Skip to main content
SpringerLink
Log in

Bacillus thuringiensis Genetics and Phages—From Transduction and Sequencing to Recombineering

  • Chapter
  • First Online:
Bacillus thuringiensis Biotechnology

  • 2417 Accesses

Abstract

Experimental mapping of genes was less intensive in the Bacillus cereus group, which includes B. thuringiensis, than in Bacillus subtilis, generally considered as the model for Gram-positive bacteria. Nevertheless the genomic sequencing equalized densities of available gene maps. Moreover, the genes responsible for such complex phenomena like virulence or psychrotolerance could only be identified using the authentic bacteria prone to possess these properties. The new experimental approaches of post-genomic genetics should therefore be considered. Phage-mediated gene transduction and recombineering perspectives for the B. cereus group are reviewed. In combination with new generation sequencing these approaches will constitute the gene identification methodologies in the post-genomics time.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 219.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 279.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ackermann HW (2003) Bacteriophage observations and evolution. Res Microbiol 154(4):245–251

    Article  CAS  Google Scholar 

  • Ackermann HW (2007) 5500 Phages examined in the electron microscope. Arch Virol 152(2):227–243

    Article  CAS  Google Scholar 

  • Ackermann HW, Azizbekyan RR, Bernier RL, de Barjac H, Saindoux S, Valero JR, Yu MX (1995) Phage typing of Bacillus subtilis and B. thuringiensis. Res Microbiol 146(8):643–657

    Article  CAS  Google Scholar 

  • Ahmed R, Sankar-Mistry P, Jackson S, Ackermann HW, Kasatiya SS (1995) Bacillus cereus phage typing as an epidemiological tool in outbreaks of food poisoning. J Clin Microbiol 33(3):636–640

    CAS  Google Scholar 

  • Alcaraz LD, Moreno-Hagelsieb G, Eguiarte LE, Souza V, Herrera-Estrella L, Olmedo G (2010) Understanding the evolutionary relationships and major traits of Bacillus through comparative genomics. BMC Genomics 11:332

    Article  CAS  Google Scholar 

  • Alonso JC, Luder G, Trautner TA (1986) Requirements for the formation of plasmid-transducing particles of Bacillus subtilis bacteriophage SPP1. EMBO J 5(13):3723–3728

    CAS  Google Scholar 

  • Alonso J C, Tavares P, Lurz R, Trautner TA (2006) Bacteriophage SPP1. In: Calendar R (ed) The Bacteriophages, 2nd edn. Oxford University Press, NY, pp 331–349

    Google Scholar 

  • Altenbern RA, Stull HB (1965) Inducible lytic systems in the genus Bacillus. J Gen Microbiol 39:53–62

    Article  CAS  Google Scholar 

  • Amjad M, Castro JM, Sandoval H, Wu JJ, Yang M, Henner DJ, Piggot PJ (1991) An SfiI restriction map of the Bacillus subtilis 168 genome. Gene 101(1):15–21

    Article  CAS  Google Scholar 

  • Anagnostopoulos C, Spizizen J (1961) Requirements for transformation in Bacillus Subtilis. J Bacteriol 81(5):741–746

    CAS  Google Scholar 

  • Anagnostopoulos C, Piggot PJ, Hoch JA (1993) The genetic map of Bacillus subtilis. In: Sonenshein AL, Hoch JA, Losick R (eds) Bacillus subtilis and other Gram-positive bacteria. American Society for Microbiology, Washington, DC, pp 425–461

    Google Scholar 

  • Anderson RM, May RM (1979) Population biology of infectious diseases: Part I. Nature 280(5721):361–367

    Article  CAS  Google Scholar 

  • Anderson RM, May RM (1982) Coevolution of hosts and parasites. Parasitology 85(Pt 2):411–426

    Article  Google Scholar 

  • Auger S, Galleron N, Bidnenko E, Ehrlich SD, Lapidus A, Sorokin A (2008) The genetically remote pathogenic strain NVH391-98 of the Bacillus cereus group is representative of a cluster of thermophilic strains. Appl Environ Microbiol 74(4):1276–1280

    Article  CAS  Google Scholar 

  • Ayora S, Missich R, Mesa P, Lurz R, Yang S, Egelman EH, Alonso JC (2002) Homologous-pairing activity of the Bacillus subtilis bacteriophage SPP1 replication protein G35P. J Biol Chem 277(39):35969–35979

    Article  CAS  Google Scholar 

  • Azevedo V, Alvarez E, Zumstein E, Damiani G, Sgaramella V, Ehrlich SD, Serror P (1993) An ordered collection of Bacillus subtilis DNA segments cloned in yeast artificial chromosomes. Proc Natl Acad Sci USA 90(13):6047–6051

    Article  CAS  Google Scholar 

  • Barbe V, Cruveiller S, Kunst F, Lenoble P, Meurice G, Sekowska A, Vallenet D, Wang T, Moszer I, Medigue C, Danchin A (2009) From a consortium sequence to a unified sequence: the Bacillus subtilis 168 reference genome a decade later. Microbiology 155(Pt 6):1758–1775

    Article  CAS  Google Scholar 

  • Baron F, Cochet MF, Grosset N, Madec MN, Briandet R, Dessaigne S, Chevalier S, Gautier M, Jan S (2007) Isolation and characterization of a psychrotolerant toxin producer, Bacillus weihenstephanensis, in liquid egg products. J Food Prot 70(12):2782–2791

    CAS  Google Scholar 

  • Barsomian GD, Robillard NJ, Thorne CB (1984) Chromosomal mapping of Bacillus thuringiensis by transduction. J Bacteriol 157(3):746–750

    CAS  Google Scholar 

  • Belliveau BH, Trevors JT (1989) Transformation of Bacillus cereus vegetative cells by electroporation. Appl Environ Microbiol 55(6):1649–1652

    CAS  Google Scholar 

  • Biaudet V, Samson F, Anagnostopoulos C, Ehrlich SD, Bessieres P (1996) Computerized genetic map of Bacillus subtilis. Microbiology 142(Pt 10):2669–2729

