxin Zhaoa,b, Hao Zhanga,b,c,d, Wei Chena,b,c, Yuzheng Xuee( ), Qixiao Zhaia,b( )
State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi 214122, China
School of Food Science and Technology, Jiangnan University, Wuxi 214122, China
National Engineering Research Center for Functional Food, Jiangnan University, Wuxi 214122, China
Wuxi Translational Medicine Research Center and Jiangsu Translational Medicine Research Institute Wuxi Branch, Wuxi 214122, China
Department of Gastroenterology, Affiliated Hospital of Jiangnan University, Wuxi 214122, China

Peer review under responsibility of Tsinghua University Press.

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Abstract

The high intraspecies heterogeneity of Baciillus coagulans leads to significant phenotypic differences among different strains. Thus, 6 B. coagulans strains were tested in the present study using an irritable bowel syndrome (IBS) animal model to determine whether the IBS-alleviating effects of B. coagulans strains are strain-specific. The results of this study showed that the ingestion of B. coagulans GBI-30, 6086, and B. coagulans CCFM1041 significantly alleviated IBS symptoms in mice. In contrast, other B. coagulans strains showed no or limited alleviating effects on IBS symptoms. According to our experimental results, the two main common features of these strains were as follows: 1) The resistance of vegetative cells to bile salts, and 2) ability to synthesize specific lipids and secondary metabolites. Screening strains based on these two indicators may greatly reduce costs and provide a basis for mining new functional B. coagulans strains. Our results also suggest that administration of B. coagulans could significantly regulate microbiota dysbiosis in animal models. Moreover, the close relationships between the gut microbiota, gut microbiota metabolites, and IBS were further confirmed in this study.

Keywords

Baciillus coagulansIrritable bowel syndromeResistance to bile saltsComparative genomic analysisGut microbiota

References

[1]

M. Majeed, K. Nagabhushanam, S. Arumugam, et al., Bacillus coagulans MTCC 5856 for the management of major depression with irritable bowel syndrome: a randomised, double-blind, placebo controlled, multi-centre, pilot clinical study, Food Nutr. Res. 62 (2018). https://doi.org/10.29219/fnr.v62.1218.
Crossref Google Scholar
[2]

Y. Liu, W. Xiao, L. Yu, et al., Evidence from comparative genomic analyses indicating that Lactobacillus-mediated irritable bowel syndrome alleviation is mediated by the conjugated linoleic acid synthesis, Food Funct. 12 (2021) 1121-1134. https://doi.org/10.1039/d0fo02616f.
Crossref Google Scholar
[3]

A.C. Ford, E.M. Quigley, B.E. Lacy, et al., Efficacy of prebiotics, probiotics, and synbiotics in irritable bowel syndrome and chronic idiopathic constipation: systematic review and meta-analysis, Am. J. Gastroenterol. 109 (2014) 1547-1561. https://doi.org/10.1038/ajg.2014.202.
Crossref Google Scholar
[4]

R.M. Lovell, A.C. Ford, Global prevalence of and risk factors for irritable bowel syndrome: a meta-analysis, Clin. Gastroenterol. Hepatol. 10 (2012) 712-721. https://doi.org/10.1016/j.cgh.2012.02.029.
Crossref Google Scholar
[5]

K.A. Gwee, U.C. Ghoshal, M. Chen, Irritable bowel syndrome in Asia: pathogenesis, natural history, epidemiology, and management, J. Gastroenterol. Hepatol. 33 (2017) 99-110. https://doi.org/10.1111/jgh.13987.
Crossref Google Scholar
[6]

H.M. Staudacher, K. Whelan, The low FODMAP diet: recent advances in understanding its mechanisms and efficacy in IBS, Gut 66 (2017) 1517-1527. https://doi.org/10.1136/gutjnl-2017-313750.
Crossref Google Scholar
[7]

R.L. Akehurst, J.E. Brazier, N. Mathers, et al., Health-related quality of life and cost impact of irritable bowel syndrome in a UK primary care setting, Pharmacoeconomics 20 (2002) 455-462. https://doi.org/10.2165/00019053-200220070-00003.
Crossref Google Scholar
[8]

U.C. Ghoshal, R. Shukla, U. Ghoshal, et al., The gut microbiota and irritable bowel syndrome: friend or foe?, Int. J. Inflam. 50 (2012) 183-199. https://doi.org/10.1016/j.gtc.2020.10.002.
Crossref Google Scholar
[9]

C.J. Martoni, S. Srivastava, G.J. Leyer, Lactobacillus acidophilus DDS-1 and Bifidobacterium lactis UABla-12 improve abdominal pain severity and symptomology in irritable bowel syndrome: randomized controlled trial, Nutrients 12 (2020) 363. https://doi.org/10.3390/nu12020363.
Crossref Google Scholar
[10]

