Brevibacillus laterosporus, a pathogen of invertebrates and a broad-spectrum antimicrobial species

Insects

Volumn 4, Issue 3, 2013, Pages 476-492

  Ruiu, Luca ^a  

^a UNIVERSITY OF SASSARI   (Italy)

Author keywords

Antimicrobial; Biological control; Biopesticide; Bioremediation; Brevibacillus laterosporus; Entomopathogenic bacteria; Insecticide; Nematicide; Pests

Indexed keywords

EID: 84884225747     PISSN: None     EISSN: 20754450     Source Type: Journal    
DOI: 10.3390/insects4030476     Document Type: Review

References (101)

1. Oliveira, E.J.; Rabinovitch, L.; Monnerat, R.G.; Passos, L.K.; Zahner, V. Molecular characterization of Brevibacillus laterosporus and its potential use in biological control. Appl. Environ. Microbiol. 2004, 70, 6657-6664.
2. Khan, M.R.; Saha, M.L.; Afroz, H. Microorganisms associated with gemstones. Bangladesh J. Bot. 2001, 30, 93-96.
3. Raymundo, A.K.; Capistrano, B.G.; Aquino, A. Isolation, characterization and identification of bacteria from lahar. Philipp. Agric. Sci. 1997, 80, 57-64.
4. Laubach, A.C. Studies on aerobic, sporebearing, non pathogenic bacteria. Spore bearing organism in water. J. Bacteriol. 1916, 1, 505-512.
5. Suslova, M.Y.; Lipko, I.A.; Mamaeva, E.V.; Parfenova, V.V. Diversity of cultivable bacteria isolated from the water column and bottom sediments of the Kara Sea shelf. Mikrobiologiia (Russ. Federation) 2012, 81, 484-491.
6. White, G.F. The cause of European foulbrood. US Dep. Agric. Bur. Entomol. 1912, 157, 1-15.
7. Roy, D.K.; Singh, G.P.; Sahay, A.; Sahay, D.N.; Suryanarayana, N. Leaf surface microflora for tasar crop improvement. Indian Silk 2006, 45, 19-21.
8. Sarkar, P.K.; Hasenack, B.; Nout, M.J.R. Diversity and functionality of Bacillus and related genera isolated from spontaneously fermented soybeans (Indian Kinema) and locust beans (African Soumbala). Int. J. Food Microbiol. 2002, 77, 175-186.
9. Adegunloye, D.V.; Adetuyi, F.C.; Akinyosoye, F.A.; Doyeni, M.O. Microbial analysis of compost using cowdung as booster. Pak. J. Nutr. 2007, 6, 506-510.
10. Varadaraj, M.C.; Devi, N.; Keshava, N.; Manjrekar, S.P. Antimicrobial activity of neutralized extracellular culture filtrates of lactic acid bacteria isolated from a cultured Indian milk product ('dahi'). Int. J. Food Microbiol. 1993, 20, 259-267.
11. Román-Blanco, C.; Sanz-Gómez, J.J.; López-Díaz, T.-M.; Otero, A.; García-López, M.-L. Numbers and species of Bacillus during the manufacture and ripening of Castellano cheese. Milchwissenschaft 1999, 54, 385-388.
12. Iurlina, M.O.; Fritz, R. Characterization of microorganisms in Argentinean honeys from different sources. Int. J. Food Microbiol. 2005, 105, 297-304.
13. Fangio, M.F.; Roura, S.I.; Fritz, R. Isolation and identification of Bacillus spp. and related genera from different starchy foods. J. Food Sci. 2010, 75, M218-M221.
14. Sharma, A.; Rao, C.L.S.N.; Ball, B.K.; Hasija, S.K. Characteristics of extracellular proteases produced by Bacillus laterosporus and Flavobacterium sp. isolated from gelatin-factory effluents. World J. Microbiol. Biotechnol. 1996, 12, 615-617.
15. Chen, Y.; Gao, H.; Zhang, Y.; Deng, M.; Wu, Z.; Zhu, L.; Duan, Q.; Xu, B.; Liang, C.; Yue, Z.; Xiao, X. Analysis of the bacterial diversity existing on animal hide and wool: Development of a preliminary PCR-restriction fragment length polymorphism fingerprint database for identifying isolates. J. AOAC Int. 2012, 95, 1750-1754.
