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Recent Advances in the Physiology of Spore Formation for Bacillus Probiotic Production

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Abstract

Spore-forming probiotic bacteria have received a wide and constantly increasing scientific and commercial interest. Among them, Bacillus species are the most studied and well-characterized Gram-positive bacteria. The use of bacilli as probiotic products is expanding especially rapidly due to their inherent ability to form endospores with unique survivability and tolerance to extreme environments and to produce a large number of valuable metabolites coupled with their bio-therapeutic potential demonstrating immune stimulation, antimicrobial activities and competitive exclusion. Ease of Bacillus spp. production and stability during processing and storage make them a suitable candidate for commercial manufacture of novel foods or dietary supplements for human and animal feeds for livestock, especially in the poultry and aquaculture industries. Therefore, the development of low-cost and competitive technologies for the production of spore-forming probiotic bacteria through understanding physiological peculiarities and mechanisms determining the growth and spore production by Bacillus spp. became necessary. This review summarizes the recent literature and our own data on the physiology of bacilli growth and spore production in the submerged and solid-state fermentation conditions, focusing on the common characteristics and unique properties of individual bacteria as well as on several approaches providing enhanced spore formation.

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References

  1. Mingmongkolchai S, Panbangred W (2018) Bacillus probiotics: an alternative to antibiotics for livestock production. J Appl Microbiol 124:1334–1346

    Article  CAS  PubMed  Google Scholar 

  2. Gilchrist MJ, Greko C, Wallinga DB, Beran GW, Riley DG, Thorne PS (2007) The potential role of concentrated animal feeding operations in infectious disease epidemics and antibiotic resistance. Environ Health Perspect 115:313–316

    Article  PubMed  Google Scholar 

  3. Flint JF, Garner MR (2009) Feeding beneficial bacteria: a natural solution for increasing efficiency and decreasing pathogens in animal agriculture. J Appl Poult Res 18:367–378

    Article  Google Scholar 

  4. Tuohy KM, Pinart-Gilberga M, Jones M, Hoyles L, McCartney AL, Gibson GR (2007) Survivability of a probiotic Lactobacillus casei in the gastrointestinal tract of healthy human volunteers and its impact on the faecal microflora. J Appl Microbiol 102:1026–1032

    CAS  PubMed  Google Scholar 

  5. Brashears MM, Amezquita A, Jaroni D (2005) Lactic acid bacteria and their uses in animal feeding to improve food safety. Adv Food Nutr Res 50:1–31

    Article  CAS  PubMed  Google Scholar 

  6. Giacchi V, Sciacca P, Betta P (2016) Multistrain probiotics: the present forward the future. In: Watson RR, Preedy VR (eds) Probiotics, prebiotics, and synbiotics. Elsevier, pp 279–302

  7. Krehbiel CR, Rust SR, Zhang G, Gilliland SE (2003) Bacterial direct-fed microbials in ruminant diets: performance response and mode of action. J Anim Sci 81:120–132

    Google Scholar 

  8. Soccol CR, Vandenberghe LPS, Spier MR, Medeiros ABP, Yamaguishi CT, Lindner JD, Pandey A, Thomaz-Soccol V (2010) The potential of probiotics. Food Technol Biotechnol 48:413–434

    CAS  Google Scholar 

  9. FAO/WHO (2002) Guidelines for the evaluation of probiotics in food. In: Food and Agriculture Organization of the United Nations and World Health Organization Working Group Report. Food and Agriculture Organization, Rome

    Google Scholar 

  10. Cutting SM (2011) Bacillus probiotics. Food Microbiol 28:214–220

    Article  PubMed  Google Scholar 

  11. Elshaghabee FMF, Rokana N, Gulhane RD, Sharma C, Panwar H (2017) Bacillus as potential probiotics: status, concerns, and future perspectives. Front Microbiol 8:1490