C. Cremon, S. Guglielmetti, G. Gargari, et al., Effect of Lactobacillus paracasei CNCM I-1572 on symptoms, gut microbiota, short chain fatty acids, and immune activation in patients with irritable bowel syndrome: a pilot randomized clinical trial, United European. Gastroenterol. J. 6 (2018) 604-613. https://doi.org/10.1177/2050640617736478.
Crossref Google Scholar
[11]

A.K. Gupta, C. Maity, Efficacy and safety of Bacillus coagulans LBSC in irritable bowel syndrome: a prospective, interventional, randomized, double-blind, placebo-controlled clinical study[CONSORT Compliant], Medicine (Baltimore) 100 (2021) 23641. https://doi.org/10.1097/MD.0000000000023641.
Crossref Google Scholar
[12]

Y.M. Chen, Y. Li, X. Wang, et al. Effect of Bacillus subtilis, Enterococcus faecium, and Enterococcus faecalis supernatants on serotonin transporter expression in cells and tissues, World J. Gastroenterol. 28 (2022) 532-546. https://doi.org/10.3748/wjg.v28.i5.532.
Crossref Google Scholar
[13]

Q. Guan, T. Xiong, M. Xie, Influence of probiotic fermented fruit and vegetables on human health and the related industrial development trend, Engineering 7 (2021) 212-218. https://doi.org/10.1016/j.eng.2020.03.018.
Crossref Google Scholar
[14]

C. Cremon, S. Guglielmetti, G. Gargari, et al., Effect of Lactobacillus paracasei CNCM I-1572 on symptoms, gut microbiota, short chain fatty acids, and immune activation in patients with irritable bowel syndrome: a pilot randomized clinical trial, United European Gastroenterol. J. 6 (2018) 604-613. https://doi.org/10.1177/2050640617736478.
Crossref Google Scholar
[15]

S.P. Shin, Y.M. Choi, W.H. Kim, et al., A double blind, placebo-controlled, randomized clinical trial that breast milk derived-Lactobacillus gasseri BNR17 mitigated diarrhea-dominant irritable bowel syndrome, J. Clin. Biochem. Nutr. 62 (2018) 179-186. https://doi.org/10.3164/jcbn.17-73.
Crossref Google Scholar
[16]

J. Cao, Z. Yu, W. Liu, et al., Probiotic characteristics of Bacillus coagulans and associated implications for human health and diseases, J. Funct. Foods 64 (2020) 103643. https://doi.org/10.1016/j.jff.2019.103643.
Crossref Google Scholar
[17]

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.
Crossref Google Scholar
[18]

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.
Crossref Google Scholar
[19]

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.
Crossref Google Scholar
[20]

C. Stevenson, R. Blaauw, E. Fredericks, et al., Randomized clinical trial: effect of Lactobacillus plantarum 299 v on symptoms of irritable bowel syndrome, Nutrition 30 (2014) 1151-1157. https://doi.org/10.1016/j.nut.2014.02.010.
Crossref Google Scholar
[21]

K. Hod, R. Dekel, N.A. Cohen, et al., The effect of a multispecies probiotic on microbiota composition in a clinical trial of patients with diarrhea-predominant irritable bowel syndrome, Neurogastroenterol. Motil. 30 (2018) 13456. https://doi.org/10.1111/nmo.13456.
Crossref Google Scholar
[22]

L.M. Begtrup, O.B.S. de Muckadell, J. Kjeldsen, et al., Long-term treatment with probiotics in primary care patients with irritable bowel syndrome-a randomised, double-blind, placebo controlled trial, Scand. J. Gastroenterol. 48 (2013) 1127-1135. https://doi.org/10.3109/00365521.2013.825314.
Crossref Google Scholar
[23]

A.R. Romijn, J.J. Rucklidge, R.G. Kuijer, et al., A double-blind, randomized, placebo-controlled trial of Lactobacillus helveticus and Bifidobacterium longum for the symptoms of depression, Aust. N. Z. J. Psychiatry 51 (2017) 810-821. https://doi.org/10.1177/0004867416686694.
Crossref Google Scholar
[24]

L.V. McFarland, T. Karakan, A. Karatas, Strain-specific and outcome-specific efficacy of probiotics for the treatment of irritable bowel syndrome: a systematic review and meta-analysis, E Clinical Medicine 41 (2021) 101154. https://doi.org/10.1016/j.eclinm.2021.101154.
Crossref Google Scholar
[25]

V. Subramaniyan, K. Gurumurthy, Diversity of probiotic adhesion genes in the gastrointestinal tract of goats, J. Cell Biochem. 120 (2019) 12422-12428. https://doi.org/10.1002/jcb.28508.
Crossref Google Scholar
[26]

