Mechanistic Insight into the Role of Peptides Secreted from Bacillus clausii
and Future Opportunities

Jyoti      Guleria; Minhaj   Ahmad   Khan

doi:10.2174/0127724328273252240201071756

Abstract

Bacillus clausii is a commercial spore probiotic known to treat multiple diseases. An increased interest in exploring the nutraceutical and probiotic properties of various microorganisms has made researchers explore more about these bacteria. The current trends in the healthcare industry are majorly focused on devising new therapies to avoid drug and pathogen resistance in patients. Antimicrobial peptides have been considered a source of antibiotics for a long time. Still, getting new therapies into the market is a big challenge. Members of the genus Bacillus have been reported to have a broad spectrum of antimicrobial peptides. One of the least explored species under this genus is Bacillus clausii, concerning peptide drug therapy. The applications of Bacillus clausii in treating or preventing gut dysbiosis and respiratory infections have been largely supported in the past two decades. Yet research is lacking in explaining the pathways at molecular levels in targeting pathogens. In this mini-review, we are going to summarise the research that has been reported so far about peptide extraction from Bacillus clausii, their mode of action and advantages to mankind, and the challenges lying in the isolation of peptides.

Keywords: Antimicrobial peptides, antibiotics, Bacillus clausii, drug resistance, lanthipeptides, drug therapy.

« Previous Next »

Graphical Abstract

[1]
Sumi CD, Yang BW, Yeo IC, Hahm YT. Antimicrobial peptides of the genus Bacillus: A new era for antibiotics. Can J Microbiol  2015; 61(2): 93-103.
 [http://dx.doi.org/10.1139/cjm-2014-0613] [PMID:  25629960]

[2]
Cryan JF, O’Riordan KJ, Cowan CSM, et al. The microbiota-gut-brain axis. Physiol Rev  2019; 99(4): 1877-2013.
 [http://dx.doi.org/10.1152/physrev.00018.2018] [PMID:  31460832]

[3]
Li Y, Xia S, Jiang X, et al. Gut microbiota and diarrhea: An updated review. Front Cell Infect Microbiol  2021; 11: 625210.www.frontiersin.org
 [http://dx.doi.org/10.3389/fcimb.2021.625210] [PMID:  33937093]

[4]
Freitas AR, Werner G. Nosocomial pathogens and antimicrobial resistance: Modern challenges and future opportunities. Microorganisms  2023; 11(7): 1685.
 [http://dx.doi.org/10.3390/microorganisms11071685] [PMID:  37512858]

[5]
Abbrescia A, Palese LL, Papa S, Gaballo A, Alifano P, Sardanelli A. Antibiotic sensitivity of Bacillus clausii strains in commercial preparation. Clin Immunol Endocr Metab Drugs  2015; 1(2): 102-10.
 [http://dx.doi.org/10.2174/2212707002666150128195631]

[6]
Patel C, Patel P, Acharya S. Therapeutic perspective of a spore-forming probiotic-Bacillus clausii UBBC07 against acetaminophen-induced uremia in rats. Probiotics Antimicrob Proteins  2020; 12(1): 253-8.
 [http://dx.doi.org/10.1007/s12602-019-09540-x] [PMID:  30879230]

[7]
Joo HS, Chang CS. Oxidant and SDS-stable alkaline protease from a halo-tolerant Bacillus clausii I-52: Enhanced production and simple purification. J Appl Microbiol  2005; 98(2): 491-7.
 [http://dx.doi.org/10.1111/j.1365-2672.2004.02464.x] [PMID:  15659203]

[8]
Gálvez-Gamboa GT, Sánchez-Servín MR, Parra-Cota F, et al. Pesticides in Mexican agriculture and promissory alternatives for their replacement. Biológico Agropecuaria Tuxpan  2018; 7(11): 1977-91.

