Bacillus As Potential Probiotics: Status, Concerns, and Future Perspectives

Fouad M F Elshaghabee, Namita Rokana, Rohini D Gulhane, Chetan Sharma, Harsh Panwar, Fouad M F Elshaghabee, Namita Rokana, Rohini D Gulhane, Chetan Sharma, Harsh Panwar

Abstract

Spore-forming bacilli are being explored for the production and preservation of food for many centuries. The inherent ability of production of large number of secretory proteins, enzymes, antimicrobial compounds, vitamins, and carotenoids specifies the importance of bacilli in food chain. Additionally, Bacillus spp. are gaining interest in human health related functional food research coupled with their enhanced tolerance and survivability under hostile environment of gastrointestinal tract. Besides, bacilli are more stable during processing and storage of food and pharmaceutical preparations, making them more suitable candidate for health promoting formulations. Further, Bacillus strains also possess biotherapeutic potential which is connected with their ability to interact with the internal milieu of the host by producing variety of antimicrobial peptides and small extracellular effector molecules. Nonetheless, with proposed scientific evidences, commercial probiotic supplements, and functional foods comprising of Bacillus spp. had not gained much credential in general population, since the debate over probiotic vs pathogen tag of Bacillus in the research and production terrains is confusing consumers. Hence, it's important to clearly understand the phenotypic and genotypic characteristics of selective beneficial Bacillus spp. and their substantiation with those having GRAS status, to reach a consensus over the same. This review highlights the probiotic candidature of spore forming Bacillus spp. and presents an overview of the proposed health benefits, including application in food and pharmaceutical industry. Moreover, the growing need to evaluate the safety of individual Bacillus strains as well as species on a case by case basis and necessity of more profound analysis for the selection and identification of Bacillus probiotic candidates are also taken into consideration.

Keywords: Bacillus; beneficial microbes; human health; intestinal microbiota; mechanism of action; probiotics; spore formers.

Figures

FIGURE 1
FIGURE 1
Pubmed trends for key words “Bacillus+ probiotic” and “Lactobacillus + probiotic” for last 25 years.
FIGURE 2
FIGURE 2
Taxonomy of genus Bacillus (Source: Bergey’s manual of systematic bacteriology: volume 3: The Firmicutes).
FIGURE 3
FIGURE 3
Phylogenetic relationships of 46 Bacillus species. The bar represents the unit length of the number of nucleotide substitutions per site (adopted from Xu and Cote, 2003).
FIGURE 4
FIGURE 4
Different possible mechanisms of health benefits of spore forming Bacillus probiotics (SFBP). Daily intake of SFBP is resulted in increased their colonization in gut resulting in increased number of beneficial microbial population and decreased number of pathogenic strains. Moreover, SFBP could proliferate different immune cell for production of anti-inflammatory cytokines to maintain immune homeostasis. DC, Dendritic cells, Treg, regulatory T cells, Th, T helper cell, IL, interleukin, IFNγ, interferon γ, TNFα, tumor necrosis factor α.

References

    1. Abdhul K., Ganesh M., Shanmughapriya S., Vanithamani S., Kanagavel M., Anbarasu K., et al. (2015). Bacteriocinogenic potential of a probiotic strain Bacillus coagulans [BDU3] from Ngari. Int. J. Biol. Macromol. 79 800–806. 10.1016/j.ijbiomac.2015.06.005
    1. Abhari K., Shekarforoush S. S., Hosseinzadeh S., Nazifi S., Sajedianfard J., Eskandari M. H. (2016). The effects of orally administered Bacillus coagulans and inulin on prevention and progression of rheumatoid arthritis in rats. Food Nutr. Res. 60:30876 10.3402/fnr.v60.30876
    1. Adami A., Cavazzoni V. (1999). Occurrence of selected bacterial groups in the faeces of piglets fed with Bacillus coagulans as probiotic. J. Basic Microbiol. 39 3–10. 10.1002/(SICI)1521-4028(199903)39:1<3::AID-JOBM3>;2-O
