1887

Chapter 6 : Systems Biology: Applications of -Omics Techniques to the Study of Endospore Formation

Authors: Ashley R. Bate1, Richard Bonneau2, Patrick Eichenberger3
VIEW AFFILIATIONS HIDE AFFILIATIONS
Affiliations: 1: Center for Genomics and Systems Biology, Department of Biology, New York University, New York, NY 10003; 2: Center for Genomics and Systems Biology, Department of Biology, New York University, New York, NY 10003; 3: Center for Genomics and Systems Biology, Department of Biology, New York University, New York, NY 10003
Content Type: Monograph
Publication Year: 2016

Category: Bacterial Pathogenesis

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Preview Magnify
Zoom in
Zoomout

Systems Biology: Applications of -Omics Techniques to the Study of Endospore Formation, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555819323/9781555816759_Chap06-1.gif /docserver/preview/fulltext/10.1128/9781555819323/9781555816759_Chap06-2.gif

Abstract:

The principal laboratory strain, strain 168, is derived from a parent strain isolated in Marburg, Germany, following a mutagenesis procedure ( ). The popularity of this strain arose after it was shown to be competent for genetic transformation ( ), which paved the way for myriad molecular genetics analyses that led to a detailed understanding of the biology of and related Gram-positive bacteria. It is therefore not surprising that strain 168 was the first Gram-positive species to have its entire genome sequenced, at a time when sequencing was a laborious and expensive process. The project to sequence the genome was set up in 1987 by a consortium of over 30 laboratories and took about 10 years to complete. Each laboratory was assigned a different region of the chromosome and used their own cloning and sequencing strategies to manage their assigned portion of the genome ( ). The final genome sequence contained 4,214,810 base pairs, and the original annotation included 4,100 protein-coding genes ( ). Following the development of sequencing technologies that were considerably faster and more efficient, the genome of strain 168 was resequenced and cleared of sequencing errors in 2009 ( ). The most recent update of the annotation brought the total of protein-coding genes to 4,458 ( ).

Citation: Bate A, Bonneau R, Eichenberger P. 2016. Systems Biology: Applications of -Omics Techniques to the Study of Endospore Formation, p 129-144. In Driks A, Eichenberger P (ed), The Bacterial Spore: from Molecules to Systems. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.TBS-0019-2013
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Bacillus subtilis Systems Biology: Applications of -Omics Techniques to the Study of Endospore Formation
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555819323.chap6-1,webId=/content/author/10.1128/9781555819323.chap6-1,properties={foaf_givenname=Ashley R., foaf_name=Ashley R. Bate, foaf_surname=Bate, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555819323.chap6-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555819323.chap6-2,webId=/content/author/10.1128/9781555819323.chap6-2,properties={foaf_givenname=Richard, foaf_name=Richard Bonneau, foaf_surname=Bonneau, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555819323.chap6-aff2]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555819323.chap6-3,webId=/content/author/10.1128/9781555819323.chap6-3,properties={foaf_givenname=Patrick, foaf_name=Patrick Eichenberger, foaf_surname=Eichenberger, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555819323.chap6-aff3]]}]]
Citation: Bate A, Bonneau R, Eichenberger P. 2016. Systems Biology: Applications of -Omics Techniques to the Study of Endospore Formation, p 129-144. In Driks A, Eichenberger P (ed), The Bacterial Spore: from Molecules to Systems. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.TBS-0019-2013
/content/10.1128/9781555819323.chap6.fig6-1
Figure 1

The life cycle of and the principal stages of sporulation. During the first stage of sporulation, the master regulator Spo0A∼P is required in combination with σ (major σ factor) and σ (stationary phase σ factor) for the expression of early sporulation genes. Next, an asymmetric division of the sporulating cell creates the mother cell (light blue) and the forespore (orange). Each compartment establishes cell-specific lines of gene expression driven by σ in the forespore and σ in the mother cell. Subsequently, the mother cell engulfs the forespore. During engulfment, proteins produced in the mother cell assemble at the forespore surface to form the coat (dark red). After engulfment, σ substitutes for σ and σ replaces σ (σ remains active during the entire process). The cortex (yellow), made of peptidoglycan, is assembled between the inner and outer forespore membranes. Once the spore is mature, the mother cell lyses. During the germination process, the cortex is hydrolyzed and the coat is shed. Adapted from references , and .

10.1128/9781555819323/fig6-1_thmb.gif
10.1128/9781555819323/fig6-1.gif
Image of Figure 1
Figure 1

The life cycle of and the principal stages of sporulation. During the first stage of sporulation, the master regulator Spo0A∼P is required in combination with σ (major σ factor) and σ (stationary phase σ factor) for the expression of early sporulation genes. Next, an asymmetric division of the sporulating cell creates the mother cell (light blue) and the forespore (orange). Each compartment establishes cell-specific lines of gene expression driven by σ in the forespore and σ in the mother cell. Subsequently, the mother cell engulfs the forespore. During engulfment, proteins produced in the mother cell assemble at the forespore surface to form the coat (dark red). After engulfment, σ substitutes for σ and σ replaces σ (σ remains active during the entire process). The cortex (yellow), made of peptidoglycan, is assembled between the inner and outer forespore membranes. Once the spore is mature, the mother cell lyses. During the germination process, the cortex is hydrolyzed and the coat is shed. Adapted from references , and .

