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What renders Bacilli genetically competent? A gaze beyond the model organism

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Abstract

Natural genetic competence enables bacteria to take in and establish exogenously supplied DNA and thus constitutes a valuable tool for strain improvement. Extensively studied in the Gram-positive model organism Bacillus subtilis genetic competence has indeed proven successful for genetic manipulation aiming at enhancement of handling, yield, and biosafety. The majority of Bacilli, particularly those relevant for industrial application, do not or only poorly develop genetic competence, although rather homologous DNA-uptake machineries are routinely encoded. Establishing the competent state solely due to high cell densities (quorum sensing dependency) appears to be restricted to the model organism, in which the small signalling peptide ComS initiates the regulatory pathway that ultimately leads to the expression of all genes necessary for reaching the competent state. Agreeing with the lack of a functional ComS peptide, competence-mediated transformation of other Bacilli depends on nutrient exhaustion rather than cell density. Genetically, competent strains of the model organism B. subtilis, cultivated for a long time and selected for laboratory purposes, display probably not least to such selection a point mutation in the promoter of a regulatory gene that favors competence development whereas the wild-type progenitor only poorly displays genetic competence. Consistent with competence being a matter of deregulation, all strains of Bacillus licheniformis displaying efficient DNA uptake were found to carry mutations in regulator genes, which are responsible for their genetic competence. Thus, strain-specific genetic equipment and regulation as well as the proven role of domestication for the well-established laboratory strains ought to be considered when attempting to broaden the applicability of competence as a genetic tool for strains other than the model organism.

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References

  • Aceves-Diez AE, Robles-Burgueno R, de la Torre M (2007) SKPDT is a signaling peptide that stimulates sporulation and cry1Aa expression in Bacillus thuringiensis but not in Bacillus subtilis. Appl Microbiol Biotechnol 76(1):203–209

    CAS  PubMed  Google Scholar 

  • Albano M, Smits WK, Ho LT, Kraigher B, Mandic-Mulec I, Kuipers OP, Dubnau D (2005) The Rok protein of Bacillus subtilis represses genes for cell surface and extracellular functions. J Bacteriol 187(6):2010–2019

    CAS  PubMed Central  PubMed  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

    PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ashikaga S, Nanamiya H, Ohashi Y, Kawamura F (2000) Natural genetic competence in Bacillus subtilis natto OK2. J Bacteriol 182(9):2411–2415

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bacon Schneider K, Palmer TM, Grossman AD (2002) Characterization of comQ and comX, two genes required for production of ComX pheromone in Bacillus subtilis. J Bacteriol 184(2):410–419

    PubMed  Google Scholar 

  • Berka R, Maranta M, Tang M, Cherry B (2010) Methods of obtaining genetic competence in Bacillus cells. USA Patent, Feb. 4, 2010

  • Biedendieck R, Borgmeier C, Bunk B, Stammen S, Scherling C, Meinhardt F, Wittmann C, Jahn D (2011) Systems biology of recombinant protein production using Bacillus megaterium. Methods Enzymol 500:165–195

    CAS  PubMed  Google Scholar 

  • Bott KF, Wilson GA (1967) Development of competence in the Bacillus subtilis transformation system. J Bacteriol 94(3):562–570

    CAS  PubMed Central  PubMed  Google Scholar 

  • Briley K Jr, Prepiak P, Dias MJ, Hahn J, Dubnau D (2011) Maf acts downstream of ComGA to arrest cell division in competent cells of B. subtilis. Mol Microbiol 81(1):23–39

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen I, Dubnau D (2004) DNA uptake during bacterial transformation. Nat Rev Microbiol 2(3):241–249

    CAS  PubMed  Google Scholar 

  • Chen I, Christie PJ, Dubnau D (2005) The ins and outs of DNA transfer in bacteria. Science 310(5753):1456–1460

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen XH, Koumoutsi A, Scholz R, Eisenreich A, Schneider K, Heinemeyer I, Morgenstern B, Voss B, Hess WR, Reva O, Junge H, Voigt B, Jungblut PR, Vater J, Sussmuth R, Liesegang H, Strittmatter A, Gottschalk G, Borriss R (2007) Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nat Biotechnol 25(9):1007–1014

    CAS  PubMed  Google Scholar 

  • Chung YS, Dubnau D (1995) ComC is required for the processing and translocation of ComGC, a pilin-like competence protein of Bacillus subtilis. Mol Microbiol 15(3):543–551

    CAS  PubMed  Google Scholar 

  • Chung YS, Dubnau D (1998) All seven comG open reading frames are required for DNA binding during transformation of competent Bacillus subtilis. J Bacteriol 180(1):41–45

    CAS  PubMed Central  PubMed  Google Scholar 

  • Comella N, Grossman AD (2005) Conservation of genes and processes controlled by the quorum response in bacteria: characterization of genes controlled by the quorum-sensing transcription factor ComA in Bacillus subtilis. Mol Microbiol 57(4):1159–1174

    CAS  PubMed  Google Scholar 

  • Core L, Perego M (2003) TPR-mediated interaction of RapC with ComA inhibits response regulator-DNA binding for competence development in Bacillus subtilis. Mol Microbiol 49(6):1509–1522