    1. Adewumi G. A., Oguntoyinbo F. A., Romi W., Singh T. A., Jeyaram K. (2014). Genome subtyping of autochthonous Bacillus species isolated from Iru, a fermented Parkia biglobosa seed. Food Biotechnol. 28 250–268. 10.1080/08905436.2014.931866
    1. Alkaya B., Laleman I., Keceli S., Ozcelik O., CenkHaytac M., Teughels W. (2016). Clinical effects of probiotics containing Bacillus species on gingivitis: a pilot randomized controlled trial. J. Periodontal. Res. 52 497–504. 10.1111/jre.12415
    1. Alou M. T., Rathored J., Khelaifia S., Michelle C., Brah S., Diallo B. A., et al. (2015). Bacillus rubiinfantis sp. nov. strain mt2T, a new bacterial species isolated from human gut. New Microbes New Infect. 8 51–60. 10.1016/j.nmni.2015.09.008
    1. Altmeyer S., Kröger S., Vahjen W., Zentek J., Scharek-Tedin L. (2014). Impact of a probiotic Bacillus cereus strain on the jejunal epithelial barrier and on the NKG2D expressing immune cells during the weaning phase of piglets. Vet. Immunol. Immunopathol. 161 57–65. 10.1016/j.vetimm.2014.07.001
    1. Angmo K., Kumari A., Bhalla T. C. (2016). Probiotic characterization of lactic acid bacteria isolated from fermented foods and beverage of Ladakh. LWT Food Sci. Technol. 66 428–435. 10.1016/j.lwt.2015.10.057
    1. Ash C., Farrow J. A. E., Wallbanks S., Collins M. D. (1991). Phylogenetic heterogeneity of the genus Bacillus revealed by comparative analysis of small-subunit-ribosomal RNA sequences. Lett. Appl. Microbiol. 13 202–206. 10.1111/j.1472-765X
    1. Bader J., Albin A., Stahl U. (2012). Spore-forming bacteria and their utilisation as probiotics. Benef. Microbes 3 67–75. 10.3920/BM2011.0039
    1. Beaumont M. (2002). Flavouring composition prepared by fermentation with Bacillus spp. Int. J. Food Microbiol. 75 189–196. 10.1016/S0168-1605(01)00706-1
    1. Berthold-Pluta A., Pluta A., Garbowska M. (2015). The effect of selected factors on the survival of Bacillus cereus in the human gastrointestinal tract. Microb. Pathog. 82 7–14. 10.1016/j.micpath.2015.03.015
    1. Bohm M. E., Huptas C., Krey V. M., Scherer S. (2015). Massive horizontal gene transfer, strictly vertical inheritance and ancient duplications differentially shape the evolution of Bacillus cereus enterotoxin operons hbl, cytK and nhe. BMC Evol. Biol. 15:246 10.1186/s12862-015-0529-4
    1. Butel M. J. (2014). Probiotics, gut microbiota and health. Med. Mal. Infect. 44 1–8. 10.1016/j.medmal.2013.10.002
    1. Cai D., Liu M., Wei X., Li X., Wang Q., Nomura C. T., et al. (2017). Use of Bacillus amyloliquefaciens HZ-12 for high-level production of the blood glucose lowering compound, 1-deoxynojirimycin (DNJ), and nutraceutical enriched soybeans via fermentation. Appl. Biochem. Biotechnol. 181 1108–1122. 10.1007/s12010-016-2272-8
    1. Casula G., Cutting S. M. (2002). Bacillus probiotics: spore germination in the gastrointestinal tract. Appl. Environ. Microbiol. 68 2344–2352. 10.1128/AEM.68.5.2344-2352.2002
    1. Chantawannakul P., Oncharoen A., Klanbut K., Chukeatirote E., Lumyong S. (2002). Characterization of proteases of Bacillus subtilis strain 38 isolated from traditionally fermented soybean in northern Thailand. Sci. Asia 28 241–245. 10.2306/scienceasia1513-1874.2002.28.241
    1. Choi J. H., Pichiah P. B. T., Kim M. J., Cha Y. S. (2016). Cheonggukjang, a soybean paste fermented with B. licheniformis 67 prevents weight gain and improves glycemic control in high fat diet induced obese mice. J. Clin. Biochem. Nutr. 59 31–38. 10.3164/jcbn.15-30
    1. Cutting S. M. (2011). Bacillus probiotics. Food Microbiol. 28 214–220. 10.1016/j.fm.2010.03.007
    1. Di Caro S., Tao H., Grillo A., Franceschi F., Elia C., Zocco M. A., et al. (2005). Bacillus clausii effect on gene expression pattern in small bowel mucosa using DNA microarray analysis. Eur. J. Gastroenterol. Hepatol. 17 951–960. 10.1097/00042737-200509000-00011
    1. Doron S., Snydman D. R. (2015). Risk and safety of probiotics. Clin. Infect. Dis. 60 S129–S134. 10.1093/cid/civ085
    1. Drago L., Rodighiero V., Celeste T., Rovetto L., De Vecchi E. (2013). Microbiological evaluation of commercial probiotic products available in the United States in 2009. J. Chemother. 22 373–377. 10.1179/joc.2010.22.6.373