16. Bagherzadeh Kasmani, F.; Karimi Torshizi, M.A.; Allameh, A.; Shariatmadari, F. A novel aflatoxin-binding Bacillus probiotic: Performance, serum biochemistry, and immunological parameters in Japanese quail. Poultry Sci. 2012, 91, 1846-1853.
17. McCray, A.H. Spore-forming bacteria of the apiary. J. Agric. Res. 1917, 8, 399-420.
18. Smith, N.R.; Gordon, R.E.; Clark, F.E. Aerobic sporeforming bacteria. US Dep. Agric. Agric. Monograph. 1952, 16, 114-116.
19. Steinhaus, E.A. An orientation with respect to members of the genus Bacillus pathogenic for insects. Bacteriol. Rev. 1946, 10, 51-61.
20. Shida, O.; Takagi, H.; Kadowaki, K.; Komagata, K. Proposal for two new genera, Brevibacillus gen. nov. and Aneurinobacillus gen. nov. Int. J. Syst. Bacteriol. 1996, 46, 939-946.
21. Ruiu, L.; Satta, A.; Floris, I. Emerging entomopathogenic bacteria for insect pest management. Bull. Insectology 2013, 66, 181-186.
22. Gilliam, M.; Valentine, D.K. Bacteria isolated from the intestinal contents of foraging worker honey bees, Apis mellifera: The Genus Bacillus. J. Invertebr. Pathol. 1976, 28, 275-276.
23. Bailey, L. The pathogenicity for honey-bee larvae of microorganisms associated with European foulbrood. J. Insect Pathol. 1963, 5, 198-205.
24. Alippi, A.M. A comparison of laboratory techniques for the detection of significant bacteria of the honey bee, Apis mellifera, in Argentina. J. Apicult. Res. 1991, 30, 75-80.
25. Shimanuki, H.; Knox, D.A. Diagnosis of honey bee diseases. US Dep. Agric. Agric. Handbook 1991, AH-690, 10-11.
26. Djukic, M.; Poehlein, A.; Thürmer, A.; Daniel, R. Genome sequence of Brevibacillus laterosporus LMG 15441, a pathogen of invertebrates. J. Bacteriol. 2011, 193, 5535-5536.
27. Sharma, V.; Singh, P.K.; Midha, S.; Ranjan, M.; Korpole, S.; Patil, P.B. Genome sequence of Brevibacillus laterosporus strain GI-9. J. Bacteriol. 2012, 194, 1279.
28. Hong, H.A.; Duc, L.H.; Cutting, S.M. The use of bacterial spore formers as probiotics. FEMS Microbiol. Rev. 2005, 29, 813-835.
29. Porubcan, R.S. Administering Bacillus laterosporus to increase poultry feed conversion and weight gain. U.S. Patent 0,099,624, 29 May 2003.
30. Umezawa, K.; Takeuchi, T. Spergualin: A new antitumour antibiotic. Biomed. Pharmacother. 1987, 41, 227-232.
31. Hannay, C.L. The parasporal body of Bacillus laterosporus Laubach. J. Biophys. Biochem. Cytol. 1957, 3, 1001-1010.
32. Fitz-James, P.C., Young, I.E. Morphological and chemical studies of the spores and parasporal bodies of Bacillus laterosporus. J. Biophys. Biochem. Cytol. 1958, 4, 639-649.
33. Montaldi, F.A.; Roth, I.L. Parasporal bodies of Bacillus laterosporus sporangia. J. Bacteriol. 1990, 172, 2168-2171.
34. Rivers, D.B.; Vann, C.N.; Zimmack, H.L.; Dean, D.H. Mosquitocidal activity of Bacillus laterosporus. J. Invertebr. Pathol. 1991, 58, 444-447.
35. Singer, S. The Utility of Morphological Group II Bacillus. Adv. Appl. Microbiol. 1996, 42, 219-261.
36. Salama, H.S.; Foda, M.S.; El-Bendary, M.A.; Abdel-Razek, A. Infection of red palm weevil, Rhynchophorus ferrugineus, by spore-forming bacilli indigenous to its natural habitat in Egypt. J. Pest Sci. 2004, 77, 27-32.