    CAS  PubMed  Google Scholar 

  • Dahl MK, Msadek T, Kunst F, Rapoport G (1992) The phosphorylation state of the DegU response regulator acts as a molecular switch allowing either degradative enzyme synthesis or expression of genetic competence in Bacillus subtilis. J Biol Chem 267(20):14509–14514

    CAS  PubMed  Google Scholar 

  • Deng X, Tian Y, Niu Q, Xu X, Shi H, Zhang H, Liang L, Zhang K, Huang X (2013) The ComP-ComA quorum system is essential for "Trojan horse" like pathogenesis in Bacillus nematocida. PLoS One 8(10):e76920

    CAS  PubMed Central  PubMed  Google Scholar 

  • D'Souza C, Nakano MM, Zuber P (1994) Identification of comS, a gene of the srfA operon that regulates the establishment of genetic competence in Bacillus subtilis. Proc Natl Acad Sci U S A 91(20):9397–9401

    PubMed Central  PubMed  Google Scholar 

  • D'Souza C, Nakano MM, Frisby DL, Zuber P (1995) Translation of the open reading frame encoded by comS, a gene of the srf operon, is necessary for the development of genetic competence, but not surfactin biosynthesis, in Bacillus subtilis. J Bacteriol 177(14):4144–4148

    PubMed Central  PubMed  Google Scholar 

  • Dubnau D (1999) DNA uptake in bacteria. Annu Rev Microbiol 53:217–244

    CAS  PubMed  Google Scholar 

  • Dubnau D, Cirigliano C (1972) Fate of transforming DNA following uptake by competent Bacillus subtilis. IV. The endwise attachment and uptake of transforming DNA. J Mol Biol 64(1):31–46

    CAS  PubMed  Google Scholar 

  • Dubnau D, Provvedi R (2000) Internalizing DNA. Res Microbiol 151(6):475–480

    CAS  PubMed  Google Scholar 

  • Duitman EH, Wyczawski D, Boven LG, Venema G, Kuipers OP, Hamoen LW (2007) Novel methods for genetic transformation of natural Bacillus subtilis isolates used to study the regulation of the mycosubtilin and surfactin synthetases. Appl Environ Microbiol 73(11):3490–3496

    CAS  PubMed Central  PubMed  Google Scholar 

  • Eppinger M, Bunk B, Johns MA, Edirisinghe JN, Kutumbaka KK, Koenig SS, Creasy HH, Rosovitz MJ, Riley DR, Daugherty S, Martin M, Elbourne LD, Paulsen I, Biedendieck R, Braun C, Grayburn S, Dhingra S, Lukyanchuk V, Ball B, Ul-Qamar R, Seibel J, Bremer E, Jahn D, Ravel J, Vary PS (2011) Genome sequences of the biotechnologically important Bacillus megaterium strains QM B1551 and DSM319. J Bacteriol 193(16):4199–4213

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fedhila S, Msadek T, Nel P, Lereclus D (2002) Distinct clpP genes control specific adaptive responses in Bacillus thuringiensis. J Bacteriol 184(20):5554–5562

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gwinn DD, Thorne CB (1964) Transformation of Bacillus licheniformis. J Bacteriol 87:519–526

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hahn J, Dubnau D (1991) Growth stage signal transduction and the requirements for srfA induction in development of competence. J Bacteriol 173(22):7275–7282

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hahn J, Albano M, Dubnau D (1987) Isolation and characterization of Tn917lac-generated competence mutants of Bacillus subtilis. J Bacteriol 169(7):3104–3109

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hahn J, Inamine G, Kozlov Y, Dubnau D (1993) Characterization of comE, a late competence operon of Bacillus subtilis required for the binding and uptake of transforming DNA. Mol Microbiol 10(1):99–111

    CAS  PubMed  Google Scholar 

  • Hahn J, Kong L, Dubnau D (1994) The regulation of competence transcription factor synthesis constitutes a critical control point in the regulation of competence in Bacillus subtilis. J Bacteriol 176(18):5753–5761

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hahn J, Bylund J, Haines M, Higgins M, Dubnau D (1995a) Inactivation of mecA prevents recovery from the competent state and interferes with cell division and the partitioning of nucleoids in Bacillus subtilis. Mol Microbiol 18(4):755–767

    CAS  PubMed  Google Scholar 

  • Hahn J, Roggiani M, Dubnau D (1995b) The major role of Spo0A in genetic competence is to downregulate abrB, an essential competence gene. J Bacteriol 177(12):3601–3605

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hahn J, Maier B, Haijema BJ, Sheetz M, Dubnau D (2005) Transformation proteins and DNA uptake localize to the cell poles in Bacillus subtilis. Cell 122(1):59–71

    CAS  PubMed  Google Scholar 

  • Haijema BJ, Hamoen LW, Kooistra J, Venema G, van Sinderen D (1995) Expression of the ATP-dependent deoxyribonuclease of Bacillus subtilis is under competence-mediated control. Mol Microbiol 15(2):203–211

    CAS  PubMed  Google Scholar 

  • Haijema BJ, van Sinderen D, Winterling K, Kooistra J, Venema G, Hamoen LW (1996) Regulated expression of the dinR and recA genes during competence development and SOS induction in Bacillus subtilis. Mol Microbiol 22(1):75–85

