A cryptic Bacillus isolate exhibited narrow 16s rRNA gene sequence divergence with Bacillus thuringiensis and showed low maintenance requirements in hyper-osmotic complex substrate cultivations

Biotechnology and Bioengineering

Volumn 91, Issue 7, 2005, Pages 838-847

  Sachidanandham, Ramaiah ^a   Al Shayji, Yousif ^a   Al Awadhi, Nader ^a   Gin, Karina Yew Hoong ^b  

^a KUWAIT INSTITUTE FOR SCIENTIFIC RESEARCH   (Kuwait)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

16S rRNA gene sequence; B. mojavensis; B. thuringiensis; Insecticidal crystal proteins; Maintenance coefficient; Surrogate host

Indexed keywords

COMPLEXATION; CRYSTALS; GENES; MATHEMATICAL MODELS; OSMOSIS; PROTEINS; SAMPLING; SOILS;

16S RRNA GENE SEQUENCE; B. MOJAVENSIS; B. THURINGIENSIS; INSECTICIDAL CRYSTAL PROTEINS; MAINTENANCE COEFFICIENT; SURROGATE HOST;

RNA;

BACTERIAL PROTEIN; CRY PROTEIN; CRYSTAL PROTEIN; RNA 16S; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS; BACILLUS THURINGIENSIS; BACTERIAL GROWTH; BACTERIUM CULTURE; BACTERIUM ISOLATE; BIOMASS; CULTURE MEDIUM; GENE SEQUENCE; GROWTH RATE; MATHEMATICAL MODEL; NONHUMAN; PHYLOGENY; RNA SEQUENCE;

BACILLUS; BACILLUS THURINGIENSIS; CULTURE MEDIA; HYPERTONIC SOLUTIONS; KUWAIT; MODELS, BIOLOGICAL; OSMOTIC PRESSURE; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SOIL MICROBIOLOGY;

BACILLUS LICHENIFORMIS; BACILLUS MOJAVENSIS; BACILLUS OLERONIUS; BACILLUS THURINGIENSIS;

EID: 25144444384     PISSN: 00063592     EISSN: None     Source Type: Journal    
DOI: 10.1002/bit.20554     Document Type: Article

References (84)