Citation: Bate A, Bonneau R, Eichenberger P. 2016. Systems Biology: Applications of -Omics Techniques to the Study of Endospore Formation, p 129-144. In Driks A, Eichenberger P (ed), The Bacterial Spore: from Molecules to Systems. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.TBS-0019-2013
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555819323.chap6
1. Burkholder PR,, Giles NH Jr . 1947. Induced biochemical mutations in Bacillus subtilis . Am J Bot 34 : 345– 348.[PubMed]
2. Spizizen J . 1958. Transformation of biochemically deficient strains of Bacillus subtilis by deoxyribonucleate. Proc Natl Acad Sci USA 44 : 1072– 1078.[PubMed]
3. Anagnostopoulos C,, Spizizen J . 1961. Requirements for transformation in Bacillus subtilis . J Bacteriol 81 : 741– 746.[PubMed]
4. Kunst F,, Vassarotti A,, Danchin A . 1995. Organization of the European Bacillus subtilis genome sequencing project. Microbiology 141 : 249– 255.[PubMed]
5. 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 : 249– 256.[PubMed] [CrossRef]
6. 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 : 1758– 1775.[PubMed] [CrossRef]
7. Belda E,, Sekowska A,, Le Fèvre F,, Morgat A,, Mornico D,, Ouzounis C,, Vallenet D,, Médigue C,, Danchin A . 2013. An updated metabolic view of the Bacillus subtilis 168 genome. Microbiology 159 : 757– 770.[PubMed] [CrossRef]
8. 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 : 357– 369.[PubMed] [CrossRef]
9. McLoon AL,, Guttenplan SB,, Kearns DB,, Kolter R,, Losick R . 2011. Tracing the domestication of a biofilm-forming bacterium. J Bacteriol 193 : 2027– 2034.[PubMed] [CrossRef]
10. Zeigler DR,, Pragai Z,, Rodriguez S,, Chevreux B,, Muffler A,, Albert T,, Bai R,, Wyss M,, Perkins JB . 2008. The origins of 168, W23, and other Bacillus subtilis legacy strains. J Bacteriol 190 : 6983– 6995.[PubMed] [CrossRef]
11. Youngman P,, Perkins JB,, Losick R . 1984. Construction of a cloning site near one end of Tn 917 into which foreign DNA may be inserted without affecting transposition in Bacillus subtilis or expression of the transposon-borne erm gene. Plasmid 12 : 1– 9.[PubMed]
12. Auchtung JM,, Lee CA,, Monson RE,, Lehman AP,, Grossman AD . 2005. Regulation of a Bacillus subtilis mobile genetic element by intercellular signaling and the global DNA damage response. Proc Natl Acad Sci USA 102 : 12554– 12559.[PubMed] [CrossRef]
13. Zeigler DR . 2011. The genome sequence of Bacillus subtilis subsp. spizizenii W23: insights into speciation within the B. subtilis complex and into the history of B. subtilis genetics. Microbiology 157 : 2033– 2041.[PubMed] [CrossRef]
14. Lazarevic V,, Abellan FX,, Moller SB,, Karamata D,, Mauel C . 2002. Comparison of ribitol and glycerol teichoic acid genes in Bacillus subtilis W23 and 168: identical function, similar divergent organization, but different regulation. Microbiology 148 : 815– 824.[PubMed]
15. Qian Z,, Yin Y,, Zhang Y,, Lu L,, Li Y,, Jiang Y . 2006. Genomic characterization of ribitol teichoic acid synthesis in Staphylococcus aureus: genes, genomic organization and gene duplication. BMC Genomics 7 : 74. doi:10.1186/1471-2164-7-74 [PubMed] [CrossRef]
16. Earl AM,, Eppinger M,, Fricke WF,, Rosovitz MJ,, Rasko DA,, Daugherty S,, Losick R,, Kolter R,, Ravel J . 2012. Whole-genome sequences of Bacillus subtilis and close relatives. J Bacteriol 194 : 2378– 2379.[PubMed] [CrossRef]
17. Schyns G,, Serra CR,, Lapointe T,, Pereira-Leal JB,, Potot S,, Fickers P,, Perkins JB,, Wyss M,, Henriques AO . 14 February 2013. Genome of a gut strain of Bacillus subtilis . Genome Announc doi:10.1128/genomeA.00184-12. [PubMed] [CrossRef]
18. Durrett R,, Miras M,, Mirouze N,, Narechania A,, Mandic-Mulec I,, Dubnau D . 20 June 2013. Genome sequence of the Bacillus subtilis biofilm-forming transformable strain PS216. Genome Announc doi:10.1128/genomeA.00288-13 [PubMed] [CrossRef]
19. Rasko DA,, Altherr MR,, Han CS,, Ravel J . 2005. Genomics of the Bacillus cereus group of organisms. FEMS Microbiol Rev 29 : 303– 329.[PubMed]