    CAS  PubMed  Google Scholar 

  • Haijema BJ, Hahn J, Haynes J, Dubnau D (2001) A ComGA-dependent checkpoint limits growth during the escape from competence. Mol Microbiol 40(1):52–64

    CAS  PubMed  Google Scholar 

  • Hamoen LW, Eshuis H, Jongbloed J, Venema G, van Sinderen D (1995) A small gene, designated comS, located within the coding region of the fourth amino acid-activation domain of srfA, is required for competence development in Bacillus subtilis. Mol Microbiol 15(1):55–63

    CAS  PubMed  Google Scholar 

  • Hamoen LW, Van Werkhoven AF, Bijlsma JJ, Dubnau D, Venema G (1998) The competence transcription factor of Bacillus subtilis recognizes short A/T-rich sequences arranged in a unique, flexible pattern along the DNA helix. Genes Dev 12(10):1539–1550

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hamoen LW, Van Werkhoven AF, Venema G, Dubnau D (2000) The pleiotropic response regulator DegU functions as a priming protein in competence development in Bacillus subtilis. Proc Natl Acad Sci U S A 97(16):9246–9251

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hamoen LW, Kausche D, Marahiel MA, van Sinderen D, Venema G, Serror P (2003a) The Bacillus subtilis transition state regulator AbrB binds to the -35 promoter region of comK. FEMS Microbiol Lett 218(2):299–304

    CAS  PubMed  Google Scholar 

  • Hamoen LW, Venema G, Kuipers OP (2003b) Controlling competence in Bacillus subtilis: shared use of regulators. Microbiology 149(Pt 1):9–17

    CAS  PubMed  Google Scholar 

  • Han CS, Xie G, Challacombe JF, Altherr MR, 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, Hill KK, Hitchcock P, Jackson PJ, Keim P, Kewalramani AR, Longmire J, Lucas S, Malfatti S, McMurry K, Meincke LJ, Misra M, Moseman BL, Mundt M, Munk AC, Okinaka RT, Parson-Quintana B, Reilly LP, Richardson P, Robinson DL, Rubin E, Saunders E, Tapia R, Tesmer JG, Thayer N, Thompson LS, Tice H, Ticknor LO, Wills PL, Brettin TS, Gilna P (2006) Pathogenomic sequence analysis of Bacillus cereus and Bacillus thuringiensis isolates closely related to Bacillus anthracis. J Bacteriol 188(9):3382–3390

    PubMed Central  PubMed  Google Scholar 

  • Hoa TT, Tortosa P, Albano M, Dubnau D (2002) Rok (YkuW) regulates genetic competence in Bacillus subtilis by directly repressing comK. Mol Microbiol 43(1):15–26

    CAS  PubMed  Google Scholar 

  • Hoffmann K, Wollherr A, Larsen M, Rachinger M, Liesegang H, Ehrenreich A, Meinhardt F (2010) Facilitation of direct conditional knockout of essential genes in Bacillus licheniformis DSM13 by comparative genetic analysis and manipulation of genetic competence. Appl Environ Microbiol 76(15):5046–5057

    CAS  PubMed Central  PubMed  Google Scholar 

  • Inamine GS, Dubnau D (1995) ComEA, a Bacillus subtilis integral membrane protein required for genetic transformation, is needed for both DNA binding and transport. J Bacteriol 177(11):3045–3051

    CAS  PubMed Central  PubMed  Google Scholar 

  • Inaoka T, Ochi K (2002) RelA protein is involved in induction of genetic competence in certain Bacillus subtilis strains by moderating the level of intracellular GTP. J Bacteriol 184(14):3923–3930

    CAS  PubMed Central  PubMed  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

    CAS  PubMed  Google Scholar 

  • Jakobs M, Hoffmann K, Grabke A, Neuber S, Liesegang H, Volland S, Meinhardt F (2014a) Unravelling the genetic basis for competence development of auxotrophic Bacillus licheniformis 9945A strains. Microbiol-SGM 160(Pt 10):2136–2147

    CAS  Google Scholar 

  • Jakobs M, Hoffmann K, Liesegang H, Volland S, Meinhardt F (2014b) The two putative comS-homologs of the biotechnologically important Bacillus licheniformis do not contribute to competence development. Appl Microbiol Biotechnol doi:10.1007/s00253-014-6291-5

  • Johnsborg O, Eldholm V, Havarstein LS (2007) Natural genetic transformation: prevalence, mechanisms and function. Res Microbiol 158(10):767–778

    CAS  PubMed  Google Scholar 

  • Kearns DB, Losick R (2003) Swarming motility in undomesticated Bacillus subtilis. Mol Microbiol 49(3):581–590

    CAS  PubMed  Google Scholar 

  • Kearns DB, Chu F, Rudner R, Losick R (2004) Genes governing swarming in Bacillus subtilis and evidence for a phase variation mechanism controlling surface motility. Mol Microbiol 52(2):357–369

    CAS  PubMed  Google Scholar 

  • Kidane D, Carrasco B, Manfredi C, Rothmaier K, Ayora S, Tadesse S, Alonso JC, Graumann PL (2009) Evidence for different pathways during horizontal gene transfer in competent Bacillus subtilis cells. PLoS Genet 5(9):e1000630