    Article  PubMed  PubMed Central  Google Scholar 

  12. Gaggìa F, Mattarelli P, Biavati B (2010) Probiotics and prebiotics in animal feeding for safe food production. Int J Food Microbiol 141:S15–S28

    Article  PubMed  Google Scholar 

  13. Market Research Report (2018) Probiotics market size, share & trends analysis report by application (food & beverages, dietary supplements, animal feed), by end-use, by region, and segment forecast, 2018–2024. http://www.grandviewresearch.com/industry-analysis/probiotics-market

  14. Aureli P, Capurso L, Castellazzi AM, Clerici M, Giovannini M, Morelli L, Poli A, Pregliasco F, Salvini F, Zuccott GV (2011) Probiotics and health: an evidence-based review. Pharmacol Res 63:366–376

    Article  CAS  PubMed  Google Scholar 

  15. Lee SH, Ingale SL, Kim JS, Kim KH, Lokhande A, Kim EK, Kwon IK, Kim YH, Chae BJ (2014) Effects of dietary supplementation with Bacillus subtilis LS1–2 fermentation biomass on growth performance, nutrient digestibility, cecal microbiota and intestinal morphology of weanling pig. Animal Feed Sci Technol 188:102–110

    Article  CAS  Google Scholar 

  16. Molnár AK, Podmaniczky B, Kürti P, Tenk I, Glávits R, Virág GI, Szabó ZS (2011) Effect of different concentrations of Bacillus subtilis on growth performance, carcase quality, gut microflora and immune response of broiler chickens. Br Poult Sci 52:658–665

    Article  CAS  PubMed  Google Scholar 

  17. Sanders ME, Morelli L, Tompkins TA (2003) Sporeformers as human probiotics: Bacillus, Sporolactobacillus, and Brevibacillus. Compr Rev Food Sci Food Saf 2:101–110

    Article  Google Scholar 

  18. Musa HH, Wu SL, Zhu CH, Seri HI, Zhu GQ (2009) The potential benefits of probiotics in animal production and health. J Anim Vet Adv 8:313–321

    Google Scholar 

  19. Foligne B, Daniel C, Pot B (2013) Probiotics from research to market: the possibilities, risks and challenges. Curr Opin Microbiol 16:284–292

    Article  PubMed  Google Scholar 

  20. Das S, Mondal K, Haque S (2017) A review on application of probiotic, prebiotic and synbiotic for sustainable development of aquaculture. J Entomol Zool Studies 5:422–429

    Google Scholar 

  21. Soccol CR, Prado MRM, Garcia LMB, Rodrigues C, Medeiros ABP, Soccol VT (2014) Current developments in probiotics. J Microb Biochem Technol 7:011–020

    Google Scholar 

  22. Zoumpopoulou G, Kazou M, Alexandraki V, Angelopoulou A, Papadimitriou K, Pot B, Tsakalidou E (2018) Probiotics and prebiotics: an overview on recent trends. In: Di Gioia D, Biavati B (eds) Probiotics and prebiotics in animal health and food safety. Springer, Cham, pp 1–34

  23. Fuller R (1989) Probiotics in man and animals. J Appl Bacteriol 66:365–378

    Article  CAS  PubMed  Google Scholar 

  24. Lam KL, Cheung PCK (2013) Non-digestible long chain beta-glucans as novel prebiotics. Bioact Carbohydr Diet Fibre 2:45–64

    Article  CAS  Google Scholar 

  25. Jose N, Bunt C, Hussain M (2015) Comparison of microbiological and probiotic characteristics of Lactobacilli isolates from dairy food products and animal rumen contents. Microorganisms 3:198–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Hoa NT, Baccigalupi L, Huxham A, Smertenko A, Van PH, Ammendola S, Ricca E, Cutting SM (2000) Characterization of Bacillus species used for oral bacteriotherapy and bacterioprophylaxis of gastrointestinal disorders. Appl Environ Microbiol 66:5241–5251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Cartman ST, La Ragione RM (2004) Spore probotics as animal feed supplements. In: Ricca E, Henriques AO, Cutting SM (Eds) Bacterial spores: probiotics and emerging applications. Horizon Scientific Press, London, pp 155–161