20. Nolling J,, Breton G,, Omelchenko MV,, Makarova KS,, Zeng Q,, Gibson R,, Lee HM,, Dubois J,, Qiu D,, Hitti J,, Wolf YI,, Tatusov RL,, Sabathe F,, Doucette-Stamm L,, Soucaille P,, Daly MJ,, Bennett GN,, Koonin EV,, Smith DR . 2001. Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum . J Bacteriol 183 : 4823– 4838.[PubMed] [CrossRef]
21. Shimizu T,, Ohtani K,, Hirakawa H,, Ohshima K,, Yamashita A,, Shiba T,, Ogasawara N,, Hattori M,, Kuhara S,, Hayashi H . 2002. Complete genome sequence of Clostridium perfringens, an anaerobic flesh-eater. Proc Natl Acad Sci USA 99 : 996– 1001.[PubMed] [CrossRef]
22. Sebaihia M,, Peck MW,, Minton NP,, Thomson NR,, Holden MT,, Mitchell WJ,, Carter AT,, Bentley SD,, Mason DR,, Crossman L,, Paul CJ,, Ivens A,, Wells-Bennik MH,, Davis IJ,, Cerdeno-Tarraga AM,, Churcher C,, Quail MA,, Chillingworth T,, Feltwell T,, Fraser A,, Goodhead I,, Hance Z,, Jagels K,, Larke N,, Maddison M,, Moule S,, Mungall K,, Norbertczak H,, Rabbinowitsch E,, Sanders M,, Simmonds M,, White B,, Whithead S,, Parkhill J . 2007. Genome sequence of a proteolytic (Group I) Clostridium botulinum strain Hall A and comparative analysis of the clostridial genomes. Genome Res 17 : 1082– 1092.[PubMed] [CrossRef]
23. Sebaihia M,, Wren BW,, Mullany P,, Fairweather NF,, Minton N,, Stabler R,, Thomson NR,, Roberts AP,, Cerdeño-Tárraga AM,, Wang H,, Holden MTG,, Wright A,, Churcher C,, Quail MA,, Baker S,, Bason N,, Brooks K,, Chillingworth T,, Cronin A,, Davis P,, Dowd L,, Fraser A,, Feltwell T,, Hance Z,, Holroyd S,, Jagels K,, Moule S,, Mungall K,, Price C,, Rabbinowitsch E,, Sharp S,, Simmonds M,, Stevens K,, Unwin L,, Whithead S,, Dupuy B,, Dougan G,, Barrell B,, Parkhill J . 2006. The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nat Genet 38 : 779– 786.[PubMed] [CrossRef]
24. Stragier P, . 2002. A gene odyssey: exploring the genomes of endospore-forming bacteria, p 519– 526. In Sonenshein AL,, Hoch JA,, Losick R (ed), Bacillus subtilis and Its Closest Relatives: From Genes to Cells. ASM Press, Washington, DC.
25. Stephenson K,, Hoch JA . 2002. Evolution of signalling in the sporulation phosphorelay. Mol Microbiol 46 : 297– 304.[PubMed]
26. Steiner E,, Dago AE,, Young DI,, Heap JT,, Minton NP,, Hoch JA,, Young M . 2011. Multiple orphan histidine kinases interact directly with Spo0A to control the initiation of endospore formation in Clostridium acetobutylicum . Mol Microbiol 80 : 641– 654.[PubMed] [CrossRef]
27. Losick R,, Stragier P . 1992. Crisscross regulation of cell-type-specific gene expression during development in B. subtilis . Nature 355 : 601– 604.[PubMed] [CrossRef]
28. Fimlaid KA,, Bond JP,, Schutz KC,, Putnam EE,, Leung JM,, Lawley TD,, Shen A . 2013. Global analysis of the sporulation pathway of Clostridium difficile . PLoS Genet 8 : e1003660. doi:10.1371/journal.pgen.1003660. [PubMed] [CrossRef]
29. Pereira FC,, Saujet L,, Tomé AR,, Serrano M,, Monot M,, Couture-Tosi E,, Martin-Verstraete I,, Dupuy B,, Henriques AO . 2013. The spore differentiation pathway in the enteric pathogen Clostridium difficile . PLoS Genet 9 : e1003782. doi:10.1371/journal.pgen.1003782. [PubMed] [CrossRef]
30. Saujet L,, Pereira FC,, Serrano M,, Soutourina O,, Monot M,, Shelyakin PV,, Gelfand MS,, Dupuy B,, Henriques AO,, Martin-Verstraete I . 2013. Genome-wide analysis of cell type-specific gene transcription during spore formation in Clostridium difficile . PLoS Genet 9 : e1003756. doi:10.1371/journal.pgen.1003756. [PubMed] [CrossRef]
31. Haraldsen JD,, Sonenshein AL . 2003. Efficient sporulation in Clostridium difficile requires disruption of the sigmaK gene. Mol Microbiol 48 : 811– 821.[PubMed]
32. de Hoon MJ,, Eichenberger P,, Vitkup D . 2010. Hierarchical evolution of the bacterial sporulation network. Curr Biol 20 : R735– R745.[PubMed] [CrossRef]
33. Xiao Y,, Francke C,, Abee T,, Wells-Bennik MH . 2011. Clostridial spore germination versus bacilli: genome mining and current insights. Food Microbiol 28 : 266– 274.[PubMed] [CrossRef]
34. Sorg JA,, Sonenshein AL . 2008. Bile salts and glycine as co-germinants for Clostridium difficile spores. J Bacteriol 190 : 2505– 2512.[PubMed] [CrossRef]