    PubMed Central  PubMed  Google Scholar 

  • Kleerebezem M, Quadri LE, Kuipers OP, de Vos WM (1997) Quorum sensing by peptide pheromones and two-component signal-transduction systems in Gram-positive bacteria. Mol Microbiol 24(5):895–904

    CAS  PubMed  Google Scholar 

  • Kobayashi K (2007) Gradual activation of the response regulator DegU controls serial expression of genes for flagellum formation and biofilm formation in Bacillus subtilis. Mol Microbiol 66(2):395–409

    CAS  PubMed  Google Scholar 

  • Konkol MA, Blair KM, Kearns DB (2013) Plasmid-encoded ComI inhibits competence in the ancestral 3610 strain of Bacillus subtilis. J Bacteriol 195(18):4085–4093

    CAS  PubMed Central  PubMed  Google Scholar 

  • Koumoutsi A, Chen XH, Henne A, Liesegang H, Hitzeroth G, Franke P, Vater J, Borriss R (2004) Structural and functional characterization of gene clusters directing nonribosomal synthesis of bioactive cyclic lipopeptides in Bacillus amyloliquefaciens strain FZB42. J Bacteriol 186(4):1084–1096

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kovacs AT, Smits WK, Mironczuk AM, Kuipers OP (2009) Ubiquitous late competence genes in Bacillus species indicate the presence of functional DNA uptake machineries. Environ Microbiol 11(8):1911–1922

    CAS  PubMed  Google Scholar 

  • Kovacs AT, Eckhardt TH, van Hartskamp M, van Kranenburg R, Kuipers OP (2013) Functional analysis of the ComK protein of Bacillus coagulans. PLoS One 8(1):e53471

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kunst F, Rapoport G (1995) Salt stress is an environmental signal affecting degradative enzyme synthesis in Bacillus subtilis. J Bacteriol 177(9):2403–2407

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kunst F, Msadek T, Bignon J, Rapoport G (1994) The DegS/DegU and ComP/ComA two-component systems are part of a network controlling degradative enzyme synthesis and competence in Bacillus subtilis. Res Microbiol 145(5–6):393–402

    CAS  PubMed  Google Scholar 

  • Kunst FON, Moszer I, Albertini AM, Alloni G, Azevedo V, Bertero MG, Bessières 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, Cordani JJ, Connerton IF, Cummings NJ, Daniel RA, Denziot F, Devine KM, Düsterhöft A, Ehrlich SD, Emmerson PT, Entian KD, Errington J, Fabret C, Ferrari E, Foulger D, Fritz C, Fujita M, Fujita Y, Fuma S, Galizzi A, Galleron N, Ghim SY, Glaser P, Goffeau A, Golightly EJ, Grandi G, Guiseppi G, Guy BJ, Haga K, Haiech J, Harwood CR, Hènaut A, Hilbert H, Holsappel S, Hosono S, Hullo MF, Itaya M, Jones L, Joris B, Karamata D, Kasahara Y, Klaerr-Blanchard M, Klein C, Kobayashi Y, Koetter P, Koningstein G, Krogh S, Kumano M, Kurita K, Lapidus A, Lardinois S, Lauber J, Lazarevic V, Lee SM, Levine A, Liu H, Masuda S, Mauël C, Médigue C, Medina N, Mellado RP, Mizuno M, Moestl D, Nakai S, Noback M, Noone D, O'Reilly M, Ogawa K, Ogiwara A, Oudega B, Park SH, Parro V, Pohl TM, Portelle D, Porwollik S, Prescott AM, Presecan E, Pujic P, Purnelle B, Rapoport G, Rey M, Reynolds S, Rieger M, Rivolta C, Rocha E, Roche B, Rose M, Sadaie Y, Sato T, Scanlan E, Schleich S, Schroeter R, Scoffone F, Sekiguchi J, Sekowska A, Seror SJ, Serror P, Shin BS, Soldo B, Sorokin A, Tacconi E, Takagi T, Takahashi H, Takemaru K, Takeuchi M, Tamakoshi A, Tanaka T, Terpstra P, Togoni A, Tosato V, Uchiyama S, Vandebol M, Vannier F, Vassarotti A, Viari A, Wambutt R, Wedler H, Weitzenegger T, Winters P, Wipat A, Yamamoto H, Yamane K, Yasumoto K, Yata K, Yoshida K, Yoshikawa HF, Zumstein E, Yoshikawa H, Danchin A (1997) The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390(6657):249–256

    CAS  PubMed  Google Scholar 

  • Lammers M, Nahrstedt H, Meinhardt F (2004) The Bacillus megaterium comE locus encodes a functional DNA uptake protein. J Basic Microbiol 44(6):451–458

    CAS  PubMed  Google Scholar 

  • Lapidus A, Galleron N, Andersen JT, Jorgensen PL, Ehrlich SD, Sorokin A (2002) Co-linear scaffold of the Bacillus licheniformis and Bacillus subtilis genomes and its use to compare their competence genes. FEMS Microbiol Lett 209(1):23–30