  28. Senesi S (2004) Bacillus spores as probiotics products for human use. In: Ricca E, Henriques AO, Cutting SM (eds) Bacterial spores: probiotics and emerging applications. Horizon Scientific Press, London, pp 132–141

    Google Scholar 

  29. Setlow P, Johnson EA (2007) Spores and their significance. Curr Opin Microbiol 6:550–556

    Article  CAS  Google Scholar 

  30. Hageman JH, Shankweiller GW, Wall PR, Franish K, McCowan G, Cauble SM, Grajeda J, Quinones C (1984) Single, chemically defined sporulation medium for Bacillus subtilis: growth, sporulation and extracellular protease production. J Bacteriol 160:438–441

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Sonenshein AL (2000) Control of sporulation initiation in Bacillus subtilis. Curr Opin Microbiol 3:561–566

    Article  CAS  PubMed  Google Scholar 

  32. Monteiro SMS, Clemente JJ, Henriques AO, Gomes RJ, Carrondo MJT, Cunha AE (2005) A procedure for high-yield spore production by Bacillus subtilis. Biotechnol Prog 21:1026–1031

    Article  CAS  PubMed  Google Scholar 

  33. Tavares M, Souza R, Luiz W, Cavalcante RM, Casaroli C, Martins E, Ferreira RC, Ferreira LS (2013) Bacillus subtilis endospores at high purity and recovery yields: optimization of growth conditions and purification method. Curr Microbiol 66:279–285

    Article  CAS  PubMed  Google Scholar 

  34. Turnbull PCB, Kramer J, Melling J (1990) Bacillus. In: Topley WWC, Wilson GS (eds) Topley and Wilson’s principles of bacteriology, virology and immunity, 8th ed., vol. 2. Edward Arnold, London, United Kingdom, pp 188–210

  35. Barbosa TM, Serra CR, La Ragione RM, Woodward MJ, Henriques AO (2005) Screening for Bacillus isolates in the broiler gastrointestinal tract. Appl Environ Microbiol 71:968–978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Samanya M, Yamauchi K (2002) Histological alterations of intestinal villi in chickens fed dried Bacillus subtilis var. natto. Comp Biochem Phys A 133:95–104

    Article  Google Scholar 

  37. Chen KL, Kho WL, You SH, Yeh RH, Tang SW, Hsieh CW (2009) Effects of Bacillus subtilis var. natto and Saccharomyces cerevisiae mixed fermented feed on the enhanced growth performance of broilers. Poult Sci 88:309–315

    Article  CAS  PubMed  Google Scholar 

  38. Ghani M, Ansari A, Aman A, Zohra RR, Siddiqui NN, Qader SAU (2013) Isolation and characterization of different strains of Bacillus licheniformis for the production of commercially significant enzymes. Pak J Pharm Sci 26:691–697

    CAS  PubMed  Google Scholar 

  39. van Dijl JM, Hecker M (2013) Bacillus subtilis: from soil bacterium to super-secreting cell factory. Microb Cell Factories 12:3

    Article  CAS  Google Scholar 

  40. Prajapati VS, Trivedi UB, Patel KC (2015) A statistical approach for the production of thermostable and alkalophilic alpha-amylase from Bacillus amyloliquefaciens KCP2 under solid-state fermentation. 3 Biotech 5:211–220

    Article  PubMed  Google Scholar 

  41. Siu-Rodas Y, de los Angeles Calixto-Romo M, Guillén-Navarro K, Sánchez JE, Zamora-Briseño JA, Amaya-Delgado L (2018) Bacillus subtilis with endocellulase and exocellulase activities isolated in the thermophilic phase from composting with coffee residues. Rev Argent Microbiol 50:234–243