35. Traag BA,, Pugliese A,, Eisen JA,, Losick R . 2013. Gene conservation among endospore-forming bacteria reveals additional sporulation genes in Bacillus subtilis . J Bacteriol 195 : 253– 260.[PubMed] [CrossRef]
36. Abecasis AB,, Serrano M,, Alves R,, Quintais L,, Pereira-Leal JB,, Henriques AO . 2013. A genomic signature and the identification of new sporulation genes. J Bacteriol 195 : 2101– 2115.[PubMed] [CrossRef]
37. Galperin MY,, Mekhedov SL,, Puigbo P,, Smirnov S,, Wolf YI,, Rigden DJ . 2012. Genomic determinants of sporulation in Bacilli and Clostridia: towards the minimal set of sporulation-specific genes. Environ Microbiol 14 : 2870– 2890.[PubMed] [CrossRef]
38. Jordan B . 2002. Historical background and anticipated developments. Ann N Y Acad Sci 975 : 24– 32.[PubMed]
39. Fawcett P,, Eichenberger P,, Losick R,, Youngman P . 2000. The transcriptional profile of early to middle sporulation in Bacillus subtilis . Proc Natl Acad Sci USA 97 : 8063– 8068.[PubMed] [CrossRef]
40. Britton RA,, Eichenberger P,, Gonzalez-Pastor JE,, Fawcett P,, Monson R,, Losick R,, Grossman AD . 2002. Genome-wide analysis of the stationary-phase sigma factor (sigma-H) regulon of Bacillus subtilis . J Bacteriol 184 : 4881– 4890.[PubMed]
41. Caldwell R,, Sapolsky R,, Weyler W,, Maile RR,, Causey SC,, Ferrari E . 2001. Correlation between Bacillus subtilis scoC phenotype and gene expression determined using microarrays for transcriptome analysis. J Bacteriol 183 : 7329– 7340.[PubMed] [CrossRef]
42. Eichenberger P,, Fujita M,, Jensen ST,, Conlon EM,, Rudner DZ,, Wang ST,, Ferguson C,, Haga K,, Sato T,, Liu JS,, Losick R . 2004. The program of gene transcription for a single differentiating cell type during sporulation in Bacillus subtilis . PLoS Biol 2 : e328. doi:10.1371/journal.pbio.0020328. [PubMed] [CrossRef]
43. Wang ST,, Setlow B,, Conlon EM,, Lyon JL,, Imamura D,, Sato T,, Setlow P,, Losick R,, Eichenberger P . 2006. The forespore line of gene expression in Bacillus subtilis . J Mol Biol 358 : 16– 37.[PubMed] [CrossRef]
44. Steil L,, Serrano M,, Henriques AO,, Volker U . 2005. Genome-wide analysis of temporally regulated and compartment-specific gene expression in sporulating cells of Bacillus subtilis . Microbiology 151 : 399– 420.[PubMed] [CrossRef]
45. Eichenberger P,, Jensen ST,, Conlon EM,, van Ooij C,, Silvaggi J,, Gonzalez-Pastor JE,, Fujita M,, Ben-Yehuda S,, Stragier P,, Liu JS,, Losick R . 2003. The sigmaE regulon and the identification of additional sporulation genes in Bacillus subtilis . J Mol Biol 327 : 945– 972.[PubMed]
46. Feucht A,, Evans L,, Errington J . 2003. Identification of sporulation genes by genome-wide analysis of the sigmaE regulon of Bacillus subtilis . Microbiology 149 : 3023– 3034.[PubMed]
47. Imamura D,, Kobayashi K,, Sekiguchi J,, Ogasawara N,, Takeuchi M,, Sato T . 2004. spoIVH ( ykvV), a requisite cortex formation gene, is expressed in both sporulating compartments of Bacillus subtilis . J Bacteriol 186 : 5450– 5459.[PubMed] [CrossRef]
48. Dworkin J,, Losick R . 2005. Developmental commitment in a bacterium. Cell 121 : 401– 409.[PubMed] [CrossRef]
49. Nicolas P,, Mader U,, Dervyn E,, Rochat T,, Leduc A,, Pigeonneau N,, Bidnenko E,, Marchadier E,, Hoebeke M,, Aymerich S,, Becher D,, Bisicchia P,, Botella E,, Delumeau O,, Doherty G,, Denham EL,, Fogg MJ,, Fromion V,, Goelzer A,, Hansen A,, Hartig E,, Harwood CR,, Homuth G,, Jarmer H,, Jules M,, Klipp E,, Le Chat L,, Lecointe F,, Lewis P,, Liebermeister W,, March A,, Mars RA,, Nannapaneni P,, Noone D,, Pohl S,, Rinn B,, Rugheimer F,, Sappa PK,, Samson F,, Schaffer M,, Schwikowski B,, Steil L,, Stulke J,, Wiegert T,, Devine KM,, Wilkinson AJ,, van Dijl JM,, Hecker M,, Volker U,, Bessieres P,, Noirot P . 2012. Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis . Science 335 : 1103– 1106.[PubMed] [CrossRef]
50. Passalacqua KD,, Varadarajan A,, Ondov BD,, Okou DT,, Zwick ME,, Bergman NH . 2009. Structure and complexity of a bacterial transcriptome. J Bacteriol 191 : 3203– 3211.[PubMed] [CrossRef]