    Article  CAS  Google Scholar 

  • Bone EJ, Ellar DJ (1989) Transformation of Bacillus thuringiensis by electroporation. FEMS Microbiol Lett 49(2–3):171–177

    Article  CAS  Google Scholar 

  • Bravo A, Alonso JC (1990) The generation of concatemeric plasmid DNA in Bacillus subtilis as a consequence of bacteriophage SPP1 infection. Nucleic Acids Res 18(16):4651–4657

    Article  CAS  Google Scholar 

  • Campbell A (2006) General aspects of lysogeny. In: Calendar R (ed) The bacteriophages, 2nd edn. Oxford University Press, NY, pp 66–73

    Google Scholar 

  • Carlson CR, Kolsto AB (1993) A complete physical map of a Bacillus thuringiensis chromosome. J Bacteriol 175(4):1053–1060

    CAS  Google Scholar 

  • Carlson CR, Gronstad A, Kolsto AB (1992) Physical maps of the genomes of three Bacillus cereus strains. J Bacteriol 174(11):3750–3756

    CAS  Google Scholar 

  • Carlson CR, Johansen T, Kolsto AB (1996) The chromosome map of Bacillus thuringiensis subsp. canadensis HD224 is highly similar to that of the Bacillus cereus type strain ATCC 14579. FEMS Microbiol Lett 141(2–3):163–167

    Article  CAS  Google Scholar 

  • Casjens S, Sampson L, Randall S, Eppler K, Wu H, Petri JB, Schmieger H (1992) Molecular genetic analysis of bacteriophage P22 gene 3 product, a protein involved in the initiation of headful DNA packaging. J Mol Biol 227(4):1086–1099

    Article  CAS  Google Scholar 

  • Casjens SR, Gilcrease EB, Winn-Stapley DA, Schicklmaier P, Schmieger H, Pedulla ML, Ford ME, Houtz JM, Hatfull GF, Hendrix RW (2005) The generalized transducing Salmonella bacteriophage ES18: complete genome sequence and DNA packaging strategy. J Bacteriol 187(3):1091–1104

    Article  CAS  Google Scholar 

  • Challacombe JF, Altherr MR, Xie G, Bhotika SS, Brown N, Bruce D, Campbell CS, Campbell ML, Chen J, Chertkov O, Cleland C, Dimitrijevic M, Doggett NA, Fawcett JJ, Glavina T, Goodwin LA, Green LD, Han CS, Hill KK, Hitchcock P, Jackson PJ, Keim P, Kewalramani AR, Longmire J, Lucas S, Malfatti S, Martinez D, McMurry K, Meincke LJ, Misra M, Moseman BL, Mundt M, Munk AC, Okinaka RT, Parson-Quintana B, Reilly LP, Richardson P, Robinson DL, Saunders E, Tapia R, Tesmer JG, Thayer N, Thompson LS, Tice H, Ticknor LO, Wills PL, Gilna P, Brettin TS (2007) The complete genome sequence of Bacillus thuringiensis Al Hakam. J Bacteriol 189(9):3680–3681

    Article  CAS  Google Scholar 

  • Clements MO, Moir A (1998) Role of the gerI operon of Bacillus cereus 569 in the response of spores to germinants. J Bacteriol 180(24):6729–6735

    CAS  Google Scholar 

  • Collins FS, Weissman SM (1984) Directional cloning of DNA fragments at a large distance from an initial probe: a circularization method. Proc Natl Acad Sci USA 81(21):6812–6816

    Article  CAS  Google Scholar 

  • Cuervo A, Vaney MC, Antson AA, Tavares P, Oliveira L (2007) Structural rearrangements between portal protein subunits are essential for viral DNA translocation. J Biol Chem 282(26):18907–18913

    Article  CAS  Google Scholar 

  • Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97(12):6640–6645

    Article  CAS  Google Scholar 

  • Datta S, Costantino N, Zhou X, Court DL (2008) Identification and analysis of recombineering functions from Gram-negative and Gram-positive bacteria and their phages. Proc Natl Acad Sci USA 105(5):1626–1631

    Article  CAS  Google Scholar 

  • de Lencastre H, Archer LJ (1979) Transducing activity of bacteriophage SPP1. Biochem Biophys Res Commun 86(3):915–919

    Article  CAS  Google Scholar 

  • de Lencastre H, Archer LJ (1980) Characterization of bacteriophage SPP1 transducing particles. J Gen Microbiol 117(2):347–355

    CAS  Google Scholar 

  • de Lencastre H, Archer LJ (1981) Molecular origin of transducing DNA in bacteriophage SPP1. J Gen Microbiol 122(2):345–349

    Google Scholar 

  • Devine KM (1995) The Bacillus subtilis genome project: aims and progress. Trends Biotechnol 13(6):210–216

    Article  CAS  Google Scholar 

  • Didelot X, Barker M, Falush D, Priest FG (2009) Evolution of pathogenicity in the Bacillus cereus group. Syst Appl Microbiol 32(2):81–90

    Article  CAS  Google Scholar 

  • Earl AM, Losick R, Kolter R (2008) Ecology and genomics of Bacillus subtilis. Trends Microbiol 16(6):269–275

    Article  CAS  Google Scholar 

  • Eiserling FA (1967) The structure of Bacillus subtilis bacteriophage PBS 1. J Ultrastruct Res 17(3):342–347

    Article  CAS  Google Scholar 

  • Fagerlund A, Brillard J, Furst R, Guinebretiere MH, Granum PE (2007) Toxin production in a rare and genetically remote cluster of strains of the Bacillus cereus group. BMC Microbiol 7:43

    Article  CAS  Google Scholar 

  • Fang G, Ho C, Qiu Y, Cubas V, Yu Z, Cabau C, Cheung F, Moszer I, Danchin A (2005) Specialized microbial databases for inductive exploration of microbial genome sequences. BMC Genomics 6:14

