title: Interspecies interactions that result in Bacillus subtilis forming biofilms are mediated mainly by members of its own genus.
abstract: Many different systems of bacterial interactions have been described. However, relatively few studies have explored how interactions between different microorganisms might influence bacterial development. To explore such interspecies interactions, we focused on Bacillus subtilis, which characteristically develops into matrix-producing cannibals before entering sporulation. We investigated whether organisms from the natural environment of B. subtilis--the soil--were able to alter the development of B. subtilis. To test this possibility, we developed a coculture microcolony screen in which we used fluorescent reporters to identify soil bacteria able to induce matrix production in B. subtilis. Most of the bacteria that influence matrix production in B. subtilis are members of the genus Bacillus, suggesting that such interactions may be predominantly with close relatives. The interactions we observed were mediated via two different mechanisms. One resulted in increased expression of matrix genes via the activation of a sensor histidine kinase, KinD. The second was kinase independent and conceivably functions by altering the relative subpopulations of B. subtilis cell types by preferentially killing noncannibals. These two mechanisms were grouped according to the inducing strain's relatedness to B. subtilis. Our results suggest that bacteria preferentially alter their development in response to secreted molecules from closely related bacteria and do so using mechanisms that depend on the phylogenetic relatedness of the interacting bacteria.
authors.affiliation: Department of Microbiology and Immunobiology, Harvard Medical School, Boston, MA 02115, USA.
authors.forename: Elizabeth A
authors.initials: EA
authors.lastname: Shank
authors.forename: Vanja
authors.initials: V
authors.lastname: Klepac-Ceraj
authors.forename: Leonardo
authors.initials: L
authors.lastname: Collado-Torres
authors.forename: Gordon E
authors.initials: GE
authors.lastname: Powers
authors.forename: Richard
authors.initials: R
authors.lastname: Losick
authors.forename: Roberto
authors.initials: R
authors.lastname: Kolter
mesh_terms: D001412:Bacillus subtilis / Q000502:physiology*; D001426:Bacterial Proteins / Q000378:metabolism*; D001483:Base Sequence; D018441:Biofilms / Q000254:growth & development*; D005109:Extracellular Matrix / Q000378:metabolism*; D005453:Fluorescence; D015964:Gene Expression Regulation, Bacterial / Q000502:physiology*; D016013:Likelihood Functions; D050296:Microbial Viability; D008957:Models, Genetic; D008969:Molecular Sequence Data; D010802:Phylogeny; D053038:Quorum Sensing / Q000502:physiology*; D012336:RNA, Ribosomal, 16S / Q000235:genetics; D017422:Sequence Analysis, DNA; D012988:Soil Microbiology; D013045:Species Specificity
chemical_list: D001426:Bacterial Proteins; D012336:RNA, Ribosomal, 16S
references.citation: Mol Microbiol. 2006 May;60(3):765-82
references.pmid: 16629676
references.citation: Appl Environ Microbiol. 2001 Oct;67(10):4399-406
references.pmid: 11571135
references.citation: J Bacteriol. 1994 Jan;176(2):269-75
references.pmid: 8288518
references.citation: J Bacteriol. 1967 Jun;93(6):1888-96
references.pmid: 4960897
references.citation: FEMS Microbiol Rev. 2010 Mar;34(2):134-49
references.pmid: 20030732
references.citation: Genes Dev. 1993 Feb;7(2):283-94
references.pmid: 8436298
references.citation: Curr Biol. 2010 Sep 14;20(17):R735-45
references.pmid: 20833318
references.citation: Mol Microbiol. 2006 Feb;59(4):1216-28
references.pmid: 16430695
references.citation: BMC Bioinformatics. 2006 May 04;7:240
references.pmid: 16672074
references.citation: Cell. 2006 Feb 10;124(3):549-59
references.pmid: 16469701