1. Agaisse H, Lereclus D. 1994. Expression in Bacillus subtilis of the Bacillus thuringiensis cryIIIA toxin gene is not dependent on a sporulation-specific sigma factor and is increased in SpoOA mutant. J Bacteriol 176:4734-4741.
2. Agaisse H, Lereclus D. 1995. How does Bacillus thuringiensis produce so much insecticidal crystal protein? J Bacteriol 177:6027-6032.
3. Aim RA, Ling LS, Moir DT, et al. 1999. Genomic-sequence comparison of two unrelated isolated of the human gastric pathogen Helicobacter pylori. Nature 397:176-180.
4. Arbige M, Chesbro WR. 1982. Very slow growth of Bacillus polymyxa: Stringent response and maintenance energy. Arch Microbiol 132:338-344.
5. Baba T, Takeuchi F, Kuroda M, et al. 2002. Genome and virulence determinants of high virulence community acquired MRSA. Lancet 359:1819-1827.
6. Bacon CW, Hinton DM. 2002. Endophytic and biological control potential of Bacillus mojavensis and related species. Biol Control 23:274-284.
7. Bailey JE. 1998. Mathematical modeling and analysis in biochemical engineering: Past accomplishments and future opportunities. Biotechnol Progr 14:8-20.
8. Bar E, Lieman-Hurwitz J, Rahamim E, Keynan A, Sandler N. 1991. Cloning and expression of Bacillus thuringiensis δ-endotoxins DNA in Bacillus sphaericus. J Invertebr Pathol 57:149-158.
9. Baum JA, Matvar T. 1995. Regulation of insecticidal crystal protein production in Bacillus thuringiensis. Mol Microbiol 18:1-12.
10. Becker P, Maerkl H. 2000. Modeling of olive oil degradation and oleic acid inhibition during chemostat and batch cultivation of Bacillus thermoleovorans IHI-91. Biotechnol Bioeng 70(6):630-637.
11. Beres SB, Sylva GL, Barbian KD, et al. 2002. Genome sequence of a serotype M3 strain of group A Streptococcus: Phage-encoded toxins, the high-virulence phenotype, and clone emergence. Proc Natl Acad Sci USA 99:10078-10083.
12. Brinkmann LJ, Mattes RE, Buckel P. 1989. High-level expression of recombinant genes in Escherichia coli dependent on the availability of the dnaY gene product. Gene 85:109-114.
13. Bulthuis BA, Koningstein GM, Stouthamer AH, van-Verseveld HW. 1989. A comparison between aerobic growth of Bacillus licheniformis in continuous culture and partial-recycling fermenter, with contributions to the discussion on maintenance energy demand. Arch Microbiol 152:499-507.
14. Carlson CR, Kolsto AB. 1993. A complete physical map of a Bacillus thuringiensis chromosome. J Bacteriol 175:1053-1060.
15. Carlson CR, Caugant DA, Kolsto AB. 1996. Genotype diversity among Bacillus cereus and Bacillus thuringiensis strains. Appl Environ Microbiol 60:1719-1725.
16. Chen GFT, Inouye M. 1990. Suppression of the negative effect of minor arginine codons on gene expression: Preferential usage of minor codons within the first 25 codons of the Escherichia coli genes. Nucleic Acids Res 18:1465-1473.
17. - ions. J Bacteriol 171:880-886.
18. Christiansen T, Michaelsen S, Wumpelmann M, Nielsen J. 2003. Production of savinase and population viability of Bacillus clausii during high-cell-density fed-batch cultivations. Biotechnol Bioeng 83(2):344-352.
19. Chunjatupornchai W, Hofte H, Seurinck J, Angsuthana-sombat C, Vaeck M. 1988. Common features of Bacillus thuringiensis toxins specific for Diptera and Lepidoptera. Eur J Biochem 173:9-16.
20. Cohan FM. 2004. Periodic selection and ecological diversity in bacteria. In: Nurminsky D, editor. Selective sweep. Georgetown, Texas: Landes Bioscience.
21. Crissman JW, Causey SC, Thorne L, Pollock TJ. 1989. Accumulation of the insecticidal crystal protein of Bacillus thuringiensis subsp. kurstaki in post-exponential-phase Bacillus subtilis. Appl Environ Microbiol 55:2302-2307.
22. De-Medicis E, Paquette J, Gauthier JJ, Shapcott D. 1986. Magnesium and manganese content of halophilic bacteria. Appl Environ Microbiol 52:567-573.