    CAS  PubMed  Google Scholar 

  • Lazazzera BA, Kurtser IG, McQuade RS, Grossman AD (1999) An autoregulatory circuit affecting peptide signaling in Bacillus subtilis. J Bacteriol 181(17):5193–5200

    CAS  PubMed Central  PubMed  Google Scholar 

  • Leonard CG, Mattheis MJ (1965) Different transforming characteristics of colonial variants from auxotrophic mutants of Bacillus licheniformis. J Bacteriol 90:558–559

  • Leonard CG, Mattheis DK, Mattheis MJ, Housewright RD (1964) Transformation to prototrophy and polyglutamic acid synthesis in Bacillus licheniformis. J Bacteriol 88:220–225

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liu L, Nakano MM, Lee OH, Zuber P (1996) Plasmid-amplified comS enhances genetic competence and suppresses sinR in Bacillus subtilis. J Bacteriol 178(17):5144–5152

    CAS  PubMed Central  PubMed  Google Scholar 

  • Londono-Vallejo JA, Dubnau D (1993) comF, a Bacillus subtilis late competence locus, encodes a protein similar to ATP-dependent RNA/DNA helicases. Mol Microbiol 9(1):119–131

    CAS  PubMed  Google Scholar 

  • Londono-Vallejo JA, Dubnau D (1994) Mutation of the putative nucleotide binding site of the Bacillus subtilis membrane protein ComFA abolishes the uptake of DNA during transformation. J Bacteriol 176(15):4642–4645

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lopez JM, Dromerick A, Freese E (1981) Response of guanosine 5'-triphosphate concentration to nutritional changes and its significance for Bacillus subtilis sporulation. J Bacteriol 146(2):605–613

    CAS  PubMed Central  PubMed  Google Scholar 

  • Maamar H, Dubnau D (2005) Bistability in the Bacillus subtilis K-state (competence) system requires a positive feedback loop. Mol Microbiol 56(3):615–624

    CAS  PubMed  Google Scholar 

  • Magnuson R, Solomon J, Grossman AD (1994) Biochemical and genetic characterization of a competence pheromone from B. subtilis. Cell 77(2):207–216

    CAS  PubMed  Google Scholar 

  • Maier B, Chen I, Dubnau D, Sheetz MP (2004) DNA transport into Bacillus subtilis requires proton motive force to generate large molecular forces. Nat Struct Mol Biol 11(7):643–649

    CAS  PubMed  Google Scholar 

  • McCuen RW, Thorne CB (1971) Genetic mapping of genes concerned with glutamyl polypeptide production by Bacillus licheniformis and a study of their relationship to the development of competence for transformation. J Bacteriol 107(3):636–645

    CAS  PubMed Central  PubMed  Google Scholar 

  • McLoon AL, Guttenplan SB, Kearns DB, Kolter R, Losick R (2011) Tracing the domestication of a biofilm-forming bacterium. J Bacteriol 193(8):2027–2034

    CAS  PubMed Central  PubMed  Google Scholar 

  • Meinhardt F, Stahl U, Ebeling W (1989) Highly efficient expression of homologous and heterologous genes in Bacillus megaterium. Appl Microbiol Biotechnol 30:343–350

    CAS  Google Scholar 

  • Mironczuk AM, Kovács Á, Kuipers O (2008) Induction of natural competence in Bacillus cereus ATCC14579. Microb Biotechnol 1(3):226–235

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mironczuk AM, Manu A, Kuipers OP, Kovacs AT (2011) Distinct roles of ComK1 and ComK2 in gene regulation in Bacillus cereus. PLoS One 6(7):e21859

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mirouze N, Desai Y, Raj A, Dubnau D (2012) Spo0A ~ P imposes a temporal gate for the bimodal expression of competence in Bacillus subtilis. PLoS Genet 8(3):e1002586

    CAS  PubMed Central  PubMed  Google Scholar 

  • Moran CP Jr, Lang N, LeGrice SF, Lee G, Stephens M, Sonenshein AL, Pero J, Losick R (1982) Nucleotide sequences that signal the initiation of transcription and translation in Bacillus subtilis. Mol Gen Genet 186(3):339–346

    CAS  PubMed  Google Scholar 

  • Msadek T (1999) When the going gets tough: survival strategies and environmental signaling networks in Bacillus subtilis. Trends Microbiol 7(5):201–207

    CAS  PubMed  Google Scholar 

  • Msadek T, Kunst F, Henner D, Klier A, Rapoport G, Dedonder R (1990) Signal transduction pathway controlling synthesis of a class of degradative enzymes in Bacillus subtilis: expression of the regulatory genes and analysis of mutations in degS and degU. J Bacteriol 172(2):824–834

    CAS  PubMed Central  PubMed  Google Scholar 

  • Msadek T, Kunst F, Klier A, Rapoport G (1991) DegS-DegU and ComP-ComA modulator-effector pairs control expression of the Bacillus subtilis pleiotropic regulatory gene degQ. J Bacteriol 173(7):2366–2377

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nagai T, Itoh Y (1997) Characterization of a Generalized Transducing Phage of Poly-(gamma)-Glutamic Acid-Producing Bacillus subtilis and Its Application for Analysis of Tn917-LTV1 Insertional Mutants Defective in Poly-(gamma)-Glutamic Acid Production. Appl Environ Microbiol 63(10):4087–4089