[9]
Wenzel M, Rautenbach M, Vosloo JA, et al. The multifaceted antibacterial mechanisms of the pioneering peptide antibiotics tyrocidine and gramicidin S. MBio  2018; 9(5): e00802-18.
 [http://dx.doi.org/10.1128/mBio.00802-18] [PMID:  30301848]

[10]
Binda E, Marinelli F, Marcone G. Old and new glycopeptide antibiotics: Action and Resistance. Antibiotics   2014; 3(4): 572-94.
 [http://dx.doi.org/10.3390/antibiotics3040572] [PMID:  27025757]

[11]
Chung The H, Le SNH. Dynamic of the human gut microbiome under infectious diarrhea. Curr Opin Microbiol  2022; 66(66): 79-85.
 [http://dx.doi.org/10.1016/j.mib.2022.01.006] [PMID:  35121284]

[12]
Valles-Colomer M, Falony G, Darzi Y, et al. The neuroactive potential of the human gut microbiota in quality of life and depression. Nat Microbiol  2019; 4(4): 623-32.
 [http://dx.doi.org/10.1038/s41564-018-0337-x] [PMID:  30718848]

[13]
Troeger C, Forouzanfar M, Rao PC, et al. Estimates of global, regional, and national morbidity, mortality, and aetiologies of diarrhoeal diseases: A systematic analysis for the Global Burden of Disease Study. Lancet Infect Dis  2015; 2017(3099): 1-40.

[14]
Sinchana B, Shreekrishna G, Christi D. International journal of
contemporary pediatrics  2018; 5(4): 1646-50.

[15]
Loris R. Bacillus clausii and gut homeostasis: state of the art and future perspectives. Expert Rev Gastroenterol Hepatol  2016; 10(8): 943-8.
 [http://dx.doi.org/10.1080/17474124.2016.1200465]

[16]
Collado MC, Meriluoto J, Salminen S. Role of commercial probiotic strains against human pathogen adhesion to intestinal mucus. Lett Appl Microbiol  2007; 45(4): 454-60.
 [http://dx.doi.org/10.1111/j.1472-765X.2007.02212.x] [PMID:  17897389]

[17]
Ghelardi E, Abreu AT, Marzet CB, Calatayud G, Perez M III, Castro AP. Current progress and future perspectives on the use of bacillus clausii. Microorganisms  2022; 10(6): 1246.
 [http://dx.doi.org/10.3390/microorganisms10061246] [PMID:  35744764]

[18]
Ahire JJ, Kashikar MS, Madempudi RS. Survival and germination of Bacillus clausii ubbc07 spores in in vitro human gastrointestinal tract simulation model and evaluation of clausin production. Front Microbiol  2020; 11: 1010.www.frontiersin.org
 [http://dx.doi.org/10.3389/fmicb.2020.01010] [PMID:  32733389]

[19]
Saroj DB, Ahire JJ, Shukla R. Genetic and phenotypic assessments for the safety of probiotic. Bacillus clausii 088AE. 3 Biotech   2023; 13(7): 238.
 [http://dx.doi.org/10.1007/s13205-023-03662-4]

[20]
Benfield AH, Henriques ST. Mode-of-action of antimicrobial peptides: membrane disruption vs. intracellular mechanisms. Frontiers in Medical Technology  2020; 2: 610997.
 [http://dx.doi.org/10.3389/fmedt.2020.610997] [PMID:  35047892]

[21]
Wingfield P. Protein precipitation using ammonium sulfate. Curr Protoc Protein Sci  1998; 13(1): 3F.
 [http://dx.doi.org/10.1002/0471140864.psa03fs13] [PMID:  18429073]

[22]
Valenzuela RV, Gamboa GTG, Rodríguez EDV, et al. Lipopeptides produced by biological control agents of the genus Bacillus: a review of analytical tools used for their study. Revista Mexicana
Ciencias Agrícolas  2020; 11(2): 419-32.

[23]
Jamshidi-Aidji M, Dimkić I, Ristivojević P, et al. Effect-directed screening of Bacillus lipopeptide extracts via hyphenated high-performance thin-layer chromatography. J Chromatogr A  2019; 1605: 460366.