37. Echeverri-Molina, D.; Santolamazza-Carbone, S. Toxicity of synthetic and biological insecticides against adults of the Eucalyptus snout-beetle Gonipterus scutellatus Gyllenhal (Coleoptera: Curculionidae). J. Pest Sci. 2010, 83, 297-305.
38. Du Rand, N.; Laing, M.D. Determination of insecticidal toxicity of three species of entomopathogenic spore-forming bacterial isolates against Tenebrio molitor L. (Coleoptera: Tenebrionidae). Afr. J. Microbiol. Res. 2011, 5, 2222-2228.
39. Arnaut, G.; Boets, A.; Damme, N.; Van Rie, J. Toxins. U.S. Patent 7,919,609, 5 April 2011.
40. Warren, G.W. Vegetative insecticidal proteins: Novel proteins for control of corn pests. In Advances in Insect Control: The Role of Transgenic Plants; Carozzi, N.B., Koziel, M.G., Eds.; Taylor & Francis: London, UK, 1997; pp. 109-121.
41. Bacillus thuringiensis Toxin Nomenclature. Available online: http://www.lifesci.sussex.ac.uk/home/Neil_Crickmore/Bt/ (accessed on 17 July 2013).
42. Schnepf, H.E.; Narva, K.E.; Stockhoff, B.A.; Lee, S.F.; Walz, M.; Sturgis, B. Pesticidal toxins and genes from Bacillus laterosporus strains. U.S. Patent 6,956,116, 18 October 2005.
43. Favret, E.M.; Yousten, A.A. Insecticidal activity of Bacillus laterosporus. J. Invertebr. Pathol. 1985, 45, 195-203.
44. Erturk, O.; Demirbag, Z. Studies on bacterial flora and biological control agent of Cydia pomonella L. (Lepidoptera: Tortricidae). Afr. J. Biotechnol. 2006, 5, 2081-2085.
45. Ruiu, L.; Floris, I.; Satta, A.; Ellar, D.J. Toxicity of a Brevibacillus laterosporus strain lacking parasporal crystals against Musca domestica and Aedes aegypti. Biol. Contr. 2007, 43, 136-143.
46. Smirnova, T.A.; Minenkova, I.B.; Orlova, M.V.; Lecadet, M.-M.; Azizbekyan, R.R. The crystal-forming strains of Bacillus laterosporus. Res. Microbiol. 1996, 147, 343-350.
47. Orlova, M.V.; Smirnova, T.A.; Ganushkina, L.A.; Yacubovich, V.Y.; Azizbekyan, R.R. Insecticidal activity of Bacillus laterosporus. Appl. Environ. Microbiol. 1998, 64, 2723-2725.
48. Goldberg, L.J.; Margalit, J. A bacterial spore demonstrating rapid larvicidal activity against Anopheles sergentii, Uranotaenia unguiculata, Culex univittatus, Aedes aegypti and Culex pipiens. Mosq. News 1977, 37, 355-358.
49. Zubasheva, M.V.; Ganushkina, L.A.; Smirnova, T.A.; Azizbekyan, R.R. Larvicidal activity of crystal-forming strains of Brevibacillus laterosporus. Appl. Biochem. Microbiol. 2010, 46, 755-762.
50. Zubasheva, M.V.; Ganushkina, L.A.; Smirnova, T.A.; Azizbekyan, R.R. Enhancement of larvicidal activity of Brevibacillus laterosporus by bioincapsulation in Protozoa Tetrahymena pyriformis and Entamoeba moshkovskii. Appl. Biochem. Microbiol. 2011, 47, 762-766.
51. Ruiu, L.; Delrio, G.; Ellar, D.J.; Floris, I.; Paglietti, B.; Rubino, S.; Satta, A. Lethal and sublethal effects of Brevibacillus laterosporus on the housefly (Musca domestica). Entomol. Exp. Appl. 2006, 118, 137-144.
52. Bravo, A.; Gill, S.S.; Soberon M. Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 2007, 49, 423-435.
53. Ruiu, L.; Satta, A.; Floris, I. Observations on house fly larvae midgut ultrastructure after Brevibacillus laterosporus ingestion. J. Invertebr. Pathol. 2012, 111, 211-216.
54. Ruiu, L; Satta, A.; Floris, I. Ultrastructural changes in the gut of adult flies after Brevibacillus laterosporus ingestion. In Proceedings of the 43rd Annual Meeting of the Society for Invertebrate Pathology, Trabzon, Turkey, 11-15 July 2010; Contributed paper 149, p. 97.