    PubMed  Google Scholar 

  42. Tanaka K, Takanaka S, Yoshida KI (2014) A second-generation Bacillus cell factory for rare inositol production. Bioengineered 5:331–334

    Article  PubMed  PubMed Central  Google Scholar 

  43. Jeong H, Kim J, Choi SK, Pan JG (2018) Genome sequence of the probiotic strain Bacillus velezensis variant polyfermenticus GF423. Microbiol Resour Announc 7:e01000–e01018

    PubMed  PubMed Central  Google Scholar 

  44. Hosoi T, Kiuchi K (2003) Natto – a food made by fermenting cooked soybeans with Bacillus subtilis (natto). In: Farnworth ER (ed) Handbook of fermented functional foods. CRC Press, Boca Raton, FL, pp 227–245

    Google Scholar 

  45. Yu GY, Sinclair JB, Hartman GL, Bertagnolli BL (2002) Production of iturin a by Bacillus amyloliquefaciens suppressing Rhizoctonia solani. Soil Biol Biochem 34:955–963

    Article  CAS  Google Scholar 

  46. Chiou AL, Wu WS (2001) Isolation, identification and evaluation of bacterial antagonists against Botrytis elliptica on lily. J Phytopathol 149:319–321

    Article  Google Scholar 

  47. Tzeng YM, Rao YK, Tsay KJ, Wu WS (2008) Effect of cultivation conditions on spore production from Bacillus amyloliquefaciens B128 and its antagonism to Botrytis elliptica. J Appl Microbiol 104:1275–1282

    Article  PubMed  Google Scholar 

  48. Larsen N, Thorsen L, Kpikpi EN, Stuer-Lauridsen B, Cantor MD, Nielsen B, Brockmann E, Derkx PMF, Jespersen L (2014) Characterization of Bacillus spp. strains for use as probiotic additives in pig feed. Appl Microbiol Biotechnol 98:1105–1118

    Article  CAS  PubMed  Google Scholar 

  49. Thirabunyanon M, Thongwittaya N (2012) Protection activity of a novel probiotic strain of Bacillus subtilis against Salmonella Enteritidis infection. Res Vet Sci 93:74–81

    Article  CAS  PubMed  Google Scholar 

  50. 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

    Article  CAS  PubMed  Google Scholar 

  51. Leser TD, Knarreborg A, Worm J (2007) Germination and outgrowth of Bacillus subtilis and Bacillus licheniformis spores in the gastrointestinal tract of pigs. J Appl Microbiol 104:1025–1033

    Article  PubMed  Google Scholar 

  52. Bohmer BM, Kramer W, Roth-Maier DA (2006) Dietary probiotic supplementation and resulting effects on performance, health status and microbial characteristics of primiparous sows. J Anim Physiol Anim Nutr 90:309–315

    Article  CAS  Google Scholar 

  53. Choi JY, Shinde PL, Ingale SL, Kim JS, Kim YW, Kim KH, Kwon IK, Chae BJ (2011) Evaluation of multi-microbe probiotics prepared by submerged liquid or solid substrate fermentation and antibiotics in weaning pigs. Livest Sci 138:144–151

    Article  Google Scholar 

  54. Kritas SK, Govaris A, Christodoulopouls G, Burriel AR (2006) Effect of Bacillus licheniformis and Bacillus subtilis supplementation of ewe's feed on sheep milk production and young lamb mortality. J Vet Med Ser 53:170–173