51. Jones SW,, Paredes CJ,, Tracy B,, Cheng N,, Sillers R,, Senger RS,, Papoutsakis ET . 2008. The transcriptional program underlying the physiology of clostridial sporulation. Genome Biol 9 : R114. doi:10.1186/gb-2008-9-7-r114. [PubMed] [CrossRef]
52. Bateman A,, Birney E,, Durbin R,, Eddy SR,, Howe KL,, Sonnhammer EL . 2000. The Pfam protein families database. Nucleic Acids Res 28 : 263– 266.[PubMed]
53. Ishii T,, Yoshida K,, Terai G,, Fujita Y,, Nakai K . 2001. DBTBS: a database of Bacillus subtilis promoters and transcription factors. Nucleic Acids Res 29 : 278– 280.[PubMed]
54. Waters LS,, Storz G . 2009. Regulatory RNAs in bacteria. Cell 136 : 615– 628.[PubMed] [CrossRef]
55. Livny J,, Waldor MK . 2007. Identification of small RNAs in diverse bacterial species. Curr Opin Microbiol 10 : 96– 101.[PubMed] [CrossRef]
56. Rasmussen S,, Nielsen HB,, Jarmer H . 2009. The transcriptionally active regions in the genome of Bacillus subtilis . Mol Microbiol 73 : 1043– 1057.[PubMed] [CrossRef]
57. Irnov I,, Sharma CM,, Vogel J,, Winkler WC . 2010. Identification of regulatory RNAs in Bacillus subtilis . Nucleic Acids Res 38 : 6637– 6651.[PubMed] [CrossRef]
58. Silvaggi JM,, Perkins JB,, Losick R . 2006. Genes for small, noncoding RNAs under sporulation control in Bacillus subtilis . J Bacteriol 188 : 532– 541.[PubMed] [CrossRef]
59. Schmalisch M,, Maiques E,, Nikolov L,, Camp AH,, Chevreux B,, Muffler A,, Rodriguez S,, Perkins J,, Losick R . 2010. Small genes under sporulation control in the Bacillus subtilis genome. J Bacteriol 192 : 5402– 5412.[PubMed] [CrossRef]
60. Hutchison CA,, Peterson SN,, Gill SR,, Cline RT,, White O,, Fraser CM,, Smith HO,, Venter JC . 1999. Global transposon mutagenesis and a minimal Mycoplasma genome. Science 286 : 2165– 2169.[PubMed]
61. Kobayashi K,, Ehrlich SD,, Albertini A,, Amati G,, Andersen KK,, Arnaud M,, Asai K,, Ashikaga S,, Aymerich S,, Bessieres P,, Boland F,, Brignell SC,, Bron S,, Bunai K,, Chapuis J,, Christiansen LC,, Danchin A,, Debarbouille M,, Dervyn E,, Deuerling E,, Devine K,, Devine SK,, Dreesen O,, Errington J,, Fillinger S,, Foster SJ,, Fujita Y,, Galizzi A,, Gardan R,, Eschevins C,, Fukushima T,, Haga K,, Harwood CR,, Hecker M,, Hosoya D,, Hullo MF,, Kakeshita H,, Karamata D,, Kasahara Y,, Kawamura F,, Koga K,, Koski P,, Kuwana R,, Imamura D,, Ishimaru M,, Ishikawa S,, Ishio I,, Le Coq D,, Masson A,, Mauel C,, Meima R,, Mellado RP,, Moir A,, Moriya S,, Nagakawa E,, Nanamiya H,, Nakai S,, Nygaard P,, Ogura M,, Ohanan T,, O’Reilly M,, O’Rourke M,, Pragai Z,, Pooley HM,, Rapoport G,, Rawlins JP,, Rivas LA,, Rivolta C,, Sadaie A,, Sadaie Y,, Sarvas M,, Sato T,, Saxild HH,, Scanlan E,, Schumann W,, Seegers JF,, Sekiguchi J,, Sekowska A,, Seror SJ,, Simon M,, Stragier P,, Studer R,, Takamatsu H,, Tanaka T,, Takeuchi M,, Thomaides HB,, Vagner V,, van Dijl JM,, Watabe K,, Wipat A,, Yamamoto H,, Yamamoto M,, Yamamoto Y,, Yamane K,, Yata K,, Yoshida K,, Yoshikawa H,, Zuber U,, Ogasawara N . 2003. Essential Bacillus subtilis genes. Proc Natl Acad Sci USA 100 : 4678– 4683.[PubMed] [CrossRef]
62. Commichau FM,, Pietack N,, Stulke J . 2013. Essential genes in Bacillus subtilis: a re-evaluation after ten years. Mol Biosyst 9 : 1068– 1075.[PubMed] [CrossRef]
63. van Opijnen T,, Bodi KL,, Camilli A . 2009. Tn-seq: high-throughput parallel sequencing for fitness and genetic interaction studies in microorganisms. Nat Methods 6 : 767– 772.[PubMed] [CrossRef]
64. Tong AH,, Evangelista M,, Parsons AB,, Xu H,, Bader GD,, Page N,, Robinson M,, Raghibizadeh S,, Hogue CW,, Bussey H,, Andrews B,, Tyers M,, Boone C . 2001. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294 : 2364– 2368.[PubMed] [CrossRef]
65. Jorgensen P,, Nelson B,, Robinson MD,, Chen Y,, Andrews B,, Tyers M,, Boone C . 2002. High-resolution genetic mapping with ordered arrays of Saccharomyces cerevisiae deletion mutants. Genetics 162 : 1091– 1099.[PubMed]