55. Ruiu, L.; Satta, A.; Floris, I. Immature house fly (Musca domestica) control in breeding sites with a new Brevibacillus laterosporus formulation. Environ. Entomol. 2008, 37, 505-509.
56. Ruiu, L.; Satta, A.; Floris, I. Comparative applications of azadirachtin and Brevibacillus laterosporus based formulations for house fly management experiments in dairy farms. J. Med. Entomol. 2011, 48, 345-350.
57. Ruiu, L.; Satta, A.; Floris, I. Susceptibility of the house fly pupal parasitoid Muscidifurax raptor (Hymenoptera: Pteromalidae) to the entomopathogenic bacteria Bacillus thuringiensis and Brevibacillus laterosporus. Biol. Contr. 2007, 43, 188-194.
58. Ruiu, L.; Floris, I.; Satta, A. Susceptibility of the honeybee (Apis mellifera L.) to entomopathogenic bacterial toxins used for the biological control. Redia 2007, 90, 87-90.
59. Bone, L.W.; Singer, S. Control of parasitic nematode ova/larvae with a Bacillus laterosporus. U.S. Patent 5,045,314, 3 September 1991.
60. Huang, X.; Tian, B.; Niu, Q.; Yang, J.; Zhang, L.; Zhang, K. An extracellular protease from Brevibacillus laterosporus G4 without parasporal crystals can serve as a pathogenic factor in infection of nematodes. Res. Microbiol. 2005, 156, 719-727.
61. Maizels, R.M.; Blaxter, M.L.; Selkir, M.E. Forms and functions of nematode surfaces. Exp. Parasitol. 1993, 77, 380-384.
62. Lian, L.H.; Tian, B.Y.; Xiong, R.; Zhu, M.Z.; Xu, J.; Zhang, K.Q. Proteases from Bacillus: A new insight into the mechanism of action for rhizobacterial suppression of nematode populations. Lett. Appl. Microbiol. 2007, 45, 262-269.
63. Tian, B.; Li, N.; Lian, L.; Liu, J.; Yang, J.; Zhang, K.Q. Cloning, expression and deletion of the cuticle-degrading protease BLG4 from nematophagous bacterium Brevibacillus laterosporus G4. Arch. Microbiol. 2006, 186, 297-305.
64. Tian, B.; Ke, C.R.; Huang, W.; Zhang, K.-Q.; Huang, J.-Z. Direct visualization of bacterial infection process in nematode hosts by an improved immunocytochemical method. World J. Microbiol. Biotechnol. 2009, 25, 909-912.
65. Tian, B.; Huang, W.; Huang, J.; Jiang, X.; Qin, L. Investigation of protease-mediated cuticledegradation of nematodes by using an improved immunofluorescence-localization method. J. Invertebr. Pathol. 2009, 101, 143-146.
66. Tian, B.; Yang, J.; Lian, L.; Wang, C.; Li, N.; Zhang, K.Q. Role of an extracellular neutral protease in infection against nematodes by Brevibacillus laterosporus strain G4. Appl. Microbiol. Biotechnol. 2007, 74, 372-380.
67. Singer, S.; Bair, T.B.; Hammill, T.B.; Berte, A.M.; Correa-Ochoa, M.M.; Stambaugh, A.D. Fermentation and toxin studies of the molluscicidal strains of Bacillus brevis. J. Ind. Microbiol. 1994, 13, 112-119.
68. Strayer, D.L.; Hattala, K.A.; Kahnle, A.W. Effects of an invasive bivalve (Dreissena polymorpha) on fish in the Hudson River estuary. Can. J. Fish. Aquat. Sci. 2004, 61, 924-941.
69. Singer, S.; Van Fleet, A.L.; Viel, J.J.; Genevese, E.E. Biological control of the zebra mussel Dreissena polymorpha and the snail Biomphalaria glabrata, using gramicidin S and D and molluscicidal strains of Bacillus. J. Ind. Microbiol. Biotechnol. 1997, 18, 226-231.
70. Chandel, S.; Allan, E.J.; Woodward, S. Biological control of Fusarium oxysporum f.sp. lycopersici on tomato by Brevibacillus brevis. J. Phytopathol. 2010, 158, 470-478.