    1. Duc L. H., Hong H. A., Barbosa T. M., Henriques A. O., Cutting S. M. (2004). Characterization of Bacillus probiotics available for human use. Appl. Environ. Microbiol. 70 2161–2171. 10.1128/AEM.70.4.2161-2171.2004
    1. Dudonné S., Varin T. V., Anhê F. F., Dubé P., Roy D., Pilon G., et al. (2015). Modulatory effects of a cranberry extract co-supplementation with Bacillus subtilis CU1 probiotic on phenolic compounds bioavailability and gut microbiota composition in high-fat diet-fed mice. Pharma Nutr. 3 89–100. 10.1016/j.phanu.2015.04.002
    1. Earl A. M., Eppinger M., Fricke W. F., Rosovitz M. J., Rasko D. A., Daugherty S., et al. (2012). Whole-genome sequences of Bacillus subtilis and close relatives. J. Bacteriol. 194 2378–2379. 10.1128/JB.05675-11
    1. Ellekilde M., Selfjord E., Larsen C. S., Jakesevic M., Rune I., Tranberg B., et al. (2014). Transfer of gut microbiota from lean and obese mice to antibiotic-treated mice. Sci. Rep. 4:5922 10.1038/srep05922
    1. Endres J. R., Clewell A., Jade K. A., Farber T., Hauswirth J., Schauss A. G. (2009). Safety assessment of a proprietary preparation of a novel probiotic, Bacillus coagulans, as a food ingredient. Food Chem. Toxicol. 47 1231–1238. 10.1016/j.fct.2009.02.018
    1. Fakhry S., Sorrentini I., Ricaa E., De Felice M., Baccigalupi L. (2008). Characterization of spore forming Bacilli isolated from the human gastrointestinal tract. J. Appl. Microbiol. 105 2178–2186. 10.1111/j.1365-2672.2008.03934.x
    1. Fan B., Blom J., Klenk H. P., Borriss R. (2017). Bacillus amyloliquefaciens, Bacillus velezensis and Bacillus siamensis form an operational group B. amyloliquefaciens within the B. subtilis species complex. Front. Microbiol. 8:22 10.3389/fmicb.2017.00022
    1. FAO/WHO (2001). Health and Nutritional Properties of Probiotics in Food Including Powder Milk With Live Lactic Acid Bacteria. Report of a joint FAO/WHO expert consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria Rome: Food and Agriculture Organization.
    1. FAO/WHO (2002). Guidelines for the Evaluation of Probiotics in Food. Food and Agriculture Organization of the United Nations and World Health Organization Working Group Report. Rome: Food and Agriculture Organization.
    1. Foligné B., Peys E., Vandenkerckhove J., Van Hemel J., Dewulf J., Breton J., et al. (2012). Spores from two distinct colony types of the strain Bacillus subtilis PB6 substantiate anti-inflammatory probiotic effects in mice. Clin. Nutr. 31 987–994. 10.1016/j.clnu.2012.05.016
    1. Fujiya M., Musch M. W., Nakagawa Y., Hu S., Alverdy J., Kohgo Y., et al. (2007). The Bacillus subtilis quorum-sensing molecule CSF contributes to intestinal homeostasis via OCTN2, a host cell membrane transporter. Cell Host Microbe 1 299–308. 10.1016/j.chom.2007.05.004
    1. Ghani M., Ansari A., Aman A., Zohra R. R., Siddiqui N. N., Qader S. A. U. (2013). Isolation and characterization of different strains of Bacillus licheniformis for the production of commercially significant enzymes. Pak. J. Pharm. Sci. 26 691–697.
    1. Ghelardi E., Celandroni F., Salvetti S., Gueye S. A., Lupetti A., Senesi S. (2015). Survival and persistence of Bacillus clausii in the human gastrointestinal tract following oral administration as spore-based probiotic formulation. J. Appl. Microbiol. 119 552–559. 10.1111/jam.12848
    1. Ghoneim M. A. M., Hassan A. I., Mahmoud M. G., Asker M. S. (2016). Effect of polysaccharide from Bacillus subtilis sp. on cardiovascular diseases and atherogenic indices in diabetic rats. BMC Complement. Altern. Med. 16:112 10.1186/s12906-016-1093-1
    1. Gobi N., Malaikozhundan B., Sekar V., Shanthi S., Vaseeharan B., Jayakumar R., et al. (2016). GFP tagged Vibrio parahaemolyticus Dahv2 infection and the protective effects of the probiotic Bacillus licheniformis Dahb1 on the growth, immune and antioxidant responses in Pangasius hypophthalmus. Fish Shellfish Immunol. 52 230–238. 10.1016/j.fsi.2016.03.006
    1. Green D. H., Wakeley P. R., Page A., Barnes A., Baccigalupi L., Ricca E., et al. (1999). Characterization of two bacillus probiotics. Appl. Environ. Microbiol. 65 4288–4291.