[24]
Malviya R, Bansal V, Pal OP, et al. High-performance liquid chromatography: A short review. J Glob Pharma Technol  2010; 2(5): 22-6.

[25]
Kong J, Yu S. Fourier transform infrared spectroscopic analysis of protein secondary structures. Acta Biochim Biophys Sin  2007; 39(8): 549-59.
 [http://dx.doi.org/10.1111/j.1745-7270.2007.00320.x] [PMID:  17687489]

[26]
Sahl HG, Bierbaum G. Lantibiotics: Biosynthesis and biological activities of uniquely modified peptides from gram-positive bacteria. Annu Rev Microbiol  1998; 52(1): 41-79.
 [http://dx.doi.org/10.1146/annurev.micro.52.1.41] [PMID:  9891793]

[27]
Rochín-Medina JJ, Ramírez-Medina HK, Rangel-Peraza JG, Pineda-Hidalgo KV, Iribe-Arellano P. Use of whey as a culture medium for Bacillus clausii for the production of protein hydrolysates with antimicrobial and antioxidant activity. Food Sci Technol Int  2018; 24(1): 35-42.
 [http://dx.doi.org/10.1177/1082013217724705] [PMID:  28816527]

[28]
Reyes M, Figueroa H, Melgar L. Production of calcium- and iron-binding peptides by probiotic strains of Bacillus subtilis, B. clausii and B. coagulans GBI-30. Revista Mexicana de Ingeniería Química  2015; 1-9.

[29]
Bukola AT, Gboyega E. Production and characterization of bioflocculants produced by Bacillus clausii NB2. Innov Romanian. Food Biotechnol  2014; (14): 13-25.

[30]
Ramírez K, Pineda-Hidalgo KV, Rochín-Medina JJ. Fermentation of spent coffee grounds by Bacillus clausii induces release of potentially bioactive peptides. Lebensm Wiss Technol  2021; 138: 110685.
 [http://dx.doi.org/10.1016/j.lwt.2020.110685]

[31]
Tsutomu S, Hiroaki Y, Shoji K, et al. Identification of novel sesterterpene/triterpene synthase from Bacillus clausii. Chembiochem  2013; 14(7): 822-5.

[32]
Yenuganti1 VR, Yadala1 R, et al. In vitro evaluation of anticancer effects of different probiotic strains on HCT-116 cell line.  J Appl Microbiol  2021; 131(4): 1958-69.
 [http://dx.doi.org/10.1111/jam.15060]

[33]
Jahani-Sherafat S, Alebouyeh M, Moghim S, Amoli H, Ghasemian-Safaei H. Role of gut microbiota in the pathogenesis of colorectal cancer; a review article. Gastroenterol Hepatol Bed Bench  2018; 11(2): 101-9.
 [PMID:  29910850]

[34]
Mouloud G, Daoud H, Bassem J, Atef I, Hani B. New bacteriocin from Bacillus clausii strainGM17: purification, characterization, and biological activity. Appl Biochem Biotechnol  2013; 171(8): 2186-200.
 [http://dx.doi.org/10.1007/s12010-013-0489-3] [PMID:  24037515]

[35]
Nighat F, Mushtaq Z, Maqsood M, Shahid M, Hanif MA, Jamil A. Cytotoxic, α-amylase inhibitory and thrombolytic activities of organic and aqueous extracts of Bacillus clausii KP10. Pak J Pharm Sci  2020; 33(1): 135-9.
 [http://dx.doi.org/10.36721/PJPS.2020.33.1.REG.135-139.1] [PMID:  32122841]

[36]
Paparo L, Tripodi L, Bruno C, et al. Protective action of Bacillus clausii probiotic strains in an in vitro model of Rotavirus infection. Sci Rep  2020; 10(1): 12636.
 [http://dx.doi.org/10.1038/s41598-020-69533-7] [PMID:  32724066]

[37]
Ahmed B. Specific interactions of clausin, a new lanthipeptide, with lipid precursors of the bacterial cell wall. Biophysical Journal  2009; 97: 1390-7.
 [http://dx.doi.org/10.1016/j.bpj.2009.06.029]