66. Costanzo M,, Baryshnikova A,, Bellay J,, Kim Y,, Spear ED,, Sevier CS,, Ding H,, Koh JL,, Toufighi K,, Mostafavi S,, Prinz J,, St Onge RP,, VanderSluis B,, Makhnevych T,, Vizeacoumar FJ,, Alizadeh S,, Bahr S,, Brost RL,, Chen Y,, Cokol M,, Deshpande R,, Li Z,, Lin ZY,, Liang W,, Marback M,, Paw J,, San Luis BJ,, Shuteriqi E,, Tong AH,, van Dyk N,, Wallace IM,, Whitney JA,, Weirauch MT,, Zhong G,, Zhu H,, Houry WA,, Brudno M,, Ragibizadeh S,, Papp B,, Pal C,, Roth FP,, Giaever G,, Nislow C,, Troyanskaya OG,, Bussey H,, Bader GD,, Gingras AC,, Morris QD,, Kim PM,, Kaiser CA,, Myers CL,, Andrews BJ,, Boone C . 2010. The genetic landscape of a cell. Science 327 : 425– 431.[PubMed] [CrossRef]
67. Nichols RJ,, Sen S,, Choo YJ,, Beltrao P,, Zietek M,, Chaba R,, Lee S,, Kazmierczak KM,, Lee KJ,, Wong A,, Shales M,, Lovett S,, Winkler ME,, Krogan NJ,, Typas A,, Gross CA . 2011. Phenotypic landscape of a bacterial cell. Cell 144 : 143– 156.[PubMed] [CrossRef]
68. Kuwana R,, Kasahara Y,, Fujibayashi M,, Takamatsu H,, Ogasawara N,, Watabe K . 2002. Proteomics characterization of novel spore proteins of Bacillus subtilis . Microbiology 148 : 3971– 3982.[PubMed]
69. Lai EM,, Phadke ND,, Kachman MT,, Giorno R,, Vazquez S,, Vazquez JA,, Maddock JR,, Driks A . 2003. Proteomic analysis of the spore coats of Bacillus subtilis and Bacillus anthracis . J Bacteriol 185 : 1443– 1454.[PubMed]
70. Abhyankar W,, Beek AT,, Dekker H,, Kort R,, Brul S,, de Koster CG . 2011. Gel-free proteomic identification of the Bacillus subtilis insoluble spore coat protein fraction. Proteomics 11 : 4541– 4550.[PubMed] [CrossRef]
71. Ong SE,, Blagoev B,, Kratchmarova I,, Kristensen DB,, Steen H,, Pandey A,, Mann M . 2002. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 1 : 376– 386.[PubMed]
72. Soufi B,, Kumar C,, Gnad F,, Mann M,, Mijakovic I,, Macek B . 2010. Stable isotope labeling by amino acids in cell culture (SILAC) applied to quantitative proteomics of Bacillus subtilis . J Proteome Res 9 : 3638– 3646.[PubMed] [CrossRef]
73. Marchadier E,, Carballido-Lopez R,, Brinster S,, Fabret C,, Mervelet P,, Bessieres P,, Noirot-Gros MF,, Fromion V,, Noirot P . 2011. An expanded protein-protein interaction network in Bacillus subtilis reveals a group of hubs: exploration by an integrative approach. Proteomics 11 : 2981– 2991.[PubMed] [CrossRef]
74. Huh WK,, Falvo JV,, Gerke LC,, Carroll AS,, Howson RW,, Weissman JS,, O’Shea EK . 2003. Global analysis of protein localization in budding yeast. Nature 425 : 686– 691.[PubMed] [CrossRef]
75. Werner JN,, Chen EY,, Guberman JM,, Zippilli AR,, Irgon JJ,, Gitai Z . 2009. Quantitative genome-scale analysis of protein localization in an asymmetric bacterium. Proc Natl Acad Sci USA 106 : 7858– 7863.[PubMed] [CrossRef]
76. McKenney PT,, Driks A,, Eskandarian HA,, Grabowski P,, Guberman J,, Wang KH,, Gitai Z,, Eichenberger P . 2010. A distance-weighted interaction map reveals a previously uncharacterized layer of the Bacillus subtilis spore coat. Curr Biol 20 : 934– 938.[PubMed] [CrossRef]
77. McKenney PT,, Eichenberger P . 2012. Dynamics of spore coat morphogenesis in Bacillus subtilis . Mol Microbiol 83 : 245– 260.[PubMed] [CrossRef]
78. Watrous J,, Roach P,, Alexandrov T,, Heath BS,, Yang JY,, Kersten RD,, van der Voort M,, Pogliano K,, Gross H,, Raaijmakers JM,, Moore BS,, Laskin J,, Bandeira N,, Dorrestein PC . 2012. Mass spectral molecular networking of living microbial colonies. Proc Natl Acad Sci USA 109 : E1743– E1752.[PubMed] [CrossRef]
79. Yang YL,, Xu Y,, Straight P,, Dorrestein PC . 2009. Translating metabolic exchange with imaging mass spectrometry. Nat Chem Biol 5 : 885– 887.[PubMed] [CrossRef]
80. Kanehisa M,, Goto S,, Sato Y,, Furumichi M,, Tanabe M . 2012. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 40 : D109– D114.[PubMed] [CrossRef]
81. Plata G,, Fuhrer T,, Hsiao TL,, Sauer U,, Vitkup D . 2012. Global probabilistic annotation of metabolic networks enables enzyme discovery. Nat Chem Biol 8 : 848– 854.[PubMed] [CrossRef]
82. Wunschel D,, Fox KF,, Black GE,, Fox A . 1994. Discrimination among the B. cereus group, in comparison to B. subtilis, by structural carbohydrate profiles and ribosomal RNA spacer region PCR. Syst Appl Microbiol 17 : 625– 635.