    1. Guo Z., Liu X. M., Zhang Q. X., Shen Z., Tian F. W., Zhang H., et al. (2013). Influence of consumption of probiotics on the plasma lipid profile: a meta-analysis of randomized controlled trials. Nutr. Metab. Cardiovasc. Dis. 21 844–850. 10.1016/j.numecd.2011.04.008
    1. Haldar L., Gandhi D. N. (2016). Effect of oral administration of Bacillus coagulans B37 and Bacillus pumilus B9 strains on fecal coliforms, Lactobacillus and Bacillus spp. in rat animal model. Vet. World 9 766 10.14202/vetworld.2016.766-772
    1. Hoffman T., Troup P., Szabo A., Hungerer C., Jahn D. (1995). The anaerobic life of Bacillus subtilis: cloning of the genes encoding the respiratory nitrate reductase system. FEMS Microbiol. Lett. 131 219–225. 10.1111/j.1574-6968.1995.tb07780.x
    1. Hong H. A., Duc le H., Cutting S. M. (2005). The use of bacterial spore formers as probiotics. FEMS Microbiol. Rev. 29 813–835. 10.1016/j.femsre.2004.12.001
    1. Hong H. A., Huang J. M., Khaneja R., Hiep L. V., Urdaci M. C., Cutting S. M. (2008). The safety of Bacillus subtilis and Bacillus indicus as food probiotics. J. Appl. Microbiol. 105 510–520. 10.1111/j.1365-2672.2008.03773.x
    1. Hong H. A., Khaneja R., Tam N. M. K., Cazzato A., Tan S., Urdaci M., et al. (2009). Bacillus subtilis isolated from the human gastrointestinal tract. Res. Microbiol. 160 134–143. 10.1016/j.resmic.2008.11.002
    1. Horosheva T. V., Vodyanoy V., Sorokulova I. (2014). Efficacy of Bacillus probiotics in prevention of antibiotic-associated diarrhoea: a randomized, double-blind, placebo-controlled clinical trial. JMM Case Rep. 1 1–6. 10.1099/jmmcr.0.004036
    1. Hosoi T., Kiuchi K. (2003). “Natto – a food made by fermenting cooked soybeans with Bacillus subtilis (natto),” in Handbook of Fermented Functional Foods ed. Farnworth E. R. (Boca Raton, FL: CRC Press; ) 227–245.
    1. Hoyles L., Honda H., Logan N. A., Halket G., La Ragione R. M., McCartney A. L. (2012). Recognition of greater diversity of Bacillus species and related bacteria in human faeces. Res. Microbiol. 163 3–13. 10.1016/j.resmic.2011.10.004
    1. Hyronimus B., Le Marrec C., Sassi A. H., Deschamps A. (2000). Acid and bile tolerance of spore-forming lactic acid bacteria. Int. J. Food Microbiol. 61 193–197. 10.1016/S0168-1605(00)00366-4
    1. Inatsu Y., Nakamura N., Yuriko Y., Fushimi T., Watanasiritum L., Kawamoto S. (2006). Characterization of Bacillus subtilis strains in Thuanao, a traditional fermented soybean food in northern Thailand. Lett. Appl. Microbiol. 43 237–242. 10.1111/j.1472-765X.2006.01966.x
    1. Jager R., Shields K. A., Lowery R. P., De Souza E. O., Partl J. M., Hollmer C., et al. (2016). Probiotic Bacillus coagulans GBI-30, 6086 reduces exercise-induced muscle damage and increases recovery. Peer J. 4:e2276 10.7717/peerj.2276
    1. Jeong H., Park S. H., Choi S. K. (2016). Draft genome sequences of four plant probiotic Bacillus strains. Genome Announc. 4:e00358–16. 10.1128/genomeA.00358-16
    1. Joseph B., Dhas B., Hena V., Raj J. (2013). Bacteriocin from Bacillus subtilis as a novel drug against diabetic foot ulcer bacterial pathogens. Asian Pac. J. Trop. Biomed. 3 942–946. 10.1016/S2221-1691(13)60183-5
    1. Kalliomäki M., Salminen S., Arvilommi H., Kero P., Koskinen P., Isolauri E. (2001). Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet 357 1076–1079. 10.1016/S0140-6736(00)04259-8
    1. Karu R., Sumeri I. (2016). Survival of Lactobacillus rhamnosus GG during simulated gastrointestinal conditions depending on food matrix. J. Food Res. 5 57–66. 10.5539/jfr.v5n5p56
    1. Khochamit N., Siripornadulsil S., Sukon P., Siripornadulsil W. (2015). Antibacterial activity and genotypic–phenotypic characteristics of bacteriocin-producing Bacillus subtilis KKU213: potential as a probiotic strain. Microbiol. Res. 170 36–50. 10.1016/j.micres.2014.09.004
    1. Khodadad A., Farahmand F., Najafi M., Shoaran M. (2013). Probiotics for the treatment of pediatric Helicobacter pylori infection: a randomized double blind clinical trial. Iran J. Pediatr. 23 79–84.
    1. Kniehl E., Becker A., Forster D. H. (2003). Pseudo-outbreak of toxigenic Bacillus cereus isolated from stools of three patients with diarrhoea after oral administration of a probiotic medication. J. Hosp. Infect. 55 33–38. 10.1016/S0195-6701(03)00133-6
    1. Kolsto A. B., Tourasse N. J., Okstad O. A. (2009). What sets Bacillus anthracis apart from other Bacillus species. Annu. Rev. Microbiol. 63 451–476. 10.1146/annurev.micro.091208.073255
    1. Kosak T., Maeda T., Nakada Y., Yukawa M., Tanaka S. (1998). Effect of Bacillus subtilis spore administration on activation of macrophages and natural killer cells in mice. Vet. Microbiol. 60 215–225. 10.1016/S0378-1135(97)00102-8
    1. Kotb E. (2015). Purification and partial characterization of serine fibrinolytic enzyme from Bacillus megaterium KSK-07 isolated from kishk, a traditional Egyptian fermented food. Appl. Biochem. Microbiol. 51 34–43. 10.1134/S000368381501007X
    1. Kramer J. M., Gilbert R. J. (1989). “Bacillus cereus and other Bacillus species,” in Foodborne Bacterial Pathogens ed. Doyle M. P. (Boca Raton, FL: CRC Press; ) 21–70.