    Article  CAS  Google Scholar 

  • Ferrari E, Canosi U, Galizzi A, Mazza G (1978) Studies on transduction process by SPP1 phage. J Gen Virol 41(3):563–572

    Article  CAS  Google Scholar 

  • Fleischmann RD, Adams MD, White O, Clayton RA, Kirkness EF, Kerlavage AR, Bult CJ, Tomb JF, Dougherty BA, Merrick JM et al (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269(5223):496–512

    Article  CAS  Google Scholar 

  • Fouts DE, Rasko DA, Cer RZ, Jiang L, Fedorova NB, Shvartsbeyn A, Vamathevan JJ, Tallon L, Althoff R, Arbogast TS, Fadrosh DW, Read TD, Gill SR (2006) Sequencing Bacillus anthracis typing phages gamma and cherry reveals a common ancestry. J Bacteriol 188(9):3402–3408

    Article  CAS  Google Scholar 

  • Fraser CM, Fleischmann RD (1997) Strategies for whole microbial genome sequencing and analysis. Electrophoresis 18(8):1207–1216

    Article  CAS  Google Scholar 

  • Giorno R, Mallozzi M, Bozue J, Moody KS, Slack A, Qiu D, Wang R, Friedlander A, Welkos S, Driks A (2009) Localization and assembly of proteins comprising the outer structures of the Bacillus anthracis spore. Microbiology 155(Pt 4):1133–1145

    Article  CAS  Google Scholar 

  • Groot MN, Nieboer F, Abee T (2008) Enhanced transformation efficiency of recalcitrant Bacillus cereus and Bacillus weihenstephanensis isolates upon in vitro methylation of plasmid DNA. Appl Environ Microbiol 74(24):7817–7820

    Article  CAS  Google Scholar 

  • Guinebretiere MH, Thompson FL, Sorokin A, Normand P, Dawyndt P, Ehling-Schulz M, Svensson B, Sanchis V, Nguyen-The C, Heyndrickx M, De Vos P (2008) Ecological diversification in the Bacillus cereus Group. Environ Microbiol 10(4):851–865

    Article  CAS  Google Scholar 

  • Gusarov II, Kreneva RA, Rybak KV, Podcherniaev DA, Iomantas Iu V, Kolibaba LG, Polanuer BM, Kozlov Iu I, Perumov DA (1997) Primary structure and functional activity of the Bacillus subtilis ribC gene. Mol Biol (Mosk) 31(5):820–825

    CAS  Google Scholar 

  • Hall SD, Kane MF, Kolodner RD (1993) Identification and characterization of the Escherichia coli RecT protein, a protein encoded by the recE region that promotes renaturation of homologous single-stranded DNA. J Bacteriol 175(1):277–287

    CAS  Google Scholar 

  • Hardies SC, Thomas JA, Serwer P (2007) Comparative genomics of Bacillus thuringiensis phage 0305phi8-36: defining patterns of descent in a novel ancient phage lineage. Virol J 4:97

    Article  CAS  Google Scholar 

  • Harwood CR, Wipat A (1996) Sequencing and functional analysis of the genome of Bacillus subtilis strain 168. FEBS Lett 389(1):84–87

    Article  CAS  Google Scholar 

  • Heierson A, Landen R, Boman HG (1983) Transductional mapping of 9 linked chromosomal genes in Bacillus thuringiensis. Mol Gen Genet 192:118–123

    Article  CAS  Google Scholar 

  • Helgason E, Okstad OA, Caugant DA, Johansen HA, Fouet A, Mock M, Hegna I, Kolsto AB (2000a) Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis—one species on the basis of genetic evidence. Appl Environ Microbiol 66(6):2627–2630

    Article  CAS  Google Scholar 

  • Helgason E, Caugant DA, Olsen I, Kolsto AB (2000b) Genetic structure of population of Bacillus cereus and B. thuringiensis isolates associated with periodontitis and other human infections. J Clin Microbiol 38(4):1615–1622

    CAS  Google Scholar 

  • Helgason E, Tourasse NJ, Meisal R, Caugant DA, Kolsto AB (2004) Multilocus sequence typing scheme for bacteria of the Bacillus cereus group. Appl Environ Microbiol 70(1):191–201

    Article  CAS  Google Scholar 

  • Hemphill HE, Whiteley HR (1975) Bacteriophages of Bacillus subtilis. Bacteriol Rev 39(3):257–315

    CAS  Google Scholar 

  • Iida S, Hiestand-Nauer R, Sandmeier H, Lehnherr H, Arber W (1998) Accessory genes in the darA operon of bacteriophage P1 affect antirestriction function, generalized transduction, head morphogenesis, and host cell lysis. Virology 251(1):49–58

    Article  CAS  Google Scholar 

  • Inal JR, Karunakaran V, Burges HD (1990) Isolation and propagation of phages naturally associated with the aizawai variety of Bacillus thuringiensis. J Appl Bacteriol 68(1):17–21

    Article  CAS  Google Scholar 

  • Inal JR, Karunakaran V, Burges HD (1992) Generalised transduction in Bacillus thuringiensis var. aizawai. J Appl Bacteriol 72:87–90

    Article  Google Scholar 

  • Inal JM, Karunakaran V, Jones DR (1996) Bacillus thuringiensis subsp. aizawai generalized transducing phage fHD248: restriction site map and potential for fine-structure chromosomal mapping. Microbiology 142:1409–1416

    Article  CAS  Google Scholar 

  • Isidro A, Henriques AO, Tavares P (2004) The portal protein plays essential roles at different steps of the SPP1 DNA packaging process. Virology 322(2):253–263

    Article  CAS  Google Scholar 

  • Itaya M, Tanaka T (1991) Complete physical map of the Bacillus subtilis 168 chromosome constructed by a gene-directed mutagenesis method. J Mol Biol 220(3):631–648