83. Ishii N,, Nakahigashi K,, Baba T,, Robert M,, Soga T,, Kanai A,, Hirasawa T,, Naba M,, Hirai K,, Hoque A,, Ho PY,, Kakazu Y,, Sugawara K,, Igarashi S,, Harada S,, Masuda T,, Sugiyama N,, Togashi T,, Hasegawa M,, Takai Y,, Yugi K,, Arakawa K,, Iwata N,, Toya Y,, Nakayama Y,, Nishioka T,, Shimizu K,, Mori H,, Tomita M . 2007. Multiple high-throughput analyses monitor the response of E. coli to perturbations. Science 316 : 593– 597.[PubMed] [CrossRef]
84. Goelzer A,, Bekkal Brikci F,, Martin-Verstraete I,, Noirot P,, Bessieres P,, Aymerich S,, Fromion V . 2008. Reconstruction and analysis of the genetic and metabolic regulatory networks of the central metabolism of Bacillus subtilis . BMC Syst Biol 2 : 20. doi:10.1186/1752-0509-2-20. [PubMed] [CrossRef]
85. Oh YK,, Palsson BO,, Park SM,, Schilling CH,, Mahadevan R . 2007. Genome-scale reconstruction of metabolic network in Bacillus subtilis based on high-throughput phenotyping and gene essentiality data. J Biol Chem 282 : 28791– 28799.[PubMed] [CrossRef]
86. Gollnick P,, Babitzke P,, Antson A,, Yanofsky C . 2005. Complexity in regulation of tryptophan biosynthesis in Bacillus subtilis . Annu Rev Genet 39 : 47– 68.[PubMed] [CrossRef]
87. Bonneau R,, Facciotti MT,, Reiss DJ,, Schmid AK,, Pan M,, Kaur A,, Thorsson V,, Shannon P,, Johnson MH,, Bare JC,, Longabaugh W,, Vuthoori M,, Whitehead K,, Madar A,, Suzuki L,, Mori T,, Chang DE,, Diruggiero J,, Johnson CH,, Hood L,, Baliga NS . 2007. A predictive model for transcriptional control of physiology in a free living cell. Cell 131 : 1354– 1365.[PubMed] [CrossRef]
88. Waltman P,, Kacmarczyk T,, Bate AR,, Kearns DB,, Reiss DJ,, Eichenberger P,, Bonneau R . 2010. Multi-species integrative biclustering. Genome Biol 11 : R96. doi:10.1186/gb-2010-11-9-r96. [PubMed] [CrossRef]
89. Fadda A,, Fierro AC,, Lemmens K,, Monsieurs P,, Engelen K,, Marchal K . 2009. Inferring the transcriptional network of Bacillus subtilis . Mol Biosyst 5 : 1840– 1852.[PubMed] [CrossRef]
90. Buescher JM,, Liebermeister W,, Jules M,, Uhr M,, Muntel J,, Botella E,, Hessling B,, Kleijn RJ,, Le Chat L,, Lecointe F,, Mader U,, Nicolas P,, Piersma S,, Rugheimer F,, Becher D,, Bessieres P,, Bidnenko E,, Denham EL,, Dervyn E,, Devine KM,, Doherty G,, Drulhe S,, Felicori L,, Fogg MJ,, Goelzer A,, Hansen A,, Harwood CR,, Hecker M,, Hubner S,, Hultschig C,, Jarmer H,, Klipp E,, Leduc A,, Lewis P,, Molina F,, Noirot P,, Peres S,, Pigeonneau N,, Pohl S,, Rasmussen S,, Rinn B,, Schaffer M,, Schnidder J,, Schwikowski B,, Van Dijl JM,, Veiga P,, Walsh S,, Wilkinson AJ,, Stelling J,, Aymerich S,, Sauer U . 2012. Global network reorganization during dynamic adaptations of Bacillus subtilis metabolism. Science 335 : 1099– 1103.[PubMed] [CrossRef]
91. Greenfield A,, Hafemeister C,, Bonneau R . 2013. Robust data-driven incorporation of prior knowledge into the inference of dynamic regulatory networks. Bioinformatics 29 : 1060– 1067.[PubMed] [CrossRef]
92. Flórez LA,, Roppel SF,, Schmeisky AG,, Lammers CR,, Stülke J . 2009. A community-curated consensual annotation that is continuously updated: the Bacillus subtilis centered wiki SubtiWiki. Database (Oxford) 2009 : bap012. doi:10.1093/database/bap012 [PubMed] [CrossRef]
93. Mader U,, Schmeisky AG,, Florez LA,, Stulke J . 2012. SubtiWiki--a comprehensive community resource for the model organism Bacillus subtilis . Nucleic Acids Res 40 : D1278– D1287.[PubMed] [CrossRef]
94. Marbach D,, Costello JC,, Küffner R,, Vega NM,, Prill RJ,, Camacho DM,, Allison KR,; DREAM5 Consortium, Kellis M,, Collins JJ,, Stolovitzky G . 2012. Wisdom for crowds for robust gene network inference. Nat Methods 9 : 796– 804.[PubMed] [CrossRef]