23. Feldgarden M, Byrd N, Cohan FM. 2003. Gradual evolution in bacteria: Evidence from Bacillus systematics. Microbiol-SGM 149:3565-3573.
24. Goeddel DV. 1990. Systems for heterologous gene expression. Method Enzymol 185:3-7.
25. Goldman E, Rosenberg AH, Zubay G, Studier FW. 1995. Consecutive low-usage leucine codons block translation only when near the 5′ end of a message in Escherichia coli. J Mol Biol 254:467-473.
26. Gonzalez JM Jr, Dulmage HT, Carlton BC. 1981. Correlation between specific plasmids and δ-endotoxin production in Bacillus thuringiensis. Plasmid 5:351-365.
27. Gurkan C, Ellar DJ. 2003. Expression of the Bacillus thuringiensis Cyt2AaI toxin in Pichia pastoris using a synthetic gene construct. Biotechnol Appl Bioc 38:25-33.
28. Hazel JR, Williams EE. 1990. The role of alterations in membrane synthetic lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res 29:167-227.
29. Heijnen JJ, vanDijken JR 1992. In search of a thermodynamic description of biomass yields for the chemotrophic growth of microorganisms. Biotechnol Bioeng 39:833-858.
30. Hinton DM, Bacon CW. 1995. Enterobacter cloacae is an endophytic symbiont of corn. Mycopathologia 129:117-125.
31. Hodgson J. 1993. Expression systems: A user's guide. Bio/Technol 11:887-893.
32. Imhoff JF. 1984. Betaine is the main compatible solute of halotolerant eubacteria. J Bacteriol 160:478-479.
33. Ivanov I, Alexandrova R, Dragulev B, Saraffova A, AbouHaidar MG. 1992. Effect of tandemly repeated AGG triplets on the translation of CAT-mRNA in E. coli. FEBS Lett 307:173-176.
34. Jianzhou Y, Songpeng Z. 2002. Study on the conditions of Bacillus thuringiensis fermentation in monosodium glutamate wastewater. Food Ferm Ind 28:28-32.
35. Kamekura M, Kushner DJ. 1984. Effect of chloride and glutamate ions on in-vitro protein synthesis by the moderate halophile Vibrio costocola. J Bacteriol 160:385-390.
36. Khampang P, Chungjatupornchai W, Luxananil P, Panyim S. 1999. Efficient expression of mosquito-larvicidal proteins in a gram-negative bacterium capable of recolonization in the guts of Anopheles dirus larva. Appl Microbiol Biot 51:79-84.
37. Kogut M, Madira WM. 1978. Dihydrostreptomycin as a probe to study the effects of salt concentration during growth on cell constituents in a moderate halophile. In: Chaplan SR, Ginzburg M, editors. Energetics and structure of halophilic microorganisms. Amsterdam, The Netherlands: Elsevier/North Holland Biomedical Press, pp 521-527.
38. Kota M, Daniell H, Varma S, Garczynski SF, Gould F. 1999. Overexpression of the Bacillus thuringiensis (Bt) Cry2Aa2 protein in chloroplasts confers resistance to plants against susceptible and Bt-resistant insects. Proc Natl Acad Sci USA 96:1840-1845.
39. Kushner DJ, Hamaide F, MacLeod RA. 1983. Development of salt-resistant active transport in a moderately halophilic bacterium. J Bacteriol 153:1163-1171.
40. Lereclus D, Agaisse H, Gominet M, Chaufaux J. 1995. Overproduction of encapsulated insecticidal crystal proteins in a Bacillus thuringiensis SpoOA mutant. Bio/Technol 13:67-71.
41. Lessard P. 1996. Metabolic engineering: The concept coalesces. Nat Biotechnol 14:1654-1655.
42. Lisansky SG, Quinlan R, Tassoni G. 1993. The Bacillus thuringiensis production handbook, Laboratory methods, manufacturing, formulation, quality control, registration. Newbury: CRL press.
43. Liu J.-W, Yap WH, Thanabalu T, Porter AG. 1996. Efficient synthesis of mosquitocidal toxins in Asticcacaulis excentricus demonstrates potential of gram-negative bacteria in mosquito control. Nat Biotechnol 14:343-347.
44. Liu Y, Tabashnik BE, Dennehy TJ, Patin AL, Bartlet AC. 1999. Development time and resistance to Bt crops. Nature 400:1.
45. MacIntosh SC, Stone TB, Sims SR, Hunst PL, Greenplate JT, Marrone PG, Perlak FJ, Fischhoff DA, Fuchs RL. 1990. Specificity and efficacy of purified Bacillus thuringiensis proteins against agronomically important insects. J Invertebr Pathol 56:258-266.