    Article  CAS  Google Scholar 

  • Ivanova N, Sorokin A, Anderson I, Galleron N, Candelon B, Kapatral V, Bhattacharyya A, Reznik G, Mikhailova N, Lapidus A, Chu L, Mazur M, Goltsman E, Larsen N, D’Souza M, Walunas T, Grechkin Y, Pusch G, Haselkorn R, Fonstein M, Ehrlich SD, Overbeek R, Kyrpides N (2003) Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. Nature 423(6935):87–91

    Article  CAS  Google Scholar 

  • Kanda K, Tan Y, Aizawa K (1989) A novel phage genome integrated into a plasmid in Bacillus thuringiensis strain AF101. J Gen Microbiol 135(11):3035–3041

    CAS  Google Scholar 

  • Kanda K, Kitajima Y, Moriyama Y, Kato F, Murata A (1998) Association of plasmid integrative J7W-1 prophage with Bacillus thuringiensis strains. Acta Virol 42(5):315–318

    CAS  Google Scholar 

  • Kanda K, Takada Y, Kawasaki F, Kato F, Murata A (2000a) Mating in Bacillus thuringiensis can induce plasmid integrative prophage J7W-1. Acta Virol 44(3):189–192

    CAS  Google Scholar 

  • Kanda K, Kayashima T, Kato F, Murata A (2000b) Temperature influences induction of a J7W-1-related phage in Bacillus thuringiensis serovar indiana. Acta Virol 44(3):183–187

    CAS  Google Scholar 

  • Klumpp J, Dorscht J, Lurz R, Bielmann R, Wieland M, Zimmer M, Calendar R, Loessner MJ (2008) The terminally redundant, nonpermuted genome of Listeria bacteriophage A511: a model for the SPO1-like myoviruses of Gram-positive bacteria. J Bacteriol 190(17):5753–5765

    Article  CAS  Google Scholar 

  • Klumpp J, Lavigne R, Loessner MJ, Ackermann HW (2010a) The SPO1-related bacteriophages. Arch Virol 155(10):1547–1561

    Article  CAS  Google Scholar 

  • Klumpp J, Calendar R, Loessner MJ (2010b) Complete nucleotide sequence and molecular characterization of Bacillus phage TP21 and its relatedness to other phages with the same name. Viruses 2:961–971

    Article  CAS  Google Scholar 

  • Koehler TM (2009) Bacillus anthracis physiology and genetics. Mol Aspects Med 30(6):386–396

    Article  CAS  Google Scholar 

  • Kolodner R, Hall SD, Luisi-DeLuca C (1994) Homologous pairing proteins encoded by the Escherichia coli recE and recT genes. Mol Microbiol 11(1):23–30

    Article  CAS  Google Scholar 

  • Kolsto AB, Gronstad A, Oppegaard H (1990) Physical map of the Bacillus cereus chromosome. J Bacteriol 172(7):3821–3825

    CAS  Google Scholar 

  • Kolsto AB, Tourasse NJ, Okstad OA (2009) What sets Bacillus anthracis apart from other Bacillus species? Annu Rev Microbiol 63:451–476

    Article  CAS  Google Scholar 

  • Kufer B, Backhaus H, Schmieger H (1982) The packaging initiation site of phage P22. Analysis of packaging events by transduction. Mol Gen Genet 187(3):510–515

    Article  CAS  Google Scholar 

  • Kunst F, Devine K (1991) The project of sequencing the entire Bacillus subtilis genome. Res Microbiol 142(7–8):905–912

    Article  CAS  Google Scholar 

  • Kunst F, Vassarotti A, Danchin A (1995) Organization of the European Bacillus subtilis genome sequencing project. Microbiology 141(Pt 2):249–255

    Article  CAS  Google Scholar 

  • Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G, Azevedo V, Bertero MG, Bessieres P, Bolotin A, Borchert S, Borriss R, Boursier L, Brans A, Braun M, Brignell SC, Bron S, Brouillet S, Bruschi CV, Caldwell B, Capuano V, Carter NM, Choi SK, Codani JJ, Connerton IF, Danchin A et al (1997) The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390(6657):249–256

    Article  CAS  Google Scholar 

  • Kuzminov A (1999) Recombinational repair of DNA damage in Escherichia coli and bacteriophage lambda. Microbiol Mol Biol Rev 63(4):751–813

    CAS  Google Scholar 

  • Landen R, Heierson A, Boman HG (1981) A phage for generalized transduction in Bacillus thuringiensis and mapping of four genes for antibiotic resistance. J Gen Microbiol 123:49–59

    Google Scholar 

  • Lapidus A, Goltsman E, Auger S, Galleron N, Segurens B, Dossat C, Land ML, Broussolle V, Brillard J, Guinebretiere MH, Sanchis V, Nguen-The C, Lereclus D, Richardson P, Wincker P, Weissenbach J, Ehrlich SD, Sorokin A (2008) Extending the Bacillus cereus group genomics to putative food-borne pathogens of different toxicity. Chem Biol Interact 171(2):236–249

    Article  CAS  Google Scholar 

  • Lebedev AA, Krause MH, Isidro AL, Vagin AA, Orlova EV, Turner J, Dodson EJ, Tavares P, Antson AA (2007) Structural framework for DNA translocation via the viral portal protein. EMBO J 26(7):1984–1994

    Article  CAS  Google Scholar 

  • Lecadet MM, Blondel MO, Ribier J (1980) Generalized transduction in Bacillus thuringiensis var. berliner 1715 using bacteriophage CP-54Ber. J Gen Microbiol 121(1):203–212

    CAS  Google Scholar 

  • Lechner S, Mayr R, Francis KP, Pruss BM, Kaplan T, Wiessner-Gunkel E, Stewart GS, Scherer S (1998) Bacillus weihenstephanensis sp. nov. is a new psychrotolerant species of the Bacillus cereus group. Int J Syst Bacteriol 48(Pt 4):1373–1382

    Article  CAS  Google Scholar 

  • Lennox ES (1955) Transduction of linked genetic characters of the host by bacteriophage P1. Virology 1(2):190–206

    Article  CAS  Google Scholar 

  • Lereclus D, Arantes O, Chaufaux J, Lecadet M (1989) Transformation and expression of a cloned delta-endotoxin gene in Bacillus thuringiensis. FEMS Microbiol Lett 51(1):211–217