95. Moszer I,, Glaser P,, Danchin A . 1995. SubtiList: a relational database for the Bacillus subtilis genome. Microbiology 141 : 261– 268.[PubMed]
96. Moszer I,, Jones LM,, Moreira S,, Fabry C,, Danchin A . 2002. SubtiList: the reference database for the Bacillus subtilis genome. Nucleic Acids Res 30 : 62– 65.[PubMed]
97. Lechat P,, Hummel L,, Rousseau S,, Moszer I . 2008. GenoList: an integrated environment for comparative analysis of microbial genomes. Nucleic Acids Res 36 : D469– D474.[PubMed] [CrossRef]
98. Killcoyne S,, Carter GW,, Smith J,, Boyle J . 2009. Cytoscape: a community-based framework for network modeling. Methods Mol Biol 563 : 219– 239.[PubMed] [CrossRef]
99. Smoot ME,, Ono K,, Ruscheinski J,, Wang PL,, Ideker T . 2011. Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27 : 431– 432.[PubMed] [CrossRef]
100. Shannon PT,, Reiss DJ,, Bonneau R,, Baliga NS . 2006. The Gaggle: an open-source software system for integrating bioinformatics software and data sources. BMC Bioinformatics 7 : 176. doi:10.1186/1471-2105-7-176 [PubMed] [CrossRef]
101. Kacmarczyk T,, Waltman P,, Bate A,, Eichenberger P,, Bonneau R . 2011. Comparative microbial modules resource: generation and visualization of multi-species biclusters. PLoS Comput Biol 7 : e1002228. doi:10.1371/journal.pcbi.1002228 [PubMed] [CrossRef]
102. Beauregard PB,, Chai Y,, Vlamakis H,, Losick R,, Kolter R . 2013. Bacillus subtilis biofilm induction by plant polysaccharides. Proc Natl Acad Sci USA 110 : E1621– E1630.[PubMed] [CrossRef]
103. Karr JR,, Sanghvi JC,, Macklin DN,, Gutschow MV,, Jacobs JM,, Bolival B Jr,, Assad-Garcia N,, Glass JI,, Covert MW . 2012. A whole-cell computational model predicts phenotype from genotype. Cell 150 : 389– 401.[PubMed] [CrossRef]
104. McKenney PT,, Driks A,, Eichenberger P . 2013. The Bacillus subtilis endospore: assembly and functions of the multilayered coat. Nat Rev Microbiol 11 : 33– 44.[PubMed] [CrossRef]
105. Fajardo-Cavazos P,, Maughan H,, Nicholson WL, . Evolution in the Bacillaceae . In Eichenberger P,, Driks A (ed), The Bacterial Spore. ASM Press, Washington, DC, in press.
106. Mandic-Mulec I,, Stefanic P,, van Elsas JD, . Ecology of Bacillaceae . In Eichenberger P,, Driks A (ed), The Bacterial Spore. ASM Press, Washington, DC, in press.
107. Galperin MY . 2013. Genomic diversity of spore-forming Firmicutes . Microbiol Spectrum 1 : TBS-0015-2012.
108. Dürre P . 2014. Physiology and sporulation in Clostridium . Microbiol Spectrum 2 : TBS-0010-2012.
109. Dworkin J . 2014. Protein targeting during Bacillus subtilis sporulation. Microbiol Spectrum 2 : TBS-0006-2013.
110. Francis MB,, Allen CA,, Shrestha R,, Sorg JA . 2013. Bile acid recognition by the Clostridium difficile germinant receptor, CspC, is important for establishing infection. PLoS Pathog 9 : e1003356.
111. Meeske AJ,, Rodrigues CD,, Brady J,, Lim HC,, Berharnd TG,, Rudner DZ . 2016. High-throughput genetic screens identify a large and diverse collection of new sporulation genes in Bacillus subtilis . PLoS Biol 14 : e1002341.
112. Arrieta-Ortiz ML,, Hafemeister C,, Bate AR,, Chu T,, Greenfield A,, Shuster B,, Barry SN,, Gallitto M,, Liu B,, Kacmarczyk T,, Santoriello F,, Chen J,, Rodrigues CD,, Sato T,, Rudner DZ,, Driks A,, Bonneau R,, Eichenberger P . 2015. An experimentally supported model of the Bacillus subtilis global transcriptional regulatory network. Mol Syst Biol 11 : 839.

Back to top
This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error