    1. Krawczyk A. O., de Jong A., Holsappel S., Eijlander R. T., van Heel A., Berendsen E. M., et al. (2016). Genome sequences of 12 spore-forming Bacillus species, comprising Bacillus coagulans, Bacillus licheniformis, Bacillus amyloliquefaciens, Bacillus sporothermodurans, and Bacillus vallismortis, isolated from foods. Genome Announc. 4 103–116. 10.1128/genomeA.00103-16
    1. Lee J. H., Nam S. H., Seo W. T., Yun H. D., Hong S. Y., Kim M. K., et al. (2012). The production of surfactin during the fermentation of cheonggukjang by potential probiotic Bacillus subtilis CSY191 and the resultant growth suppression of MCF-7 human breast cancer cells. Food Chem. 131 1347–1354. 10.1016/j.foodchem.2011.09.133
    1. Lee Y., Yoshitsugu R., Kikuchi K., Joe G. H., Tsuji M., Nose T., et al. (2016). 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. 116 603–610. 10.1017/S0007114516002270
    1. Lefevre M., Racedo S. M., Ripert G., Housez B., Cazaubiel M., Maudet C. P., et al. (2015). Probiotic strain Bacillus subtilis CU1 stimulates immune system of elderly during common infectious disease period: a randomized, double-blind placebo-controlled study. Immun. Ageing 12 24 10.1186/s12979-015-0051-y
    1. Li J., Xu Y., Jin L., Li X. (2015). Effects of a probiotic mixture (Bacillus subtilis YB-1 and Bacillus cereus YB-2) on disease resistance and non-specific immunity of sea cucumber, Apostichopus japonicus (Selenka). Aquac. Res. 46 3008–3019. 10.1111/are.12453
    1. London L. E., Kumar A. H., Wall R., Casey P. G., O’Sullivan O., Shanahan F., et al. (2014). Exopolysaccharide-producing probiotic Lactobacilli reduce serum cholesterol and modify enteric microbiota in ApoE-deficient mice. J. Nutr. 144 1956–1962. 10.3945/jn.114.191627
    1. Lopetuso L. R., Scaldaferri F., Franceschi F., Gasbarrini A. (2016). Bacillus clausii and gut homeostasis: state of the art and future perspectives. Expert Rev. Gastroenterol. Hepatol. 10 943–948. 10.1080/17474124
    1. Majeed M., Majeed S., Nagabhushanam K., Natarajan S., Sivakumar A., Ali F. (2016). Evaluation of the stability of Bacillus coagulans MTCC 5856 during processing and storage of functional foods. Int. J. Food Sci. Technol. 51 894–901. 10.1111/ijfs.13044
    1. Mallappa R. H., Rokana N., Duary R. K., Panwar H., Batish V. K., Grover S. (2012). Management of metabolic syndrome through probiotic and prebiotic interventions. Indian J. Endocrinol. Metab. 16 20–27. 10.4103/2230-8210.91178
    1. Maneerat S., Lehtinen M. J., Childs C. E., Forssten S. D., Alhoniemi E., Tiphaine M., et al. (2014). Consumption of Bifidobacterium lactis Bi-07 by healthy elderly adults enhances phagocytic activity of monocytes and granulocytes. J. Nutr. Sci. 44 1–10. 10.1017/jns.2013.31
    1. Manhar A. K., Bashir Y., Saikia D., Nath D., Gupta K., Konwar B. K., et al. (2016). Cellulolytic potential of probiotic Bacillus Subtilis AMS6 isolated from traditional fermented soybean (Churpi): An in-vitro study with regards to application as an animal feed additive. Microbiol. Res. 186 62–70. 10.1016/j.micres.2016.03.004
    1. Mohammed Y., Lee B., Kang Z., Du G. (2014). Development of a two-step cultivation strategy for the production of vitamin B12 by Bacillus megaterium. Microb. Cell Fact. 13 102 10.1186/s12934-014-0102-7
    1. Mullany P., Barbosa T. M., Scott K., Roberts A. P. (2004). “Mechanisms of gene transfer and the spread of antibiotic resistance in spore forming organisms in the GI tract,” in Bacterial Spore Formers: Probiotics and Emerging Applications eds Ricca E., Henriques A. O., Cutting S. M. (Norfolk: Horizon Bioscience; ) 113–129.