    CAS  Google Scholar 

  • Lhuillier S, Gallopin M, Gilquin B, Brasiles S, Lancelot N, Letellier G, Gilles M, Dethan G, Orlova EV, Couprie J, Tavares P, Zinn-Justin S (2009) Structure of bacteriophage SPP1 head-to-tail connection reveals mechanism for viral DNA gating. Proc Natl Acad Sci USA 106(21):8507–8512

    Article  CAS  Google Scholar 

  • Li Z, Karakousis G, Chiu SK, Reddy G, Radding CM (1998) The beta protein of phage lambda promotes strand exchange. J Mol Biol 276(4):733–744

    Article  CAS  Google Scholar 

  • Lopes A, Amarir-Bouhram J, Faure G, Petit MA, Guerois R (2010) Detection of novel recombinases in bacteriophage genomes unveils Rad52, Rad51 and Gp2.5 remote homologs. Nucleic Acids Res 38(12):3952–3962

    Article  CAS  Google Scholar 

  • Lovett PS, Young FE (1970) Genetic analysis in Bacillus pumilus by PBSI-mediated transduction. J Bacteriol 101(2):603–608

    CAS  Google Scholar 

  • Lovett PS, Bramucci D, Bramucci MG, Burdick BD (1974) Some properties of the PBP1 transduction system in Bacillus pumilus. J Virol 13(1):81–84

    CAS  Google Scholar 

  • Macaluso A, Mettus AM (1991) Efficient transformation of Bacillus thuringiensis requires nonmethylated plasmid DNA. J Bacteriol 173(3):1353–1356

    CAS  Google Scholar 

  • Markowitz VM, Chen IM, Palaniappan K, Chu K, Szeto E, Grechkin Y, Ratner A, Anderson I, Lykidis A, Mavromatis K, Ivanova NN, Kyrpides NC (2010) The integrated microbial genomes system: an expanding comparative analysis resource. Nucleic Acids Res 38(Database issue):D382–D390

    Article  CAS  Google Scholar 

  • Martinez-Jimenez MI, Alonso JC, Ayora S (2005) Bacillus subtilis bacteriophage SPP1-encoded gene 34.1 product is a recombination-dependent DNA replication protein. J Mol Biol 351(5):1007–1019

    Article  CAS  Google Scholar 

  • Martinsohn JT, Radman M, Petit MA (2008) The lambda red proteins promote efficient recombination between diverged sequences: implications for bacteriophage genome mosaicism. PLoS Genet 4(5):e1000065

    Article  CAS  Google Scholar 

  • Masson L, Prefontaine G, Brousseau R (1989) Transformation of Bacillus thuringiensis vegetative cells by electroporation. FEMS Microbiol Lett 51(3):273–277

    Article  CAS  Google Scholar 

  • Medigue C, Moszer I (2007) Annotation, comparison and databases for hundreds of bacterial genomes. Res Microbiol 158(10):724–736

    Article  CAS  Google Scholar 

  • Metzker ML (2009) Sequencing technologies—the next generation. Nat Rev Genet 11(1):31–46

    Article  CAS  Google Scholar 

  • Minakhin L, Semenova E, Liu J, Vasilov A, Severinova E, Gabisonia T, Inman R, Mushegian A, Severinov K (2005) Genome sequence and gene expression of Bacillus anthracis bacteriophage Fah. J Mol Biol 354(1):1–15

    Article  CAS  Google Scholar 

  • Mironov AS, Gusarov I, Rafikov R, Lopez LE, Shatalin K, Kreneva RA, Perumov DA, Nudler E (2002) Sensing small molecules by nascent RNA: a mechanism to control transcription in bacteria. Cell 111(5):747–756

    Article  CAS  Google Scholar 

  • Mock M, Fouet A (2001) Anthrax. Annu Rev Microbiol 55:647–671

    Article  CAS  Google Scholar 

  • Moody KL, Driks A, Rother GL, Cote CK, Brueggemann EE, Hines HB, Friedlander AM, Bozue J (2010) Processing, assembly and localization of a Bacillus anthracis spore protein. Microbiology 156(Pt 1):174–183

    Article  CAS  Google Scholar 

  • Moszer I, Glaser P, Danchin A (1995) SubtiList: a relational database for the Bacillus subtilis genome. Microbiology 141(Pt 2):261–268

    Article  CAS  Google Scholar 

  • Muniyappa K, Radding CM (1986) The homologous recombination system of phage lambda. Pairing activities of beta protein. J Biol Chem 261(16):7472–7478

    CAS  Google Scholar 

  • Muyrers JP, Zhang Y, Testa G, Stewart AF (1999) Rapid modification of bacterial artificial chromosomes by ET-recombination. Nucleic Acids Res 27(6):1555–1557

    Article  CAS  Google Scholar 

  • Muyrers JP, Zhang Y, Stewart AF (2001) Techniques: recombinogenic engineering—new options for cloning and manipulating DNA. Trends Biochem Sci 26(5):325–331

    Article  CAS  Google Scholar 

  • Oliveira L, Cuervo A, Tavares P (2010) Direct interaction of the bacteriophage SPP1 packaging ATPase with the portal protein. J Biol Chem 285(10):7366–7373

    Article  CAS  Google Scholar 

  • Orlova EV, Gowen B, Droge A, Stiege A, Weise F, Lurz R, van Heel M, Tavares P (2003) Structure of a viral DNA gatekeeper at 10 A resolution by cryo-electron microscopy. EMBO J 22(6):1255–1262

    Article  CAS  Google Scholar 

  • Peng D, Luo Y, Guo S, Zeng H, Ju S, Yu Z, Sun M (2009) Elaboration of an electroporation protocol for large plasmids and wild-type strains of Bacillus thuringiensis. J Appl Microbiol 106(6):1849–1858