I.C. Lee, G. Caggianiello, I.I.V. Swam et al., Strain-specific features of extracellular polysaccharides and their impact on Lactobacillus plantarum-host interactions, Appl. Environ. Microbiol. 82 (2016) 3959-3970. https://doi.org/10.1002/jcb.28508.
Crossref Google Scholar
[27]

S. Yan, B. Yang, J. Zhao, et al., A ropy exopolysaccharide producing strain Bifidobacterium longum subsp. longum YS108R alleviates DSS-induced colitis by maintenance of the mucosal barrier and gut microbiota modulation, Food Funct. 10 (2019) 1595-1608. https://doi.org/10.1039/c9fo00014c.
Crossref Google Scholar
[28]

D. Ohye, W. Murrell, Formation and structure of the spore of Bacillus coagulans, J. Cell Biol. 14 (1962) 111-123. https://doi.org/10.1083/jcb.14.1.111.
Crossref Google Scholar
[29]

W. Wang, Y. Li, X. Guo, A mouse model of Citrobacter rodentium oral infection and evaluation of innate and adaptive immune responses, STAR Protoc. 1 (2020) 100218. https://doi.org/10.1016/j.xpro.2020.100218.
Crossref Google Scholar
[30]

P.A. Maragkoudakis, G. Zoumpopoulou, C. Miaris, et al., Probiotic potential of Lactobacillus strains isolated from dairy products, Int. Dairy J. 16 (2006) 189-199. https://doi.org/10.1016/j.idairyj.2005.02.009.
Crossref Google Scholar
[31]

T.J. Kochan, M.J. Somers, A.M. Kaiser, et al., Intestinal calcium and bile salts facilitate germination of Clostridium difficile spores, PLoS Pathog. 13 (2017) 1006443. https://doi.org/10.1371/journal.ppat.1006443.
Crossref Google Scholar
[32]

B. Hyronimus, C.L. Marrec, A.H. Sassi, et al., Acid and bile tolerance of spore-forming lactic acid bacteria, Int. J. Food Microbiol. 61 (2000) 193-197. https://doi.org/10.1016/s0168-1605(00)00366-4.
Crossref Google Scholar
[33]

Q. Chen, Y. Ren, J. Lu, et al., A novel prebiotic blend product prevents irritable bowel syndrome in mice by improving gut microbiota and modulating immune response, Nutrients 9 (2017) 1341. https://doi.org/10.3390/nu9121341.
Crossref Google Scholar
[34]

Q. Pan, S. Cen, L. Yu, et al., Niche-Specific adaptive evolution of Lactobacillus plantarum strains isolated from human feces and paocai, Front. Cell Infect. Microbiol. 10 (2021) 804. https://doi.org/10.3389/fcimb.2020.615876.
Crossref Google Scholar
[35]

Y. Mu, Y. Cong, Bacillus coagulans and its applications in medicine, Benef. Microbes 10 (2019) 679-688. https://doi.org/10.3920/BM2019.0016.
Crossref Google Scholar
[36]

G. Konuray, Z. Erginkaya, Potential use of Bacillus coagulans in the food industry, Foods 7 (2018) 92. https://doi.org/10.3390/foods7060092.
Crossref Google Scholar
[37]

B. 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.
Crossref Google Scholar
[38]

X. Gao, Z. Wang, X. Li, et al., A new Lactobacillus gasseri strain HMV18 inhibits the growth of pathogenic bacteria, Food Sci. Hum. Wellness 11 (2022) 247-254. https://doi.org/10.1016/j.fshw.2021.11.010.
Crossref Google Scholar
[39]

S. Binda, C. Hill, E. Johansen, et al., Criteria to qualify microorganisms as “probiotic” in foods and dietary supplements, Front. Microbiol. 11 (2020) 1662. https://doi.org/10.3389/fmicb.2020.01662.
Crossref Google Scholar
[40]

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.
Crossref Google Scholar
[41]

V. Laroute, H. Tormo, C. Couderc, et al., From genome to phenotype: an integrative approach to evaluate the biodiversity of Lactococcus lactis, Microorganisms 5 (2017) 27. https://doi.org/10.3390/microorganisms5020027.
Crossref Google Scholar
[42]

J. Zhang, L. Song, Y. Wang, et al., Beneficial effect of butyrate-producing Lachnospiraceae on stress-induced visceral hypersensitivity in rats, J. Gastroenterol. Hepatol. 34 (2019) 1368-1376. https://doi.org/10.1111/jgh.14536.
Crossref Google Scholar
[43]

T. Pérez-Berezo, J. Pujo, P. Martin, et al., Identification of an analgesic lipopeptide produced by the probiotic Escherichia coli strain Nissle 1917, Nat. Commun. 8 (2017) 1-12. https://doi.org/10.1038/s41467-017-01403-9.
Crossref Google Scholar
[44]