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nagai T, Phan Tran LS, Inatsu Y, Itoh Y (2000) A new IS4 family insertion sequence, IS4Bsu1, responsible for genetic instability of poly-gamma-glutamic acid production in Bacillus subtilis. J Bacteriol 182(9):2387–2392

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nahrstedt H, Schröder C, Meinhardt F (2005) Evidence for two recA genes mediating DNA repair in Bacillus megaterium. Microbiology 151(Pt 3):775–787

    CAS  PubMed  Google Scholar 

  • Nakano MM, Zuber P (1991) The primary role of comA in establishment of the competent state in Bacillus subtilis is to activate expression of srfA. J Bacteriol 173(22):7269–7274

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nakano MM, Corbell N, Besson J, Zuber P (1992) Isolation and characterization of sfp: a gene that functions in the production of the lipopeptide biosurfactant, surfactin, in Bacillus subtilis. Mol Gen Genet 232(2):313–321

    CAS  PubMed  Google Scholar 

  • Nijland R, Burgess JG, Errington J, Veening JW (2010) Transformation of environmental Bacillus subtilis isolates by transiently inducing genetic competence. PLoS One 5(3):e9724. doi:10.1371/journal.pone.0009724

    PubMed Central  PubMed  Google Scholar 

  • Ogura M, Liu L, Lacelle M, Nakano MM, Zuber P (1999) Mutational analysis of ComS: evidence for the interaction of ComS and MecA in the regulation of competence development in Bacillus subtilis. Mol Microbiol 32(4):799–812

    CAS  PubMed  Google Scholar 

  • Ogura M, Yamaguchi H, Kobayashi K, Ogasawara N, Fujita Y, Tanaka T (2002) Whole-genome analysis of genes regulated by the Bacillus subtilis competence transcription factor ComK. J Bacteriol 184(9):2344–2351

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ohsawa T, Tsukahara K, Ogura M (2009) Bacillus subtilis response regulator DegU is a direct activator of pgsB transcription involved in gamma-poly-glutamic acid synthesis. Biosci Biotechnol Biochem 73(9):2096–2102

    CAS  PubMed  Google Scholar 

  • O'Reilly M, Devine KM (1997) Expression of AbrB, a transition state regulator from Bacillus subtilis, is growth phase dependent in a manner resembling that of Fis, the nucleoid binding protein from Escherichia coli. J Bacteriol 179(2):522–529

    PubMed Central  PubMed  Google Scholar 

  • Perego M (1997) A peptide export-import control circuit modulating bacterial development regulates protein phosphatases of the phosphorelay. Proc Natl Acad Sci U S A 94(16):8612–8617

    CAS  PubMed Central  PubMed  Google Scholar 

  • Perego M, Hanstein C, Welsh KM, Djavakhishvili T, Glaser P, Hoch JA (1994) Multiple protein-aspartate phosphatases provide a mechanism for the integration of diverse signals in the control of development in B. subtilis. Cell 79(6):1047–1055

    CAS  PubMed  Google Scholar 

  • Perego M, Glaser P, Hoch JA (1996) Aspartyl-phosphate phosphatases deactivate the response regulator components of the sporulation signal transduction system in Bacillus subtilis. Mol Microbiol 19(6):1151–1157

    CAS  PubMed  Google Scholar 

  • Persuh M, Turgay K, Mandic-Mulec I, Dubnau D (1999) The N- and C-terminal domains of MecA recognize different partners in the competence molecular switch. Mol Microbiol 33(4):886–894

    CAS  PubMed  Google Scholar 

  • Prepiak P, Dubnau D (2007) A peptide signal for adapter protein-mediated degradation by the AAA+ protease ClpCP. Mol Cell 26(5):639–647

    CAS  PubMed Central  PubMed  Google Scholar 

  • Provvedi R, Dubnau D (1999) ComEA is a DNA receptor for transformation of competent Bacillus subtilis. Mol Microbiol 31(1):271–280

    CAS  PubMed  Google Scholar 

  • Provvedi R, Chen I, Dubnau D (2001) NucA is required for DNA cleavage during transformation of Bacillus subtilis. Mol Microbiol 40(3):634–644

    CAS  PubMed  Google Scholar 

  • Rasko DA, Ravel J, Okstad OA, Helgason E, Cer RZ, Jiang L, Shores KA, Fouts DE, Tourasse NJ, Angiuoli SV, Kolonay J, Nelson WC, Kolsto AB, Fraser CM, Read TD (2004) The genome sequence of Bacillus cereus ATCC 10987 reveals metabolic adaptations and a large plasmid related to Bacillus anthracis pXO1. Nucleic Acids Res 32(3):977–988

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ratnayake-Lecamwasam M, Serror P, Wong KW, Sonenshein AL (2001) Bacillus subtilis CodY represses early-stationary-phase genes by sensing GTP levels. Genes Dev 15(9):1093–1103

    CAS  PubMed Central  PubMed  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