    Article  CAS  Google Scholar 

  • Perlak FJ, Mendelsohn CL, Thorne CB (1979) Converting bacteriophage for sporulation and crystal formation in Bacillus thuringiensis. J Bacteriol 140(2):699–706

    CAS  Google Scholar 

  • Piggot PJ, Hoch JA (1985) Revised genetic linkage map of Bacillus subtilis. Microbiol Rev 49(2):158–179

    CAS  Google Scholar 

  • Priest FG, Barker M, Baillie LW, Holmes EC, Maiden MC (2004) Population structure and evolution of the Bacillus cereus group. J Bacteriol 186(23):7959–7970

    Article  CAS  Google Scholar 

  • Raj AS, Raj AY, Schmieger H (1974) Phage genes involved in the formation generalized transducing particles in Salmonella—Phage P22. Mol Gen Genet 135(2):175–184

    Article  CAS  Google Scholar 

  • Rao VB, Feiss M (2008) The bacteriophage DNA packaging motor. Annu Rev Genet 42:647–681

    Article  CAS  Google Scholar 

  • Rasko DA, Altherr MR, Han CS, Ravel J (2005) Genomics of the Bacillus cereus group of organisms. FEMS Microbiol Rev 29(2):303–329

    CAS  Google Scholar 

  • Ravantti JJ, Gaidelyte A, Bamford DH, Bamford JK (2003) Comparative analysis of bacterial viruses Bam35, infecting a gram-positive host, and PRD1, infecting gram-negative hosts, demonstrates a viral lineage. Virology 313(2):401–414

    Article  CAS  Google Scholar 

  • Read TD, Peterson SN, Tourasse N, Baillie LW, Paulsen IT, Nelson KE, Tettelin H, Fouts DE, Eisen JA, Gill SR, Holtzapple EK, Okstad OA, Helgason E, Rilstone J, Wu M, Kolonay JF, Beanan MJ, Dodson RJ, Brinkac LM, Gwinn M, DeBoy RT, Madpu R, Daugherty SC, Durkin AS, Haft DH, Nelson WC, Peterson JD, Pop M, Khouri HM, Radune D, Benton JL, Mahamoud Y, Jiang L, Hance IR, Weidman JF, Berry KJ, Plaut RD, Wolf AM, Watkins KL, Nierman WC, Hazen A, Cline R, Redmond C, Thwaite JE, White O, Salzberg SL, Thomason B, Friedlander AM, Koehler TM, Hanna PC, Kolsto AB, Fraser CM (2003) The genome sequence of Bacillus anthracis Ames and comparison to closely related bacteria. Nature 423(6935):81–86

    Article  CAS  Google Scholar 

  • Rice EW, Rose LJ, Johnson CH, Boczek LA, Arduino MJ, Reasoner DJ (2004) Boiling and Bacillus spores. Emerg Infect Dis 10(10):1887–1888

    Article  Google Scholar 

  • Rivolta C, Pagni M (1999) Genetic and physical maps of the Bacillus subtilis chromosome. Genetics 151(4):1239–1244

    CAS  Google Scholar 

  • Ruhfel RE, Robillard NJ, Thorne CB (1984) Interspecies transduction of plasmids among Bacillus anthracis, B. cereus, and B. thuringiensis. J Bacteriol 157(3):708–711

    CAS  Google Scholar 

  • Sastalla I, Rosovitz MJ, Leppla SH (2010) Accidental selection and intentional restoration of sporulation-deficient Bacillus anthracis mutants. Appl Environ Microbiol 76(18):6318–6321

    Article  CAS  Google Scholar 

  • Sauer U, Hatzimanikatis V, Bailey JE, Hochuli M, Szyperski T, Wuthrich K (1997) Metabolic fluxes in riboflavin-producing Bacillus subtilis. Nat Biotechnol 15(5):448–452

    Article  CAS  Google Scholar 

  • Sawitzke JA, Thomason LC, Costantino N, Bubunenko M, Datta S, Court DL (2007) Recombineering: in vivo genetic engineering in E. coli, S. enterica, and beyond. Methods Enzymol 421:171–199

    Article  CAS  Google Scholar 

  • Schmieger H (1972) Phage P22-mutants with increased or decreased transduction abilities. Mol Gen Genet 119(1):75–88

    Article  CAS  Google Scholar 

  • Schmieger H, Backhaus H (1976) Altered cotransduction frequencies exhibited by HT-mutants of Salmonella-phage P22. Mol Gen Genet 143(3):307–309

    Article  CAS  Google Scholar 

  • Schmieger H, Buch U (1975) Appearance of transducing particles and the fate of host DNA after infection of Salmonella typhimurium with P22-mutants with increased transducing ability (HT-mutants). Mol Gen Genet 140(2):111–122

    Article  CAS  Google Scholar 

  • Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, Feitelson J, Zeigler DR, Dean DH (1998) Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol Rev 62(3):775–806

    CAS  Google Scholar 

  • Schuch R, Fischetti VA (2006) Detailed genomic analysis of the Wbeta and gamma phages infecting Bacillus anthracis: implications for evolution of environmental fitness and antibiotic resistance. J Bacteriol 188(8):3037–3051

    Article  CAS  Google Scholar 

  • Schuch R, Fischetti VA (2009) The secret life of the anthrax agent Bacillus anthracis: bacteriophage-mediated ecological adaptations. PLoS One 4(8):e6532

    Article  CAS  Google Scholar 

  • Schurter W, Geiser M, Mathe D (1989) Efficient transformation of Bacillus thuringiensis and B. cereus via electroporation: transformation of acrystalliferous strains with a cloned delta-endotoxin gene. Mol Gen Genet 218(1):177–181

    Article  CAS  Google Scholar 

  • Shelton AM, Zhao JZ, Roush RT (2002) Economic, ecological, food safety, and social consequences of the deployment of bt transgenic plants. Annu Rev Entomol 47:845–881