    1. Muscettola M., Grasso G., Blach-Olszewska Z., Migliaccio P., Borghesi-Nicoletti C., Giarratan M., et al. (1992). Effects of Bacillus subtilis spores on interferon production. Pharmacol. Res. 26 176–177. 10.1016/1043-6618(92)90652-R
    1. Muscettola M., Grasso G., Migliaccio P., Gallo V. C. (1991). Plasma interferon-like activity in rabbits after oral administration of Bacillus subtilis spores. J. Chemother. 3 130–132.
    1. Nagal S., Okimura K., Kaizawa N., Ohki K., Kanatomo S. (1996). Study on surfactin, a cyclic depsipeptide II synthesis of surfactin B2 produced by Bacillus natto KMD 2311. Chem. Phar. Bull. (Tokyo). 44 5–10. 10.1248/cpb.44.5
    1. Nyangale E. P., Farmer S., Cash K., Chernoff D., Gibson G. R. (2015). Bacillus coagulans GBI-30 6086 modulates Faecalibacterium prausnitziiin older men and women. J. Nutr. 145 1446–1452. 10.3945/jn.114.199802
    1. Nyangale E. P., Farmer S., Keller D., Chernoff D., Gibson G. R. (2014). Effect of prebiotics on the fecal microbiota of elderly volunteers after dietary supplementation of Bacillus coagulans GBI-30, 6086. Anaerobe 30 75–81. 10.1016/j.anaerobe.2014.09.002
    1. Ouattara H. G., Reverchon S., Niamke S. L., Nasser W. (2017). Regulation of the synthesis of pulp degrading enzymes in Bacillus isolated from cocoa fermentation. Food Microbiol. 63 255–262. 10.1016/j.fm.2016.12.004
    1. Ozawa K., Yagu-Uchi K., Yamanaka K., Yamashita Y., Ueba K., Miwatani T. (1979). Bacillus natto and Streptococcus faecalis on growth of Candida albicans. Microbiol. Immunol. 23 1147–1156. 10.1111/j.1348-0421.1979.tb00547.x
    1. Panwar H., Calderwood D., Grant I. R., Grover S., Green B. D. (2014). Lactobacillus strains isolated from infant faeces possess potent inhibitory activity against intestinal alpha-and beta-glucosidases suggesting anti-diabetic potential. Eur. J. Nutr. 53 1465–1474. 10.1007/s00394-013-0649-9
    1. Panwar H., Calderwood D., Grant I. R., Grover S., Green B. D. (2016). Lactobacilli possess inhibitory activity against dipeptidyl peptidase-4 (DPP-4). Ann. Microbiol. 66 505–509. 10.1007/s13213-015-1129-7
    1. Pinchuk I. V., Bressollier P., Verneuil B., Fenet B., Sorokulova I. B., Megraud F., et al. (2001). In vitro Anti-Helicobacter pylori Activity of the probiotic strain Bacillus subtilis 3 is due to secretion of antibiotics. Antimicrob. Agents Chemother. 45 3156–3161. 10.1128/AAC.45.11.3156-3161.2001
    1. Prokesova L., Novakova M., Julak J., Mara M. (1994). Effect of Bacillus firmus and other sporulating aerobic microorganisms on in vitro stimulation of human lymphocytes. A comparative study. Folia Microbiol. 39 501–504. 10.1007/BF02814071
    1. Ramarao N., Lereclus D. (2006). Adhesion and cytotoxicity of Bacillus cereus and Bacillus thuringiensis to epithelial cells are FlhA and PlcR dependent, respectively. Microbes Infect. 8 1483–1491. 10.1016/j.micinf.2006.01.005
    1. Rani R. P., Anandharaj M., Hema S., Deepika R., Ravindran A. D. (2016). Purification of antilisterial aeptide (Subtilosin A) from novel Bacillus tequilensis FR9 and demonstrate their pathogen invasion protection ability using human carcinoma cell line. Front. Microbiol. 7:1910 10.3389/fmicb.2016.01910
    1. Ranji P., Akbarzadeh A., Rahmati-Yamchi M. (2015). Associations of probiotics with vitamin D and leptin receptors and their effects on colon cancer. Asian Pac. J. Cancer Prev. 16 3621–3627. 10.7314/APJCP.2015
    1. Rao K. P., Chennappa G., Suraj U., Nagaraja H., Raj A. C., Sreenivasa M. Y. (2015). Probiotic potential of Lactobacillus strains isolated from sorghum-based traditional fermented food. Probiotics Antimicrob. Proteins 7 146–156. 10.1007/s12602-015-9186-6
    1. Redman M. G., Ward E. J., Phillips R. S. (2014). The efficacy and safety of probiotics in people with cancer: a systematic review. Ann. Oncol. 25 1919–1929. 10.1093/annonc/mdu106