    CAS  PubMed  Google Scholar 

  • Rey MW, Ramaiya P, Nelson BA, Brody-Karpin SD, Zaretsky EJ, Tang M, Lopez de Leon A, Xiang H, Gusti V, Clausen IG, Olsen PB, Rasmussen MD, Andersen JT, Jorgensen PL, Larsen TS, Sorokin A, Bolotin A, Lapidus A, Galleron N, Ehrlich SD, Berka RM (2004) Complete genome sequence of the industrial bacterium Bacillus licheniformis and comparisons with closely related Bacillus species. Genome Biol 5(10):R77

    PubMed Central  PubMed  Google Scholar 

  • Richhardt J, Larsen M, Meinhardt F (2010) An improved transconjugation protocol for Bacillus megaterium facilitating a direct gene knock-out. Appl Microbiol Biotechnol 86:1959–1965

    CAS  PubMed  Google Scholar 

  • Roggiani M, Dubnau D (1993) ComA, a phosphorylated response regulator protein of Bacillus subtilis, binds to the promoter region of srfA. J Bacteriol 175(10):3182–3187

    CAS  PubMed Central  PubMed  Google Scholar 

  • Serror P, Sonenshein AL (1996) CodY is required for nutritional repression of Bacillus subtilis genetic competence. J Bacteriol 178(20):5910–5915

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shivers RP, Sonenshein AL (2004) Activation of the Bacillus subtilis global regulator CodY by direct interaction with branched-chain amino acids. Mol Microbiol 53(2):599–611

    CAS  PubMed  Google Scholar 

  • Singh PK, Ramachandran G, Duran-Alcalde L, Alonso C, Wu LJ, Meijer WJ (2012) Inhibition of Bacillus subtilis natural competence by a native, conjugative plasmid-encoded comK repressor protein. Environ Microbiol 14(10):2812–2825

    CAS  PubMed  Google Scholar 

  • Solomon JM, Lazazzera BA, Grossman AD (1996) Purification and characterization of an extracellular peptide factor that affects two different developmental pathways in Bacillus subtilis. Genes Dev 10(16):2014–2024

    CAS  PubMed  Google Scholar 

  • Spizizen J (1958) Transformation of Biochemically Deficient Strains of Bacillus subtilis by Deoxyribonucleate. Proc Natl Acad Sci U S A 44(10):1072–1078

    CAS  PubMed Central  PubMed  Google Scholar 

  • Spizizen J, Prestidge L (1969) Conditions for competence in the Bacillus licheniformis transformation system. J Bacteriol 99(1):70–77

    CAS  PubMed Central  PubMed  Google Scholar 

  • Stanley NR, Lazazzera BA (2005) Defining the genetic differences between wild and domestic strains of Bacillus subtilis that affect poly-gamma-DL-glutamic acid production and biofilm formation. Mol Microbiol 57(4):1143–1158

    CAS  PubMed  Google Scholar 

  • Strauch MA, Hoch JA (1993) Transition-state regulators: sentinels of Bacillus subtilis post-exponential gene expression. Mol Microbiol 7(3):337–342

    CAS  PubMed  Google Scholar 

  • Strauch MA, Spiegelman GB, Perego M, Johnson WC, Burbulys D, Hoch JA (1989) The transition state transcription regulator abrB of Bacillus subtilis is a DNA binding protein. Embo J 8(5):1615–1621

    CAS  PubMed Central  PubMed  Google Scholar 

  • Susanna KA, van der Werff AF, den Hengst CD, Calles B, Salas M, Venema G, Hamoen LW, Kuipers OP (2004) Mechanism of transcription activation at the comG promoter by the competence transcription factor ComK of Bacillus subtilis. J Bacteriol 186(4):1120–1128

    CAS  PubMed Central  PubMed  Google Scholar 

  • Susanna KA, Fusetti F, Thunnissen AM, Hamoen LW, Kuipers OP (2006) Functional analysis of the competence transcription factor ComK of Bacillus subtilis by characterization of truncation variants. Microbiology 152(Pt 2):473–483

    CAS  PubMed  Google Scholar 

  • Takahashi K, Sekine Y, Chibazakura T, Yoshikawa H (2007) Development of an intermolecular transposition assay system in Bacillus subtilis 168 using IS4Bsu1 from Bacillus subtilis (natto). Microbiology 153(Pt 8):2553–2559

    CAS  PubMed  Google Scholar 

  • Takami H, Nakasone K, Takaki Y, Maeno G, Sasaki R, Masui N, Fuji F, Hirama C, Nakamura Y, Ogasawara N, Kuhara S, Horikoshi K (2000) Complete genome sequence of the alkaliphilic bacterium Bacillus halodurans and genomic sequence comparison with Bacillus subtilis. Nucleic Acids Res 28(21):4317–4331

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tanaka T, Koshikawa T (1977) Isolation and characterization of four types of plasmids from Bacillus subtilis (natto). J Bacteriol 131(2):699–701

    CAS  PubMed Central  PubMed  Google Scholar 

  • Thorne CB, Stull HB (1966) Factors affecting transformation of Bacillus licheniformis. J Bacteriol 91(3):1012–1020

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tortosa P, Logsdon L, Kraigher B, Itoh Y, Mandic-Mulec I, Dubnau D (2001) Specificity and genetic polymorphism of the Bacillus competence quorum-sensing system. J Bacteriol 183(2):451–460