    Article  CAS  Google Scholar 

  • Smeesters PR, Dreze PA, Bousbata S, Parikka KJ, Timmery S, Hu X, Perez-Morga D, Deghorain M, Toussaint A, Mahillon J, Van Melderen L (2011) Characterization of a novel temperate phage originating from a cereulide-producing Bacillus cereus strain. Res Microbiol 162(4):446–459

    Article  CAS  Google Scholar 

  • Sorokin A, Candelon B, Guilloux K, Galleron N, Wackerow-Kouzova N, Ehrlich SD, Bourguet D, Sanchis V (2006) Multiple-locus sequence typing analysis of Bacillus cereus and Bacillus thuringiensis reveals separate clustering and a distinct population structure of psychrotrophic strains. Appl Environ Microbiol 72(2):1569–1578

    Article  CAS  Google Scholar 

  • Sozhamannan S, Chute MD, McAfee FD, Fouts DE, Akmal A, Galloway DR, Mateczun A, Baillie LW, Read TD (2006) The Bacillus anthracis chromosome contains four conserved, excision-proficient, putative prophages. BMC Microbiol 6:34

    Article  CAS  Google Scholar 

  • Sozhamannan S, McKinstry M, Lentz SM, Jalasvuori M, McAfee F, Smith A, Dabbs J, Ackermann HW, Bamford JK, Mateczun A, Read TD (2008) Molecular characterization of a variant of Bacillus anthracis-specific phage AP50 with improved bacteriolytic activity. Appl Environ Microbiol 74(21):6792–6796

    Article  CAS  Google Scholar 

  • Srivatsan A, Han Y, Peng J, Tehranchi AK, Gibbs R, Wang JD, Chen R (2008) High-precision, whole-genome sequencing of laboratory strains facilitates genetic studies. PLoS Genet 4(8):e1000139

    Article  CAS  Google Scholar 

  • Stahl FW (1998) Recombination in phage lambda: one geneticist’s historical perspective. Gene 223(1–2):95–102

    Article  CAS  Google Scholar 

  • Stenfors Arnesen LP, Fagerlund A, Granum PE (2008) From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol Rev 32(4):579–606

    Article  CAS  Google Scholar 

  • Stenfors LP, Mayr R, Scherer S, Granum PE (2002) Pathogenic potential of fifty Bacillus weihenstephanensis strains. FEMS Microbiol Lett 215(1):47–51

    Article  CAS  Google Scholar 

  • Sternberg N (1990) Bacteriophage P1 cloning system for the isolation, amplification, and recovery of DNA fragments as large as 100 kilobase pairs. Proc Natl Acad Sci USA 87(1):103–107

    Article  CAS  Google Scholar 

  • Stewart CR, Casjens SR, Cresawn SG, Houtz JM, Smith AL, Ford ME, Peebles CL, Hatfull GF, Hendrix RW, Huang WM, Pedulla ML (2009) The genome of Bacillus subtilis bacteriophage SPO1. J Mol Biol 388(1):48–70

    Article  CAS  Google Scholar 

  • Stromsten NJ, Benson SD, Burnett RM, Bamford DH, Bamford JK (2003) The Bacillus thuringiensis linear double-stranded DNA phage Bam35, which is highly similar to the Bacillus cereus linear plasmid pBClin15, has a prophage state. J Bacteriol 185(23):6985–6989

    Article  CAS  Google Scholar 

  • Susskind MM, Botstein D (1978) Molecular genetics of bacteriophage P22. Microbiol Rev 42(2):385–413

    CAS  Google Scholar 

  • Swingle B, Markel E, Costantino N, Bubunenko MG, Cartinhour S, Court DL (2010) Oligonucleotide recombination in Gram-negative bacteria. Mol Microbiol 75(1):138–148

    Article  CAS  Google Scholar 

  • Takahashi I (1961) Genetic transduction in Bacillus subtilis. Biochem Biophys Res Commun 5:171–175

    Article  CAS  Google Scholar 

  • Thomason LC, Costantino N, Court DL (2007) E. coli genome manipulation by P1 transduction. In: Ausubel FM et al (eds) Current protocols in molecular biology, Chapter 1:Unit 1 17

    Google Scholar 

  • Thorne CB (1962) Transduction in Bacillus subtilis. J Bacteriol 83:106–111

    CAS  Google Scholar 

  • Thorne CB (1968a) Transduction in Bacillus cereus and Bacillus anthracis. Bacteriol Rev 32(4 Pt 1):358–361

    CAS  Google Scholar 

  • Thorne CB (1968b) Transducing bacteriophage for Bacillus cereus. J Virol 2(7):657–662

    CAS  Google Scholar 

  • Thorne CB (1978) Transduction in Bacillus thuringiensis. Appl Environ Microbiol 35(6):1109–1115

    CAS  Google Scholar 

  • Tosato V, Bruschi CV (2004) Knowledge of the Bacillus subtilis genome: impacts on fundamental science and biotechnology. Appl Microbiol Biotechnol 64(1):1–6

    Article  CAS  Google Scholar 

  • Tourasse NJ, Kolsto AB (2007) SuperCAT: a supertree database for combined and integrative multilocus sequence typing analysis of the Bacillus cereus group of bacteria (including B. cereus, B. anthracis and B. thuringiensis). Nucleic Acids Res

    Google Scholar 

  • Tourasse NJ, Helgason E, Klevan A, Sylvestre P, Moya M, Haustant M, Okstad OA, Fouet A, Mock M, Kolsto AB (2010a) Extended and global phylogenetic view of the Bacillus cereus group population by combination of MLST, AFLP, and MLEE genotyping data. Food Microbiol 28(2):236–244

    Article  Google Scholar 

  • Tourasse NJ, Okstad OA, Kolsto AB (2010b) HyperCAT: an extension of the SuperCAT database for global multi-scheme and multi-datatype phylogenetic analysis of the Bacillus cereus group population. Database (Oxford) 2010:baq017

    Google Scholar 

  • Turgeon N, Laflamme C, Ho J, Duchaine C (2006) Elaboration of an electroporation protocol for Bacillus cereus ATCC 14579. J Microbiol Methods 67(3):543–548