    Article  CAS  Google Scholar 

  55. Hong HA, Duc LH, Cutting SM (2005) The use of bacterial spore formers as probiotics. FEMS Microbiol Rev 29:813–835

    Article  CAS  PubMed  Google Scholar 

  56. Cartman ST, La Ragione RM, Woodward MJ (2008) Bacillus subtilis spores germinate in the chicken gastrointestinal tract. Appl Environ Microbiol 74:5254–5258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Jia R, Ma Q, Fan Y, Ji C, Zhang J, Liu T, Zhao L (2016) The toxic effects of combined aflatoxins and zearalenone in naturally contaminated diets on laying performance, egg quality and mycotoxins residues in eggs of layers and the protective effect of Bacillus subtilis biodegradation product. Food Chem Toxicol 90:142–150

    Article  CAS  PubMed  Google Scholar 

  58. Chistyakov V, Melnikov V, Chikindas ML, Khutsishvili M, Chagelishvili A, Bren A, Kostina N, Cavera V, Elisashvili V (2015) Poultry-beneficial solid-state Bacillus amyloliquefaciens B-1895 fermented soy bean formulation. Biosci Microbiota Food Health 34:25–28

    Article  CAS  PubMed  Google Scholar 

  59. Mazanko MS, Gorlov IF, Prazdnova EV, Makarenko MS, Usatov AV, Bren AB, Chistyakov VA, Tutelyan AV, Komarova ZB, Mosolova NI, Pilipenko DN, Krotova OE, Struk AN, Lin A, Chikindas ML (2018) Bacillus probiotic supplementations improve laying performance, egg quality, hatching of laying hens, and sperm quality of roosters. Probiotics Antimicro Prot 10:367–373

    Article  CAS  Google Scholar 

  60. Opanlinski M, Maiorka A, Dahlke F, Cunha F, Vargas FSC, Cardozo E (2007) On the use of probiotic (Bacillus subtilis-strain DSM 17299) as growth promoter in broiler diets. Braz J Poult Sci 9:99–103

    Article  Google Scholar 

  61. Sen S, Ingale SL, Kim YW, Kim JS, Kim KH, Lohakare JD, Kim EK, Kim HS, Ryu MH, Kwon IK, Chae BJ (2012) Effect of supplementation of Bacillus subtilis LS 1-2 to broiler diets on growth performance, nutrient retention, caecal microbiology and small intestinal morphology. Res Vet Sci 93:264–268

    Article  PubMed  Google Scholar 

  62. Huang MK, Choi YJ, Houde R, Lee JW, Lee B, Zhao X (2004) Effects of lactobacilli and an acidophilic fungus on the production performance and immune responses in broiler chickens. Poult Sci 83:788–795

    Article  CAS  PubMed  Google Scholar 

  63. Li L, Xu CL, Ma Q, Hao K, Jin ZY, Li K (2006) Effects of a dried Bacillus subtilis culture on egg quality. Poult Sci 85:364–368

    Article  CAS  PubMed  Google Scholar 

  64. Posada-Uribe LF, Romero-Tabarez M, Villegas-Escobar V (2015) Effect of medium components and culture conditions in Bacillus subtilis EA-CB0575 spore production. Bioprocess Biosyst Eng 38:1879–1888

    Article  CAS  PubMed  Google Scholar 

  65. Fayol-Messaoudi D, Berger CN, Coconnier-Polter MH, Lievin-Le MV, Servin AL (2005) pH-Lactic acid-, and non-lactic acid dependent activities of probiotic Lactobacilli against Salmonella enterica serovar typhimurium. Appl Environ Microbiol 71:6008–6013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. De Vries YP, Atmadja RD, Hornstra LM, de Vos WM, Abee T (2005) Influence of glutamate on growth, sporulation, and spore properties of Bacillus cereus ATCC 14579 in defined medium. Appl Environ Microbiol 71:3248–3254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Warriner K, Waites WM (1999) Enhanced sporulation in Bacillus subtilis grown on medium containing glucose:ribose. Lett Appl Microbiol 29:97–102

    Article  CAS  Google Scholar 

  68. Khardziani T, Kachlishvili E, Sokhadze K, Elisashvili V, Weeks R, Chikindas ML, Chistyakov V (2017) Elucidation of Bacillus subtilis KATMIRA 1933 potential for spore production in submerged fermentation of plant raw materials. Probiotics Antimicro Prot 9:435–443