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tran LS, Nagai T, Itoh Y (2000) Divergent structure of the ComQXPA quorum-sensing components: molecular basis of strain-specific communication mechanism in Bacillus subtilis. Mol Microbiol 37(5):1159–1171

    CAS  PubMed  Google Scholar 

  • Tsuji F, Ishihara A, Nakagawa A, Okada M, Kitamura S, Kanamaru K, Masuda Y, Murakami K, Irie K, Sakagami Y (2012) Lack of the consensus sequence necessary for tryptophan prenylation in the ComX pheromone precursor. Biosci Biotechnol Biochem 76(8):1492–1496

    CAS  PubMed  Google Scholar 

  • Turgay K, Hamoen LW, Venema G, Dubnau D (1997) Biochemical characterization of a molecular switch involving the heat shock protein ClpC, which controls the activity of ComK, the competence transcription factor of Bacillus subtilis. Genes Dev 11(1):119–128

    CAS  PubMed  Google Scholar 

  • Turgay K, Hahn J, Burghoorn J, Dubnau D (1998) Competence in Bacillus subtilis is controlled by regulated proteolysis of a transcription factor. Embo J 17(22):6730–6738

    CAS  PubMed Central  PubMed  Google Scholar 

  • van Sinderen D, Venema G (1994) comK acts as an autoregulatory control switch in the signal transduction route to competence in Bacillus subtilis. J Bacteriol 176(18):5762–5770

    CAS  PubMed Central  PubMed  Google Scholar 

  • van Sinderen D, Luttinger A, Kong L, Dubnau D, Venema G, Hamoen L (1995) comK encodes the competence transcription factor, the key regulatory protein for competence development in Bacillus subtilis. Mol Microbiol 15(3):455–462

    PubMed  Google Scholar 

  • Vary PS (1994) Prime time for Bacillus megaterium. Microbiology 140(Pt 5):1001–1013

    CAS  PubMed  Google Scholar 

  • Vary PS, Garbe JC, Franzen M, Frampton EW (1982) MP13, a generalized transducing bacteriophage for Bacillus megaterium. J Bacteriol 149(3):1112–1119

    CAS  PubMed Central  PubMed  Google Scholar 

  • Veith B, Herzberg C, Steckel S, Feesche J, Maurer KH, Ehrenreich P, Baumer S, Henne A, Liesegang H, Merkl R, Ehrenreich A, Gottschalk G (2004) The complete genome sequence of Bacillus licheniformis DSM13, an organism with great industrial potential. J Mol Microbiol Biotechnol 7(4):204–211

    CAS  PubMed  Google Scholar 

  • Venema G, Pritchard RH, Venema-Schroeder T (1965) Fate of Transforming Deoxyribonucleic Acid in Bacillus subtilis. J Bacteriol 89:1250–1255

    CAS  PubMed Central  PubMed  Google Scholar 

  • Verhamme DT, Kiley TB, Stanley-Wall NR (2007) DegU co-ordinates multicellular behaviour exhibited by Bacillus subtilis. Mol Microbiol 65(2):554–568

    CAS  PubMed  Google Scholar 

  • Waschkau B, Waldeck J, Wieland S, Eichstädt R, Meinhardt F (2008) Generation of readily transformable Bacillus licheniformis mutants. Appl Microbiol Biotechnol 78(1):181–188

    CAS  PubMed  Google Scholar 

  • Weinrauch Y, Penchev R, Dubnau E, Smith I, Dubnau D (1990) A Bacillus subtilis regulatory gene product for genetic competence and sporulation resembles sensor protein members of the bacterial two-component signal-transduction systems. Genes Dev 4(5):860–872

    CAS  PubMed  Google Scholar 

  • Wemhoff S, Meinhardt F (2013) Generation of biologically contained, readily transformable, and genetically manageable mutants of the biotechnologically important Bacillus pumilus. Appl Microbiol Biotechnol 97(17):7805–7819

    CAS  PubMed  Google Scholar 

  • Yadav T, Carrasco B, Myers AR, George NP, Keck JL, Alonso JC (2012) Genetic recombination in Bacillus subtilis: a division of labor between two single-strand DNA-binding proteins. Nucleic Acids Res 40(12):5546–5559

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yadav T, Carrasco B, Hejna J, Suzuki Y, Takeyasu K, Alonso JC (2013) Bacillus subtilis DprA recruits RecA onto single-stranded DNA and mediates annealing of complementary strands coated by SsbB and SsbA. J Biol Chem 288(31):22437–22450

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yang M, Ferrari E, Chen E, Henner DJ (1986) Identification of the pleiotropic sacQ gene of Bacillus subtilis. J Bacteriol 166(1):113–119

    CAS  PubMed Central  PubMed  Google Scholar 

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  1. Westfälische Wilhelms-Universität Münster, Institut für Molekulare Mikrobiologie und Biotechnologie, Corrensstrasse 3, 48149, Münster, Germany

    Mareike Jakobs & Friedhelm Meinhardt

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Jakobs, M., Meinhardt, F. What renders Bacilli genetically competent? A gaze beyond the model organism. Appl Microbiol Biotechnol 99, 1557–1570 (2015). https://doi.org/10.1007/s00253-014-6316-0

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