    Article  CAS  Google Scholar 

  • Tye BK, Chan RK, Botstein D (1974) Packaging of an oversize transducing genome by Salmonella phage P22. J Mol Biol 85(4):485–500

    Article  CAS  Google Scholar 

  • Tye BK, Huberman JA, Botstein D (1974) Non-random circular permutation of phage P22 DNA. J Mol Biol 85(4):501–528

    Article  CAS  Google Scholar 

  • Tyeryar FJ Jr, Taylor MJ, Lawton WD, Goldberg ID (1969) Cotransduction and cotransformation of genetic markers in Bacillus subtilis and Bacillus licheniformis. J Bacteriol 100(2):1027–1036

    Google Scholar 

  • Van Arsdell SW, Perkins JB, Yocum RR, Luan L, Howitt CL, Chatterjee NP, Pero JG (2005) Removing a bottleneck in the Bacillus subtilis biotin pathway: bioA utilizes lysine rather than S-adenosylmethionine as the amino donor in the KAPA-to-DAPA reaction. Biotechnol Bioeng 91(1):75–83

    Article  CAS  Google Scholar 

  • Vary P (1993) The genetic map of Bacillus megaterium. In: Sonenshein AL, Hoch JA, Losick R (eds) Bacillus subtilis and other Gram-positive bacteria. American Society for Microbiology, Washington, DC, pp 475–481

    Google Scholar 

  • Vellani TS, Myers RS (2003) Bacteriophage SPP1 Chu is an alkaline exonuclease in the SynExo family of viral two-component recombinases. J Bacteriol 185(8):2465–2474

    Article  CAS  Google Scholar 

  • Verheust C, Jensen G, Mahillon J (2003) pGIL01, a linear tectiviral plasmid prophage originating from Bacillus thuringiensis serovar israelensis. Microbiology 149(Pt 8):2083–2092

    Article  CAS  Google Scholar 

  • Verheust C, Fornelos N, Mahillon J (2005) GIL16, a new gram-positive tectiviral phage related to the Bacillus thuringiensis GIL01 and the Bacillus cereus pBClin15 elements. J Bacteriol 187(6):1966–1973

    Article  CAS  Google Scholar 

  • Wall JD, Harriman PD (1974) Phage P1 mutants with altered transducing abilities for Escherichia coli. Virology 59(2):532–544

    Article  CAS  Google Scholar 

  • Walter TM, Aronson AI (1991) Transduction of certain genes by an autonomously replicating Bacillus thuringiensis phage. Appl Environ Microbiol 57(4):1000–1005

    CAS  Google Scholar 

  • Weigel C, Seitz H (2006) Bacteriophage replication modules. FEMS Microbiol Rev 30(3):321–381

    Article  CAS  Google Scholar 

  • Wu SC, Wong SL (2002) Engineering of a Bacillus subtilis strain with adjustable levels of intracellular biotin for secretory production of functional streptavidin. Appl Environ Microbiol 68(3):1102–1108

    Article  CAS  Google Scholar 

  • Yamagishi H, Takahashi I (1968) Transducing particles of PBS 1. Virology 36(4):639–645

    Article  CAS  Google Scholar 

  • Yelton DB, Thorne CB (1970) Transduction in Bacillus cereus by each of two bacteriophages. J Bacteriol 102(2):573–579

    CAS  Google Scholar 

  • Yelton DB, Thorne CB (1971) Comparison of Bacillus cereus bacteriophages CP-51 and CP-53. J Virol 8(2):242–253

    CAS  Google Scholar 

  • Yu D, Ellis HM, Lee EC, Jenkins NA, Copeland NG, Court DL (2000) An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci USA 97(11):5978–5983

    Article  CAS  Google Scholar 

  • Yu D, Sawitzke JA, Ellis H, Court DL (2003) Recombineering with overlapping single-stranded DNA oligonucleotides: testing a recombination intermediate. Proc Natl Acad Sci USA 100(12):7207–7212

    Article  CAS  Google Scholar 

  • Zahler SA (ed) (1982) Specialized transduction in Bacillus subtilis, vol 1. The molecular biology of the Bacilli. Academic Press, London

    Google Scholar 

  • Zhang Y, Buchholz F, Muyrers JP, Stewart AF (1998) A new logic for DNA engineering using recombination in Escherichia coli. Nat Genet 20(2):123–128

    Article  CAS  Google Scholar 

  • Zhang Y, Muyrers JP, Testa G, Stewart AF (2000) DNA cloning by homologous recombination in Escherichia coli. Nat Biotechnol 18(12):1314–1317

    Article  CAS  Google Scholar 

  • Zhu Y, Shang H, Zhu Q, Ji F, Wang P, Fu J, Deng Y, Xu C, Ye W, Zheng J, Zhu L, Ruan L, Peng D, Sun M (2011) Complete genome sequence of Bacillus thuringiensis serovar finitimus strain YBT-020. J Bacteriol 193(9):2379–2380

    Article  CAS  Google Scholar 

  • Zinder ND, Lederberg J (1952) Genetic exchange in Salmonella. J Bacteriol 64(5):679–699

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Genome Analysis Team ANALGEN, UMR1319 MICALIS, Centre de Recherche de Jouy-en-Josas, Institut National de la Recherche Agronomique (INRA), bat. 440, Domaine de Vilvert, 78352, Jouy en Josas cedex, France

    Dr. Alexei Sorokin

Authors
  1. Dr. Alexei Sorokin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexei Sorokin .

Editor information

Editors and Affiliations

  1. Autónoma de Puebla, Facultad de Ciencias Químicas, Benemérita Universidad, Blv. 14 sur y Av. San Claudio, Puebla, 72570, Mexico

    Estibaliz Sansinenea

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Sorokin, A. (2012). Bacillus thuringiensis Genetics and Phages—From Transduction and Sequencing to Recombineering. In: Sansinenea, E. (eds) Bacillus thuringiensis Biotechnology. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-3021-2_7

Download citation

Publish with us

Policies and ethics

Search

Navigation