    Article  CAS  Google Scholar 

  69. Khardziani T, Sokhadze K, Kachlishvili E, Chistyakov V, Elisashvili V (2017) Optimization of enhanced probiotic spore production in submerged cultivation of Bacillus amyloliquefaciens B-1895. J Microbiol Biotechnol Food Sci 7:132–136

    Article  CAS  Google Scholar 

  70. Chen ZM, Li Q, Liu HM, Yu N, Xie TJ, Yang MY, Shen P, Chen XD (2010) Greater enhancement of Bacillus subtilis spore yields in submerged cultures by optimization of medium composition through statistical experimental designs. Appl Microbiol Biotechnol 85:1353–1360

    Article  CAS  PubMed  Google Scholar 

  71. Rao YK, Tsay KJ, Wu WS, Tzeng YM (2007) Medium optimization of carbon and nitrogen sources for the production of spores from Bacillus amyloliquefaciens B128 using response surface methodology. Process Biochem 42:535–541

    Article  CAS  Google Scholar 

  72. Monteiro SMS, Clemente JJ, Carrondo MJT, Cunha AE (2014) Enhanced spore production of Bacillus subtilis grown in a chemically defined medium. Adv Microbiol 4:444–454

    Article  CAS  Google Scholar 

  73. Shi F, Zhu Y (2007) Application of statistically-based experimental designs in medium optimization for spore production of Bacillus subtilis from distillery effluent. BioControl 52:845–853

    Article  Google Scholar 

  74. Ren H, Su Y, Guo X (2018) Rapid optimization of spore production from Bacillus amyloliquefaciens in submerged cultures based on dipicolinic acid fluorimetry assay. AMB Expr 8:21

    Article  CAS  Google Scholar 

  75. Wangka-Orm C, Deeseenthum S, Leelavatcharamas V (2014) Low cost medium for spore production of Bacillus KKU02 and KKU03 and the effects of the produced spores on growth of giant freshwater prawn (Macrobrachium rosenbergii de man). Pak J Biol Sci 17:1015–1022

    Article  CAS  PubMed  Google Scholar 

  76. Sreena CP, Vimal KP, Denoj S (2016) Production of cellulases and xylanase from Bacillus subtilis MU S1 isolated from protected areas of Munnar wildlife division. J Microbiol Biotechnol Food Sci 5:500–504

    Article  CAS  Google Scholar 

  77. Feng Y, He Z, Ong SL, Hu J, Zhang Z, Ng WJ (2003) Optimization of agitation, aeration, and temperature conditions for maximum b-mannanase production. Enzyme Microbial Technol 32:282–289

    Article  CAS  Google Scholar 

  78. Kulpreecha S, Boonruangthavorn A, Meksiriporn B, Thongchul N (2009) Inexpensive fed-batch cultivation for high poly(3-hydroxybutyrate) production by a new isolate of Bacillus megaterium. J Biosci Bioeng 107:240–245

    Article  CAS  PubMed  Google Scholar 

  79. Abbas AA, Planchon S, Jobin M, Schmitt P (2014) A new chemically defined medium for the growth and sporulation of Bacillus cereus strains in anaerobiosis. J Microbiol Methods 105:54–58

    Article  CAS  PubMed  Google Scholar 

  80. O’Hara MB, Hageman J (1990) Energy and calcium ion dependence of proteolysis during sporulation of Bacillus subtilis cells. J Bacteriol 172:4161–4170

    Article  PubMed  PubMed Central  Google Scholar 

  81. Slieman TA, Nicholson WL (2001) Role of dipicolinic acid in survival of Bacillus subtilis spores exposed to artificial an solar UV radiation. Appl Env Microbiol 67:1274–1279