    1. Rey M. W., Ramaiya P., Nelson B. A., Brody-Karpin S. D., Zaretsky E. J., Tang M., et al. (2004). Complete genome sequence of the industrial bacterium Bacillus licheniformis and comparisons with closely related Bacillus species. Genome Biol. 5:77 10.1186/gb-2004-5-10-r77
    1. Ripert G., Racedo S. M., Elie A. M., Jacquot C., Bressollier P., Urdaci M. C. (2016). 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. 60 3445–3454. 10.1128/AAC.02815-15
    1. Rowan N. J., Deans K., Anderson J. G., Gemmell C. G., Hunter I. S., Chaithong T. (2001). Putative virulence factor expression by clinical and food isolates of Bacillus spp. after growth in reconstituted infant milk formulae. Appl. Environ. Microbiol. 67 3873–3881. 10.1128/AEM.67.9.3873-3881.2001
    1. Sah B. N. P., Vasiljevic T., McKechnie S., Donkor O. N. (2014). Effect of probiotics on antioxidant and antimutagenic activities of crude peptide extract from yogurt. Food Chem. 156 264–270. 10.1016/j.foodchem.2014.01.105
    1. Sanchez B., Arias S., Chaignepain S., Denayrolles M., Schmitter J. M., Bressollier P., et al. (2009). Identification of surface proteins involved in the adhesion of a probiotic Bacillus cereus strain to mucin and fibronectin. Microbiology 155 1708–1716. 10.1099/mic.0.025288-0
    1. SCAN (1999). Opinion of of the Scientific Steering Committee on Antimicrobial Resistance. European Commission, Health and Consumer Protection Directorate-General. (SCAN) Scientific Committee on Animal Nutrition. Available at:
    1. SCAN (2002). Opinion of the Scientific Committee on Animal Nutrition (SCAN) on the use of Bacillus licheniformis NCTC 13123 in Feeding Stuffs for Pigs (product AlCare). European Commission, Health and Consumer Protection Directorate-General. (SCAN) Scientific Committee on Animal Nutrition. Available at:
    1. SCAN (2003). Opinion of the Scientific Committee on Animal Nutrition, on the Criteria for Assessing the Safety of Microorganisms Resistant to Antibiotics of Human Clinical and Veterinary Importance. European Commission, Health and Consumer Protection Directorate-General. (SCAN) Scientific Committee on Animal Nutrition. Available at:
    1. Schierack P., Wieler L. H., Taras D., Herwig V., Tachu B., Hlinak A., et al. (2007). Bacillus cereus var. toyoi enhanced systemic immune response in piglets. Vet. Immunol. Immunopathol. 118 1–11. 10.1016/j.vetimm.2007.03.006
    1. Scott K. P., Antoine J. M., Midtvedt T., van Hemert S. (2015). Manipulating the gut microbiota to maintain health and treat disease. Microb. Ecol. Health Dis. 26 25877 10.3402/mehd.v26.25877
    1. Senesi S., Celandroni F., Tavanti A., Ghelardi E. (2001). Molecular characterization and identification of Bacillus clausii strains marketed for use in oral bacteriotherapy. Appl. Environ. Microbiol. 67 834–839. 10.1128/AEM.67.2.834-839.200
    1. Shida K., Nomoto K. (2013). Probiotics as efficient immuno potentiators: translational role in cancer prevention. Indian J. Med. Res. 138 808–814.
    1. Shimizu K., Ogura H., Asahara T., Nomoto K., Morotomi M., Tasaki O., et al. (2013). Probiotic/synbiotic therapy for treating critically ill patients from a gut microbiota perspective. Dig. Dis. Sci. 58 23–32. 10.1007/s10620-012-2334-x
    1. Shobharani P., Padmaja R. J., Halami P. M. (2015). Diversity in the antibacterial potential of probiotic cultures Bacillus licheniformis MCC2514 and Bacillus licheniformis MCC2512. Res. Microbiol. 166 546–554. 10.1016/j.resmic.2015.06.003
    1. Sorokulova I. B., Pinchuk I. V., Denayrolles M., Osipova I. G., Huang J. M., Cutting S., et al. (2008). The safety of two Bacillus probiotic strains for human use. Dig. Dis. Sci. 53 954–963. 10.1007/s10620-007-9959-1
    1. Stein T. (2005). Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol. Microbiol. 56 845–857. 10.1111/j.1365-2958.2005.04587.x
    1. Sudha R. M., Bhonagiri S. (2012). Efficacy of Bacillus coagulans strain Unique IS-2 in the treatment of patients with acute diarrhea. Int. J. Probiotics Prebiotics 7 33–37.