71. Saikia, R.; Gogoi, D.K.; Mazumder, S.; Yadav, A.; Sarma, R.K.; Bora, T.C.; Gogoi, B.K. Brevibacillus laterosporus strain BPM3, a potential biocontrol agent isolated from a natural hot water spring of Assam, India. Microbiol. Res. 2011, 166, 216-225.
72. Song, Z.; Liu, K.; Lu, C.; Yu, J.; Ju, R.; Liu, X. Isolation and characterization of a potential biocontrol Brevibacillus laterosporus. Afr. J. Microbiol. Res. 2011, 5, 2675-2681.
73. Idris, H.A.; Labuschagne, N.; Korsten, L. Suppression of Pythium ultimum root rot of sorghum by rhizobacterial isolates from Ethiopia and South Africa. Biol. Contr. 2008, 45, 72-84.
74. Zhang, S.; Reddy, M.S.; Kokalis-Burelle, N.; Wells, L.W.; Nightengale, S.P.; Kloepper, J.W. Lack of induced systemic resistance in peanut to late leaf spot disease by plant growth-promoting rhizobacteria and chemical elicitors. Plant Dis. 2001, 85, 879-884.
75. Yobo, K.S.; Laing, M.D.; Hunter, C.H. Effect of commercially available rhizobacteria strains on growth and production of lettuce, tomato and pepper. S. Afr. J. Plant Soil 2004, 21, 230-235.
76. Li, X.; Wang, Z.; Dong, X.; Wang, G.; Jia, Y. Bioactivity quantification of a novel antimicrobial peptide by agar diffusion bioassay. In Proceedings of the 2011 International Conference on New Technology of Agricultural Engineering, Zibo, China, 27 May 2011; Article number 5943979, pp. 1096-1099.
77. Zhao, J.; Guo, L.; Zeng, H.; Yang, X.; Yuan, J.; Shi, H. Xiong, Y.; Chen, M.; Han, L.; Qiu, D. Purification and characterization of a novel antimicrobial peptide from Brevibacillus laterosporus strain A60. Peptides 2012, 33, 206-211.
78. Brogden, K.A. Antimicrobial peptides: Pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 2005, 3, 238-250.
79. Prasanna, L.; Eijsink, V.G.H.; Meadow, R.; Gaseidnes, S. A novel strain of Brevibacillus laterosporus produces chitinases that contribute to its biocontrol potential. Appl. Microbiol. Biotechnol. 2013, 97, 1601-1611.
80. Singh, P.K.; Chittpurna; Ashish; Sharma, V.; Patil, P.B.; Korpole, S. Identification, purification and characterization of laterosporulin, a novel bacteriocin produced by Brevibacillus sp. strain GI-9. PLoS One 2012, 7, e31498.
81. Alippi, A.M.; Reynaldi, F.J. Inhibition of the growth of Paenibacillus larvae, the causal agent of American foulbrood of honeybees, by selected strains of aerobic spore-forming bacteria isolated from apiarian sources. J. Invertebr. Pathol. 2006, 91, 141-146.
82. Shoji, J.; Sakazaki, R.; Wakisaka, Y.; Koizumi, K.; Mayama, M. Isolation of a new antibiotic, laterosporamine. (Studies on antibiotics from the genus Bacillus. XIII). J. Antibiot. 1976, 29, 390-393.
83. Barsby, T.; Kelly, M.T.; Andersen, R.J. Tupuseleiamides and basiliskamides, new acyldipeptides and antifungal polyketides produced in culture by a Bacillus laterosporus isolate obtained from a tropical marine habitat. J. Nat. Prod. 2002, 65, 1447-1451.
84. Desjardine, K.; Pereira, A.; Wright, H.; Matainaho, T.; Kelly, M.; Andersen, R.J. Tauramamide, a lipopeptide antibiotic produced in culture by Brevibacillus laterosporus isolated from a marine habitat: Structure elucidation and synthesis. J. Nat. Prod. 2007, 70, 1850-1853.
85. Qin, C.; Xu, C.; Zhang, R.; Niu, W.; Shang, X. On-resin cyclization and antimicrobial activity of Laterocidin and its analogues. Tetrahedron Lett. 2010, 51, 1257-1261.