    Article  CAS  Google Scholar 

  82. El-blendary MA (2006) Bacillus thuringiensis and Bacillus sphaericus biopesticides production. J Basic Microbiol 46:158–170

    Article  CAS  Google Scholar 

  83. Shim YH, Shinde PL, Choi JY, Kim JS, Seo DK, Pak JI, Chae BJ, Kwon IK (2010) Evaluation of multi-microbial probiotics produced by submerged liquid and solid substrate fermentation methods in broilers. Asian-Aust J Anim Sci 23:521–529

    Article  CAS  Google Scholar 

  84. Badu KR, Satyanarayana T (1995) α-Amylase production by thermophilic Bacillus coagulans in solid state fermentation. Process Biochem 30:305–309

    Article  Google Scholar 

  85. Holker U, Hofer M, Lenz J (2004) Biotechnological advantages of laboratory scale solid-state fermentation with fungi. Appl Microbiol Biotechnol 64:175–186

    Article  CAS  PubMed  Google Scholar 

  86. Gangadharan D, Sivaramakrishnan S, Nampoothiri KM, Pandey A (2006) Solid culturing of Bacillus amyloliquefaciens for alpha amylase production. Food Technol Biotechnol 44:269–274

    CAS  Google Scholar 

  87. Zhao S, Hu N, Huang J, Liang Y, Zhao B (2008) High-yield spore production from Bacillus licheniformis by solid state fermentation. Biotechnol Lett 30:295–297

    Article  CAS  PubMed  Google Scholar 

  88. Ying W, Zhu R, Lu W, Gong L (2009) A new strategy to apply Bacillus subtilis MA139 for the production of solid-state fermentation feed. Lett Appl Microbiol 49:229–234

    Article  CAS  PubMed  Google Scholar 

  89. Zhang YR, Xiong HR, Guo XH (2014) Enhanced viability of Lactobacillus reuteri for probiotics production in mixed solid-state fermentation in the presence of Bacillus subtilis. Folia Microbiol 59:31–36

    Article  CAS  Google Scholar 

  90. Berikashvili V, Sokhadze K, Kachlishvili E, Elisashvili V, Chikindas ML (2017) Bacillus amyloliquefaciens spore production under solid-state fermentation of lignocellulosic residues. Probiotics Antimicro Prot 9:435–443

    Article  CAS  Google Scholar 

  91. Sen R, Babu KS (2005) Modelling and optimization of the process conditions for biomass production and sporulation of a probiotic culture. Process Biochem 40:2531–2538

    Article  CAS  Google Scholar 

  92. Das S, Kharkwal S, Pandey SK, Sen R (2010) Multi-objective process optimization and integration for the sequential and increased production of biomass, lipase and endospores of a probiotic bacterium. Biochem Eng J 50:77–81

    Article  CAS  Google Scholar 

  93. Riesenberg D, Guthke R (1999) High-cell-density cultivation of microorganisms. Appl Microbiol Biotechnol 51:422–430

    Article  CAS  PubMed  Google Scholar 

  94. Pandey KR, Vakil BV (2016) Development of bioprocess for high density cultivation yield of the probiotic Bacillus coagulans and its spores. J BioSci Biotechnol 5:173–181

    Google Scholar 

  95. Luna CL, Mariano RLR, Souto-Maior AM (2002) Production of a biocontrol agent for crucifers black rot disease. Braz J Chem Eng 19:133–140

    Article  CAS  Google Scholar 

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Acknowledgements

The authors are grateful for the financial support provided in the applied science project AR/106/7-280/14 by the Shota Rustaveli National Science Foundation of Georgia.

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Elisashvili, V., Kachlishvili, E. & Chikindas, M.L. Recent Advances in the Physiology of Spore Formation for Bacillus Probiotic Production. Probiotics & Antimicro. Prot. 11, 731–747 (2019). https://doi.org/10.1007/s12602-018-9492-x

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