    1. Takano H. (2016). The regulatory mechanism underlying light-inducible production of carotenoids in non phototrophic bacteria. Biosci. Biotechnol. Biochem. 80 1264–1273. 10.1080/09168451.2016.1156478
    1. Tam N. K., Uyen N. Q., Hong H. A., Duc L. H., Hoa T. T., Serra C. R., et al. (2006). The intestinal life cycle of Bacillus subtilis and close relatives. J. Bacteriol. 188 2692–2700. 10.1128/JB.188.7.2692-2700.2006
    1. Tamang J. P., Watanabe K., Holzapfel W. H. (2016). Review: diversity of microorganisms in global fermented foods and beverages. Front. Microbiol. 7:377 10.3389/fmicb.2016.00377
    1. Tanaka K., Takanaka S., Yoshida K. I. (2014). A second-generation Bacillus cell factory for rare inositol production. Bioengineered 5 331–334. 10.4161/bioe.29897
    1. Taras D., Vahjen W., Macha M., Simon O. (2005). Response of performance characteristics and fecal consistency to long-lasting dietary supplementation with the probiotic strain Bacillus cereus var. toyoi to sows and piglets. Arch. Anim. Nutr. 59 405–417. 10.1080/17450390500353168
    1. Terlabie N. N., Sakyi-Dawson E., Amoa-Awua W. K. (2006). The comparative ability of four isolates of Bacillus subtilis to ferment soybeans into dawadawa. Int. J. Food Microbiol. 106 145–152. 10.1016/j.ijfoodmicro.2005.05.021
    1. Tewari V. V., Dubey S. K., Gupta G. (2015). Bacillus clausii for prevention of late-onset sepsis in preterm infants: a randomized controlled trial. J. Trop. Pediatr. 61 377–385. 10.1093/tropej/fmv050
    1. Thakur N., Rokana N., Panwar H. (2016). Probiotics: selection criteria, safety and role in health and disease. J. Innov. Biol. 3 259–270.
    1. Trocino A., Xiccato G., Carraro L., Jimenez G. (2005). Effect of diet supplementation with Toyocerin® (Bacillus cereus var. toyoi) on performance and health of growing rabbits. World Rabbit Sci. 13 17–28.
    1. Urgesi R., Casale C., Pistelli R., Rapaccini G. L., De Vitis I. (2014). 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.
    1. Von Mollendorff J. W., Vaz-Velho M., Todorov S. D. (2016). “Boza, a traditional cereal-based fermented beverage: a rich source of probiotics and bacteriocin-producing lactic acid bacteria,” in Functional Properties of Traditional Foods eds Kristbergsson K., Ötles S. (Boston, MA: Springer; ) 157–188.
    1. Wang J., Tang H., Zhang C., Zhao Y., Derrien M., Rocher E., et al. (2015). Modulation of gut microbiota during probiotic-mediated attenuation of metabolic syndrome in high fat diet-fed mice. ISME J. 9 1–15. 10.1038/ismej.2014.99
    1. Weese J. S., Martin H. (2011). Assessment of commercial probiotic bacterial contents and label accuracy. Can. Vet. J. 52 43.
    1. Xu D., Cote J. C. (2003). Phylogenetic relationships between Bacillus species and related genera inferred from comparison of 3′ end 16S rDNA and 5′ end 16S–23S ITS nucleotide sequences. Int. J. Syst. Evol. Microbiol. 53 695–704. 10.1099/ijs.0.02346-0
    1. Yang H. J., Kwon D. Y., Kim H. J., Kim M. J., Jung D. Y., Kang H. J., et al. (2014). Fermenting soybeans with Bacillus licheniformis potentiates their capacity to improve cognitive function and glucose homeostaisis in diabetic rats with experimental Alzheimer’s type dementia. Eur. J. Nutr. 54 77–88. 10.1007/s00394-014-0687-y
    1. Yang O. O., Kelesidis T., Cordova R., Khanlou H. (2014). Immunomodulation of antiretroviral drug-suppressed chronic HIV-1 infection in an oral probiotic double-blind placebo-controlled trial. AIDS Res. Hum. Retroviruses 30 988–995. 10.1089/aid.2014.0181
    1. Zhang H. L., Li W. S., Xu D. N., Zheng W. W., Liu Y., Chen J., et al. (2016). Mucosa-reparing and microbiota-balancing therapeutic effect of Bacillus subtilis alleviates dextrate sulfate sodium-induced ulcerative colitis in mice. Exp. Ther. Med. 12 2554–2562. 10.3892/etm.2016.3686
    1. Zhao C., Lv X., Fu J., He C., Hua H., Yan Z. (2016). In vitro inhibitory activity of probiotic products against oral Candida species. J. Appl. Microbiol. 121 254–262. 10.1111/jam.13138
    1. Zheng L. P., Zou T., Ma Y. J., Wang J. W., Zhang Y. Q. (2016). Antioxidant and DNA damage arotecting Activity of exopolysaccharides from the endophytic bacterium Bacillus Cereus SZ1. Molecules 21:174 10.3390/molecules21020174
    1. Zhu K., Hölzel C. S., Cui Y., Mayer R., Wang Y., Dietrich R., et al. (2016). Probiotic Bacillus cereus strains, a potential risk for public health in China. Front. Microbiol. 7:718 10.3389/fmicb.2016.00718
    1. Zouari R., Abdallah-Kolsi R. B., Hamden K., Feki A. E., Chaabouni K., Makni-Ayadi F., et al. (2015). Assessment of the antidiabetic and antilipidemic properties of Bacillus subtilis SPB1 biosurfactant in alloxan-induced diabetic rats. Pept. Sci. 104 764–774. 10.1002/bip.22705

Source: PubMed

Sponsoren und Mitarbeiter

Krankheiten

Drogeninterventionen

3
Abonnieren