[38]
Ripert G, Racedo SM, Elie AM, Jacquot C, Bressollier P, Urdaci MC. Secreted compounds of the probiotic Bacillus clausii strain O/C inhibit the cytotoxic effects induced by Clostridium difficile and Bacillus cereus toxins. Antimicrob Agents Chemother  2016; 60(6): 3445-54.
 [http://dx.doi.org/10.1128/AAC.02815-15] [PMID:  27001810]

[39]
Biniarz P, Łukaszewicz M, Janek T. Screening concepts, characterization and structural analysis of microbial-derived bioactive lipopeptides: A review. Crit Rev Biotechnol  2017; 37(3): 393-410.
 [http://dx.doi.org/10.3109/07388551.2016.1163324] [PMID:  27098391]

[40]
Khokhlova E, Colom J, Simon A, et al. Immunomodulatory and antioxidant properties of a novel potential probiotic bacillus clausii CSI08. Microorganisms  2023; 11(2): 240.
 [http://dx.doi.org/10.3390/microorganisms11020240] [PMID:  36838205]

[41]
Zhao X, Kuipers OP. Identification and classification of known and putative antimicrobial compounds produced by a wide variety of Bacillales species. BMC Genomics  2016; 17(1): 882.
 [http://dx.doi.org/10.1186/s12864-016-3224-y] [PMID:  27821051]

[42]
Krishnappa L, Dreisbach A, Otto A, et al. Extracytoplasmic proteases determining the cleavage and release of secreted proteins, lipoproteins, and membrane proteins in Bacillus subtilis. J Proteome Res  2013; 12(9): 4101-10.
 [http://dx.doi.org/10.1021/pr400433h] [PMID:  23937099]

[43]
Roland P, Roman G, Michal B. On the physiology and pathophysiology of antimicrobial peptides. Mol Med  2009; 15(1-2): 51-9.
 [http://dx.doi.org/10.2119/molmed.2008.00087]

[44]
Field D, Cotter PD, Hill C, Ross RP. Bioengineering lantibiotics for therapeutic success. Front Microbiol  2015; 6: 1363.
 [http://dx.doi.org/10.3389/fmicb.2015.01363] [PMID:  26640466]

[45]
Wimley WC. Describing the mechanism of antimicrobial peptide action with the interfacial activity model. ACS Chem Biol  2010; 5(10): 905-17.
 [http://dx.doi.org/10.1021/cb1001558] [PMID:  20698568]

[46]
Henriques ST, Costa J, Castanho MARB. Re‐evaluating the role of strongly charged sequences in amphipathic cell‐penetrating peptides. FEBS Lett  2005; 579(20): 4498-502.
 [http://dx.doi.org/10.1016/j.febslet.2005.06.085] [PMID:  16083883]

[47]
Davies AH, Roberts AK, Shone CC, Acharya KR. Super toxins from a super bug: Structure and function of Clostridium difficile toxins. Biochem J  2011; 436(3): 517-26.
 [http://dx.doi.org/10.1042/BJ20110106] [PMID:  21615333]

[48]
Freire JM, Gaspar D, de la Torre BG, Veiga AS, Andreu D, Castanho MARB. Monitoring antibacterial permeabilization in real time using time-resolved flow cytometry. Biochim Biophys Acta Biomembr  2015; 1848(2): 554-60.
 [http://dx.doi.org/10.1016/j.bbamem.2014.11.001] [PMID:  25445678]

[49]
Sanz Y, De Palma G. Gut microbiota and probiotics in modulation of epithelium and gut-associated lymphoid tissue function. Int Rev Immunol  2009; 28(6): 397-413.
 [http://dx.doi.org/10.3109/08830180903215613] [PMID:  19954356]

[50]
Repka LM, Chekan JR, Nair SK, van der Donk WA. Mechanistic understanding of lanthipeptide biosynthetic enzymes. Chem Rev  2017; 117(8): 5457-520.
 [http://dx.doi.org/10.1021/acs.chemrev.6b00591] [PMID:  28135077]