J. Sun, X. Feng, C. Lyu, et al., Effects of different processing methods on the lipid composition of hazelnut oil: a lipidomics analysis, Food Sci. Hum. Wellness 11 (2022) 427-435. https://doi.org/10.1016/j.fshw.2021.11.024.
Crossref Google Scholar
[45]

I.M. Carroll, T. Ringel-Kulka, T.O. Keku, et al., Molecular analysis of the luminal-and mucosal-associated intestinal microbiota in diarrhea-predominant irritable bowel syndrome, Am. J. Physiol. Gastrointest. Liver. Physiol. 301 (2011) 799-807. https://doi.org/10.1152/ajpgi.00154.2011.
Crossref Google Scholar
[46]

B.D. Cash, Eluxadoline: a promising therapy that raises many questions, Transl. Gastroenterol. Hepatol. 1 (2016) 76. https://doi.org/10.21037/tgh.2016.09.06.
Crossref Google Scholar
[47]

M. Rajilić-Stojanović, E. Biagi, H.G.H.J. Heilig, et al., Global and deep molecular analysis of microbiota signatures in fecal samples from patients with irritable bowel syndrome, Gastroenterology 141 (2011) 1792-1801. https://doi.org/10.1053/j.gastro.2011.07.043.
Crossref Google Scholar
[48]

M. Bellini, D. Gambaccini, C. Stasi, et al., Irritable bowel syndrome: a disease still searching for pathogenesis, diagnosis and therapy, World J. Gastroenterol. 20 (2014) 8807-8820. https://doi.org/10.3748/wjg.v20.i27.8807.
Crossref Google Scholar
[49]

C. Binda, L.R. Lopetuso, G. Rizzatti, et al., Actinobacteria: a relevant minority for the maintenance of gut homeostasis, Dig. Liver Dis. 50 (2018) 421-428. https://doi.org/10.1016/j.dld.2018.02.012.
Crossref Google Scholar
[50]

P.A. Hughes, A.M. Harrington, J. Castro, et al., Sensory neuro-immune interactions differ between irritable bowel syndrome subtypes, Gut 62 (2013) 1456-1465. https://doi.org/10.1136/gutjnl-2011-301856.
Crossref Google Scholar
[51]

M. Schmulson, D. Pulido-London, O. Rodriguez, et al., Lower serum IL-10 is an independent predictor of IBS among volunteers in Mexico, Am. J. Gastroenterol. 107 (2012) 747-753. https://doi.org/10.1038/ajg.2011.484.
Crossref Google Scholar
[52]

E.K. Brint, J. MacSharry, A. Fanning, et al., Differential expression of toll-like receptors in patients with irritable bowel syndrome, Am. J. Gastroenterol. 106 (2011) 329-336. https://doi.org/10.1038/ajg.2010.438.
Crossref Google Scholar
[53]

A. Dlugosz, P. Nowak, M. D’Amato, et al., Increased serum levels of lipopolysaccharide and antiflagellin antibodies in patients with diarrhea-predominant irritable bowel syndrome, Neurogastroenterol. Motil. 27 (2015) 1747-1754. https://doi.org/10.1111/nmo.12670.
Crossref Google Scholar
[54]

L. Crouzet, E. Gaultier, C. Del’Homme, et al., The hypersensitivity to colonic distension of IBS patients can be transferred to rats through their fecal microbiota, Neurogastroenterol. Motil. 25 (2013) 272-282. https://doi.org/10.1111/nmo.12103.
Crossref Google Scholar
[55]

G. Barbara, V. Stanghellini, R.D. Giorgio, et al., Activated mast cells in proximity to colonic nerves correlate with abdominal pain in irritable bowel syndrome, Gastroenterology 126 (2004) 693-702. https://doi.org/10.1053/j.gastro.2003.11.055.
Crossref Google Scholar
[56]

N. Cenac, Protease-activated receptors as therapeutic targets in visceral pain, Curr. Neuropharmacol. 11 (2013) 598-605. https://doi.org/10.2174/1570159X113119990039.
Crossref Google Scholar
Food Science and Human Wellness
Volume 13 Issue 4,
July 2024
Pages 1845-1855
DOI: 10.26599/FSHW.2022.9250153
Cite this article:
Cao J, Yu L, Zhao J, et al. Alleviative effects of Bacillus coagulans strains on irritable bowel syndrome-unraveling strain specificity through physiological and genomic analysis. Food Science and Human Wellness, 2024, 13(4): 1845-1855. https://doi.org/10.26599/FSHW.2022.9250153

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Received: 31 July 2022
Revised: 07 October 2022
Accepted: 28 November 2022
Published: 20 May 2024
© 2024 Beijing Academy of Food Sciences. Publishing services by Tsinghua University Press.

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