86. Kamiyama, T.; Umino, T.; Nakamura, Y.; Itezono, Y.; Sawairi, S.; Satoh, T.; Yokose, K. Bacithrocins A, B and C, novel thrombin inhibitors. J. Antibiot. 1994, 47, 959-968.
87. Aoyagi, T.; Yoshida, S.; Matsuda, N.; Ikeda, T.; Hamada, M.; Takeuchi, T. Leuhistin, a new inhibitor of aminopeptidase M, produced by Bacillus laterosporus BMI156-14F1. I. Taxonomy, production, isolation, physico-chemical properties and biological activities. J. Antibiot. 1991, 44, 573-578.
88. Aramori, I.; Fukagawa, M.; Tsumura, M.; Iwami, M.; Yokota, Y.; Kojo, H.; Kohsaka, M.; Ueda, Y.; Imanaka, H. Isolation of soil strains producing new cephalosporin acylases. J. Ferment. Bioeng. 1991, 72, 227-231.
89. Wolfenden, R.E.; Pumford, N.R.; Morgan, M.J.; Shivaramaiah, S.; Wolfenden, A.D.; Pixley, C.M.; Green, J.; Tellez, G.; Hargis, B.M. Evaluation of selected direct-fed microbial candidates on live performance and Salmonella reduction in commercial turkey brooding houses. Poultry Sci. 2011, 90, 2627-2631.
90. Kuznetsova, N.I.; Azizbekyan, R.R., Konyukhov, I.V., Pogosyan, S.I.; Rubin, A.B. Inhibition of photosynthesis in cyanobacteria and plankton algae by the bacterium Brevibacillus laterosporus metabolites. Dokl. Biochem. Biophys. 2008, 421, 181-184.
91. Wen, J.; XiangHu, H.; ChangLing, L.; JiaHui, Z. Research on algicidal effect of bioactive metabolites of Brevibacillus laterosporus on Oscillattoria sp. in shrimp pond. J. Fish. Chin. 2013, 37, 465-472.
92. Lim, J.G.; Park, D.H. Degradation of polyvinyl alcohol by Brevibacillus laterosporus: Metabolic pathway of polyvinyl alcohol to acetate. J. Microbiol. Biotechnol. 2001, 11, 928-933.
93. Gomare, S.S.; Govindwar, S.P. Brevibacillus laterosporus MTCC 2298: A potential azo dye degrader. J. Appl. Microbiol. 2009, 106, 993-1004.
94. Jeyaseelan, A.; Sivashanmugam, K.; Jayaraman, K. Comparative applications of bioreactor and shake flask system for the biodegradation of tannin and biotreatment of composite tannery effluents. Pollut. Res. 2008, 27, 371-375.
95. Reda, A.B.; Ashraf, T.A.-H. Optimization of bacterial biodegradation of toluene and phenol under different nutritional and environmental conditions. J. Appl. Sci. Res. 2010, 6, 1086-1095.
96. Zouboulis, A.I.; Loukidou, M.X.; Matis, K.A. Biosorption of toxic metals from aqueous solutions by bacteria strains isolated from metal-polluted soils. Process Biochem. 2004, 39, 909-916.
97. Holail, H.; Al-Bahadly, A.; Olama, Z. Detoxification of hexavalent chromium Cr(VI) by Bacillus laterosporus and its application in Lebanese waste water. WIT Trans. Ecol. Environ. 2011, 153, 233-242.
98. Kamika, I.; Momba, M.N.B. Comparing the tolerance limits of selected bacterial and protozoan species to nickel in wastewater systems. Sci. Total Environ. 2011, 410-411, 172-181.
99. Zahner, V.; Rabinovitch, L.; Suffys, P.; Momen, H. Genotypic diversity among Brevibacillus laterosporus strains. Appl. Environ. Microbiol. 1999, 65, 5182-5185.
100. Arulmani, M.; Aparanjini, K.; Vasanthi, K.; Arumugam, P.; Arivuchelvi, M.; Kalaichelvan, P.T. Purification and partial characterization of serine protease from thermostable alkalophilic Bacillus laterosporus-AK1. World J. Microbiol. Biotechnol. 2007, 23, 475-481.
101. Usharani, B.; Muthuraj, M. Production and characterization of protease enzyme from Bacillus laterosporus. Afr. J. Microbiol. Res. 2010, 4, 1057-1063.