[51]
Epand RM, Epand RF. Bacterial membrane lipids in the action of antimicrobial agents. J Pept Sci  2011; 17(5): 298-305.
 [http://dx.doi.org/10.1002/psc.1319] [PMID:  21480436]

[52]
Maturana P, Martinez M, Noguera ME, et al. Lipid selectivity in novel antimicrobial peptides: Implication on antimicrobial and hemolytic activity. Colloids Surf B Biointerfaces  2017; 153: 152-9.
 [http://dx.doi.org/10.1016/j.colsurfb.2017.02.003] [PMID:  28236791]

[53]
van Heijenoort J. Recent advances in the formation of the bacterial peptidoglycan monomer unit. Nat Prod Rep  2001; 18: 503-19.
 [http://dx.doi.org/10.1039/a804532a]

[54]
Akash K, Rabi B. Quantitative and qualitative characterization of a commercially available oral suspension of probiotic products containing. Bacillus clausii spores Kharwar et al. BMC Microbiology  2022; 22: 217.
 [http://dx.doi.org/10.1186/s12866-022-02631-w]

[55]
Hatta M, Supriatmo MA, et al. Comparison of zinc-probiotic combination therapy to zinc therapy alone in reducing the severity of acute diarrhea. Paediatr Indones  2011; 51(1): 1-6.

[56]
Hodges K, Gill R. Infectious diarrhea Cellular and molecular mechanisms. Gut Microbes  2010; 4-21.
 [http://dx.doi.org/10.4161/gmic.1.1.11036]

[57]
Lahiri KR, Singh R, Apte M, et al. Efficacy and safety of Bacillus clausii (O/C, N/R, SIN, T) probiotic combined with oral rehydration therapy (ORT) and zinc in acute diarrhea in children: A randomized, double-blind, placebo-controlled study in India. Trop Dis Travel Med Vaccines  2022; 8(1): 9.
 [http://dx.doi.org/10.1186/s40794-022-00166-6] [PMID:  35397572]

[58]
Chen Q, Wang P, Wang J, et al. Zinc laurate protects against intestinal barrier dysfunction and inflammation induced by ETEC in a mice model. Nutrients  2022; 15(1): 54.
 [http://dx.doi.org/10.3390/nu15010054] [PMID:  36615713]

[59]
Elshaghabee FMF, Rokana N, Gulhane RD, Sharma C, Panwar H. Bacillus as potential probiotics: Status, concerns, and future perspectives. Front Microbiol  2017; 8: 1490.
 [http://dx.doi.org/10.3389/fmicb.2017.01490] [PMID:  28848511]

[60]
Özkoç M, Can B, Şentürk H, Dönmez D, Kanbak G. Possible curative effects of boric acid and bacillus clausii treatments on TNBS-induced ulcerative colitis in rats. Biol Trace Elem Res  2023; 201(3): 1237-51.
 [http://dx.doi.org/10.1007/s12011-022-03215-5] [PMID:  35349007]

[61]
Kabeer S, Mushtaq Z. Synergistic and antagonistic effects on antimicrobial properties of organic and aqueous extracts of Bacillus clausii KP10 in combination with conventional antibiotics. J Animal Plant Sci  2023; 33(1): 149-58.
 [http://dx.doi.org/10.36899/JAPS.2023.1.0603]

[62]
Ramlucken U, Ramchuran SO, Moonsamy G, van Rensburg C, Thantsha MS, Lalloo R. Production and stability of a multi-strain Bacillus based probiotic product for commercial use in poultry. Biotechnol Rep  2021; 29: e00575.
 [http://dx.doi.org/10.1016/j.btre.2020.e00575] [PMID:  33659192]

[63]
Enciso-Huerta HA, Ruiz-Cabrera MA, Lopez-Martinez LA, Gonzalez-Garcia R, Martinez-Gutierrez F, Saavedra-Leos MZ. Evaluation of two active system encapsulant matrices with quercetin and bacillus clausii for functional foods. Polymers  2022; 14(23): 5225.
 [http://dx.doi.org/10.3390/polym14235225] [PMID:  36501619]