46. Margalith Y, Ben-Dov E. 2000. Biological control by Bacillus thuringiensis subsp. israelensis. In: Rechcigl JE, Rechcigl NA, editors. Insect pest management: Techniques for environmental protection. Boca Raton FL: CRC Press, pp 243-301.
47. Marino MH. 1989. Expression systems for heterologous protein production. BioPharm 2:18-33.
48. Mignone CF, Avignone-Rossa C. 1996. Analysis of glucose carbon fluxes in continuous cultures of Bacillus thuringiensis. Appl Microbiol Biot 46:78-84.
49. Neijssel OM, Tempest DW. 1976. Bioenegetics aspects of aerobic growth of Klebsiella aerogens NCTC 418 in carbon-limited and carbon sufficient culture. Arch Microbiol Physiol 107:215-221.
50. Oh H, Lee SJ, Jang M, Yoon B. 2000. Microcystin production by Microcystis aeruginosa in a phosphate-limited chemostat. Appl Environ Microbiol 66:176-179.
51. Pirt SJ. 1982. Maintenance energy: A general model for energy-limited and energy-sufficient growth. Arch Microbiol 133:300-302.
52. Qaim M, Zilberman D. 2003. Yield effects of genetically modified crops in developing countries. Science 5608:900-902.
53. Roberts MS, Cohan FM. 1995. Recombination and migration rates in natural population of Bacillus subtilis and Bacillus mojavensis. Evolution 49:1081-1094.
54. Roth WG, Leckie MP, Dietzler DN. 1985a. Osmotic stress drastically inhibits active transport of carbohydrates of Escherichia coli. Biochem Biophys Res Commun 126:434-441.
55. Roth WG, Porter SE, Leckie MP, Porter BE, Dietzler DN. 1985b. Restoration of cell volume and the reversal of carbohydrate transport and growth inhibition of osmotically up-shocked Escherichia coli. Biochem Biophys Res Commun 126:442-449.
56. Sachidanandham R, Gin KYH. 2003. Flow cytometric detection of β-D-glucuronidase gene in wild-type bacteria cells using in-situ PCR. Biotechnol Bioeng 82(2):127-133.
57. Sachidanandham R, Kalaiselvi G. 1998. Maintenance requirements in Bacillus sphaericus 1593M under dual substrate limitations estimated at zero growth rate in a total cell retention culture. Bioproc Biosyst Eng 19:243-245.
58. Sachidanandham R, Jenny K, Fiechter A, Jayaraman K. 1997. Stabilization and increased production of insecticidal crystal proteins of Bacillus thuringiensis subsp. galleriae in steady and transient state continuous cultures. Appl Microbiol Biotechnol 47:12-17.
59. Sachidanandham R, Gin KYH, Laa PC. 2005. Monitoring of active but non-culturable bacterial cells by flow cytometry. Biotechnol Bioeng 89:24-31.
60. San-Martin R, Bushell D, Leak DJ, Hartley BS, Martin RS. 1994. Cultivation of an L-lactate dehydrogenase mutant of Bacillus stearothermophilus in continuous culture with cell recycle. Biotechnol Bioeng 44:21-28.
61. Schnepf E, Crickmore N, Van-Rie J, Lereclus D, Baum J, Fietelson J, Zeigler DR, Dean DH. 1998. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol R 62:775-806.
62. Scholten JCM, Conrad R. 2000. Energetics of syntrophic propionate oxidation in defined batch and chemostat cocultures. Appl Environ Microbiol 66(7):2934-2942.
63. Shivakumar AG, Gunling GJ, Benson TA, Casuto D, Miller F, Spear BB. 1986. Vegetative expression of the δ-endotoxin genes of Bacillus thuringiensis subsp. kurstaki in Bacillus subtilis. J Bacteriol 166:194-204.
64. Shivakumar AG, Vanags RI, Wilcox DR, Katz L, Vary PS, Fox JL. 1989. Gene dosage effect on the expression of the delta-endotoxin genes of Bacillus thuringiensis subsp. kurstaki in Bacillus subtilis and Bacillus megaterium. Gene 79:21-31.
65. Singh-Bora R, Murty MG, Shenbagarathai R, Sekar V. 1994. Introduction of a lepidopteran specific insecticidal crystal protein gene of Bacillus thuringiensis subsp. kurstaki by conjugal transfer into a Bacillus megaterium strain that persists in the cotton phyllosphere. Appl Environ Microbiol 60:214-222.