references.citation: J Ind Microbiol Biotechnol. 2006 Jul;33(7):496-9
references.pmid: 16552582
references.citation: Mol Microbiol. 2000 Nov;38(3):535-42
references.pmid: 11069677
references.citation: J Bacteriol. 1999 Sep;181(17):5476-81
references.pmid: 10464223
references.citation: FEMS Microbiol Rev. 2011 May;35(3):415-24
references.pmid: 20955377
references.citation: Mol Microbiol. 2009 Nov;74(3):609-18
references.pmid: 19775247
references.citation: Genes Dev. 2008 Apr 1;22(7):945-53
references.pmid: 18381896
references.citation: Syst Biol. 2008 Oct;57(5):758-71
references.pmid: 18853362
references.citation: Annu Rev Microbiol. 2009;63:99-118
references.pmid: 19566421
references.citation: Mol Microbiol. 2001 Dec;42(5):1199-209
references.pmid: 11886552
references.citation: Nat Rev Microbiol. 2007 Sep;5(9):689-99
references.pmid: 17676055
references.citation: Biometrics. 1987 Dec;43(4):783-91
references.pmid: 3427163
references.citation: J Bacteriol. 2005 Feb;187(4):1357-68
references.pmid: 15687200
references.citation: Curr Opin Microbiol. 2009 Apr;12(2):205-14
references.pmid: 19251475
references.citation: Proc Natl Acad Sci U S A. 2010 Sep 14;107(37):16286-90
references.pmid: 20805502
references.citation: Mol Microbiol. 2004 May;52(3):847-60
references.pmid: 15101989
references.citation: Annu Rev Microbiol. 2008;62:193-210
references.pmid: 18537474
references.citation: Mol Microbiol. 2003 Dec;50(5):1683-701
references.pmid: 14651647
references.citation: FEBS Lett. 2007 Jan 9;581(1):151-6
references.pmid: 17184776
references.citation: Bioinformatics. 2004 Sep 22;20(14):2317-9
references.pmid: 15073015
references.citation: J Bacteriol. 2004 Feb;186(4):1136-46
references.pmid: 14762009
references.citation: Annu Rev Cell Dev Biol. 2005;21:319-46
references.pmid: 16212498
references.citation: Mol Microbiol. 2009 Nov;74(4):876-87
references.pmid: 19788541
references.citation: Nucleic Acids Res. 2007;35(21):7188-96
references.pmid: 17947321
references.citation: Mol Microbiol. 2008 Jan;67(2):254-63
references.pmid: 18047568
references.citation: mBio. 2010 May 18;1(1):
references.pmid: 20689749
references.citation: Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11621-6
references.pmid: 11572999
references.citation: Science. 2003 Jul 25;301(5632):510-3
references.pmid: 12817086
references.citation: J Virol. 1974 Apr;13(4):916-21
references.pmid: 4206943
references.citation: FEMS Microbiol Ecol. 2004 May 1;48(2):119-27
references.pmid: 19712395
references.citation: Trends Microbiol. 2008 Jun;16(6):269-75
references.pmid: 18467096
references.citation: Genes Dev. 2010 Apr 15;24(8):754-65
references.pmid: 20351052
references.citation: J Bacteriol. 2009 Nov;191(22):6822-32
references.pmid: 19767430
references.citation: Science. 2006 Feb 24;311(5764):1113-6
references.pmid: 16497924
references.citation: FEMS Microbiol Rev. 2009 Jan;33(1):152-63
references.pmid: 19054118
references.citation: Mol Microbiol. 2005 Feb;55(3):739-49
references.pmid: 15661000
references.citation: Cell Mol Life Sci. 2002 Mar;59(3):410-6
references.pmid: 11964119
references.citation: Genes Dev. 2005 Dec 15;19(24):3083-94
references.pmid: 16357223
references.citation: Mol Microbiol. 2008 Jun;68(5):1117-27
references.pmid: 18430133
references.citation: Proc Natl Acad Sci U S A. 2010 Feb 2;107(5):2230-4
references.pmid: 20080671
references.citation: Microbiology (Reading). 2008 Jul;154(Pt 7):1845-1858
references.pmid: 18599814
references.citation: Mol Microbiol. 2006 Feb;59(4):1229-38
references.pmid: 16430696
references.citation: J Bacteriol. 2007 Jul;189(13):4920-31
references.pmid: 17468240
references.citation: Mol Microbiol. 2010 Oct;78(1):218-29
references.pmid: 20923420
references.citation: Proc Natl Acad Sci U S A. 2009 Jan 6;106(1):280-5
references.pmid: 19114652