[64]
Vázquez-Maldonado D, Espinosa-Solis V, Leyva-Porras C, et al. Preparation of spray-dried functional food: Effect of adding bacillus clausii bacteria as a co-microencapsulating agent on the conservation of resveratrol. Processes  2020; 8(7): 849.
 [http://dx.doi.org/10.3390/pr8070849]

[65]
Shayestehpour M, Rahimi MR, Piroozmand A, Khaledi A, Fateminasab ZS. In vitro evaluation of antiviral activity effect of selenium, Bacillus clausii supernatant, and their combination on the replication of herpes simplex virus 1. Jundishapur J Microbiol  2022; 15(8): e129848.
 [http://dx.doi.org/10.5812/jjm-129848]

[66]
Jaleel A, Hiba AM, Abbas R. Biosynthesis of selenium nanoparticles using probiotic Bacillus clausii and their antibacterial efficacy against multidrug-resistant bacteria. J Pharmaceut Negative Results  2022; 13(7): 1011-9.

[67]
Abbasi-Hosseini SM, Eftekhar F, Yakhchali B, et al. Cloning and enhanced expression of an extracellular alkaline protease from a soil isolate of Bacillus clausii in Bacillus subtilis. Iran J Biotechnol  2011; 9(4)

[68]
Cheng Z, Yanfen X, Yanhe M, et al. Ma1 Characterization and high-efficiency secreted expression in Bacillus subtilis of a thermo- alkaline β-mannanase from an alkaliphilic Bacillus clausii strain S10 Zhou et al. Microb Cell Fact  2018; 17: 124.
 [http://dx.doi.org/10.1186/s12934-018-0973-0]

[69]
Díaz-Madriz JP, Zavaleta-Monestel E, Rojas-Chinchilla C, et al. Bacteremia following alkalihalobacillus clausii (formerly bacillus clausii) administration in immunosuppressed adults: A case series. Bacteria  2023; 2(4): 185-95.
 [http://dx.doi.org/10.3390/bacteria2040014]

[70]
Dunlap CA, Bowman MJ, Rooney AP. Iturinic lipopeptide diversity in the bacillus subtilis species group important anti-fungals for plant disease biocontrol applications. Front Microbiol  2019; 10: 1794.
 [http://dx.doi.org/10.3389/fmicb.2019.01794] [PMID:  31440222]

[71]
Marseglia GL, Tosca M, Cirillo I, et al. Efficacy of Bacillus clausii spores in the prevention of recurrent respiratory infections in children: a pilot study. Ther Clin Risk Manag  2007; 3(1): 13-7.
 [http://dx.doi.org/10.2147/tcrm.2007.3.1.13] [PMID:  18360611]

[72]
Tabandeh F, Moghaddam HR, Yakhchali B, Shariati P, Mousavian MT, Ghasemi F. Fed-batch fermentation of bacillus clausii for efficient production of alkaline protease using different feeding strategies. Chem Eng Commun  2011; 198(9): 1063-74.
 [http://dx.doi.org/10.1080/00986445.2011.552024]

[73]
Sonia S, Francesco C, Arianna T, et al. Molecular characterization and identification of bacillus clausii strains marketed for use in oral bacteriotherapy. Applied And Environmental Microbiology  2001; 834-9.
 [http://dx.doi.org/10.1128/AEM.67.2.834-839.2001]

Rights & Permissions Print Cite

Article Metrics

19

2

Journal Information

For Authors

For Editors

For Reviewers

Explore Articles

Open Access

Open Access Articles

For Visitors

DOI https://dx.doi.org/10.2174/0127724328273252240201071756	Print ISSN 2772-4328
Publisher Name Bentham Science Publisher	Online ISSN 2772-4336

Current Reviews in Clinical and Experimental Pharmacology

Mechanistic Insight into the Role of Peptides Secreted from Bacillus clausii and Future Opportunities

Abstract

Graphical Abstract

Related Journals

Related Books