66. Soltes-Rak E, Kushner DJ, Williams DD, Coleman JR. 1995. Factors regulating cryIVB expression in the cyanobacterium Synecchococcus PCC7942. Mol Gen Genet 246:301-308.
67. Stouthamer AH, Bulthuis BA, van-Verseveld HW. 1990. Energetics of growth at low growth rates and its relevance for the maintenance concept. In: Poole RK, Bazin MJ, Keevil CW, editors. Microbial growth dynamics. Oxford, United Kingdom: IRL Press, pp 85-102.
68. Sturz AV, Christie BR, Nowak J. 2000. Bacterial endophytes: Potential role in developing sustainable systems of crop production. Crit Rev Plant Sci 19:1-30.
69. Tappe W, Laverman A, Bohland M, Braster M, Rittershaus S, Groeneweg J, van-Verseveld HW. 1999. Maintenance energy demand and starvation recovery dynamics of Nitrosomonas europaea and Nitrobacter winogradskyi cultivated in a retentostat with complete biomass retention. Appl Environ Microbiol 65:2471-2477.
70. Thanabalu T, Hindley T, Brenner S, Oei C, Berry C. 1992. Expression of the mosquitocidal toxins of Bacillus sphaericus and Bacillus thuringiensis subsp. israelensisby recombinant Caulobacter crescentus, a vehicle for biological control aquatic insect larvae. Appl Environ Microbiol 58:905-910.
71. Thauer RK, Jungermann K, Decker K. 1977. Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41:100-180.
72. Tijhuis L, VanLoosdrecht MCM, Heijnen JJ. 1993. A thermodynamically based correlation for maintenance gibbs energy requirements in aerobic and anaerobic chemostrophic growth. Biotechnol Bioeng 42:509-519.
73. Traore AS, Gaudin C, Hatchikian CE, Gall JL, Belaich JL. 1983. Energetics of growth of a defined mixed culture of Desulfovibrio vulgaris and Methanosarcina barkeri: Maintenance energy coefficient of the sulfate-reducing organism in the absence and presence of its partner. J Bacteriol 155:1260-1264.
74. van-Verseveld HW, Arbige M, Chesbro WR. 1984. Continuous culture of bacteria with biomass retention. Trends Biotechnol 2:8-12.
75. van-Verseveld HW, de-Hollander JA, Frankena J, Braster M, Leeuwerik FJ, Stouthamer AH. 1986. Modeling of microbial substrate conversion, growth and product formation in a recycling fermenter. Antonie Leeuwenhoek 52:325-342.
76. Vidyarthi AS, Tyagi RD, Valero JR, Surampalli RY. 2002. Studies on the production of Bacillus thuringiensis based biopesticides using wastewater sludge as a raw material. Water Res 36:4850-48601.
77. Vreeland RH, Mierau BD, Litchfield CD, Martin EL. 1983. Relationship of the internal solute composition to the salt tolerance of Halomonas elongate. Can J Microbiol 29:407-414.
78. Ward ES, Ellar DJ. 1988. Cloning and expression of two homologous genes of Bacillus thuringiensis subsp. israelensis which endcode 130-kilodalton mosquitocidal proteins. J Bacteriol 170:727-735.
79. Ward ES, Ridley AR, Ellar DJ, Todd JA. 1996. Bacillus thuringiensis var israelensis δ-endotoxin. Cloning and expression of the toxin in sporogenic and asporogenic strains of Bacillus subtilis. J Mol Biol 191:13-22.
80. Weisser J, Truper HG. 1985. Osmoregulation in a new haloalkaliphilic Bacillus from the Wadi Natrun (Egypt). Syst Appl Microbiol 6:7-11.
81. Wirth MC, Georghiou GP, Federici BA. 1997. CytA enables CryIV endotoxins of Bacillus thuringiensis to overcome high levels of CryIV resistance in the mosquito Culex quinquefasciatus. Proc Natl Acad Sci USA 94:10536-10540.
82. Wydro RM, Madira W, Hiramatsu T, Kogut M, Kushner DJ. 1977. Salt-sensitive in vitro protein synthesis by a moderately halophilic bacterium. Nature 269:824-825.
83. Yoshida K, Sen K, Sakai H, Komano T. 1989. Expression of two 130-kDa protein genes of Bacillus thuringiensisvar isrelensis in Bacillus subtilis. Agric Biol Chem 53:3033-3035.
84. Zouari N, Jaoua S. 1999. Production and characterization of metalloproteases synthesized concomitantly with δ-endotoxin by Bacillus thuringiensis subsp. kurstaki strain grown on gruel-based media. Enz Microbial Tech 25:364-371.