Cell differentiation in a bacillus thuringiensis population during planktonic growth, biofilm formation, and host infection

mBio

Volumn 6, Issue 3, 2015, Pages 1-10

  Verplaetse, Emilie ^a   Slamti, Leyla ^a   Gohar, Michel ^a   Lereclus, Didier ^a  

^a UMR1319 MICALIS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; BACILLUS THURINGIENSIS; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERIUM CULTURE; BIOFILM; CELL DIFFERENTIATION; CELL HETEROGENEITY; CELL LINEAGE; CONTROLLED STUDY; CULTURE MEDIUM; EVOLUTIONARY ADAPTATION; HOST PATHOGEN INTERACTION; INSECT CELL; NONHUMAN; NPRR GENE; PLCR GENE; PRIORITY JOURNAL; QUORUM SENSING; SINGLE CELL ANALYSIS; SPO0A GENE; SPOROGENESIS; ADAPTATION; ANIMAL; BACTERIAL SPORE; CHEMISTRY; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; INSECT; LARVA; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

BACILLUS THURINGIENSIS; HEXAPODA;

BACTERIAL PROTEIN; CULTURE MEDIUM; PLCR PROTEIN, BACILLUS; TRANSACTIVATOR PROTEIN;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; BIOFILMS; CELL DIFFERENTIATION; CULTURE MEDIA; GENE EXPRESSION REGULATION, BACTERIAL; INSECTS; LARVA; QUORUM SENSING; SPORES, BACTERIAL; TRANS-ACTIVATORS;

EID: 84936934052     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00138-15     Document Type: Article

References (42)

1. López D, Vlamakis H, Kolter R. 2010. Biofilms. Cold Spring Harb Perspect Biol 2:a000398. http://dx.doi.org/10.1101/cshperspect.a000398.
2. Marlow VL, Cianfanelli FR, Porter M, Cairns LS, Dale JK, Stanley-Wall NR. 2014. The prevalence and origin of exoprotease-producing cells in the Bacillus subtilis biofilm. Microbiology 160:56-66. http://dx.doi.org/ 10.1099/mic.0.072389-0.
3. Vlamakis H, Aguilar C, Losick R, Kolter R. 2008. Control of cell fate by the formation of an architecturally complex bacterial community. Genes Dev 22:945-953. http://dx.doi.org/10.1101/gad.1645008.
4. Zottola EA, Sasahara KC. 1994. Microbial biofilms in the food processing industry-should they be a concern? Int J Food Microbiol 23:125-148. http://dx.doi.org/10.1016/0168-1605(94)90047-7.
5. 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 423:87-91. http://dx.doi.org/10.1038/ nature01582.
6. Agaisse H, Gominet M, Okstad OA, Kolstø AB, Lereclus D. 1999. PlcR is a pleiotropic regulator of extracellular virulence factor gene expression in Bacillus thuringiensis. Mol Microbiol 32:1043-1053. http://dx.doi.org/ 10.1046/j.1365-2958.1999.01419.x.
7. Perchat S, Dubois T, Zouhir S, Gominet M, Poncet S, Lemy C, Aumont-Nicaise M, Deutscher J, Gohar M, Nessler S, Lereclus D. 2011. A cell-cell communication system regulates protease production during sporulation in bacteria of the Bacillus cereus group. Mol Microbiol 82: 619-633. http://dx.doi.org/10.1111/j.1365-2958.2011.07839.x.
8. Slamti L, Perchat S, Huillet E, Lereclus D. 2014. Quorum sensing in Bacillus thuringiensis is required for completion of a full infectious cycle in the insect. Toxins (Basel) 6:-2239-2255. http://dx.doi.org/10.3390/ toxins6082239.
9. Salamitou S, Ramisse F, Brehélin M, Bourguet D, Gilois N, Gominet M, Hernandez E, Lereclus D. 2000. The PlcR regulon is involved in the opportunistic properties of Bacillus thuringiensis and Bacillus cereus in mice and insects. Microbiology 146:2825-2832.
10. Dubois T, Perchat S, Verplaetse E, Gominet M, Lemy C, Aumont-Nicaise M, Grenha R, Nessler S, Lereclus D. 2013. Activity of the Bacillus thuringiensis NprR-NprX cell-cell communication system is co-ordinated to the physiological stage through a complex transcriptional regulation. Mol Microbiol 88:48-63. http://dx.doi.org/10.1111/mmi.12168.
11. Dubois T, Faegri K, Perchat S, Lemy C, Buisson C, Nielsen-LeRoux C, Gohar M, Jacques P, Ramarao N, Kolstø AB, Lereclus D. 2012. Necrotrophism is a quorum-sensing-regulated lifestyle in Bacillus thuringiensis. PLoS Pathog 8:e1002629. http://dx.doi.org/10.1371/journal.ppat.1002629.
12. Bongiorni C, Stoessel R, Shoemaker D, Perego M. 2006. Rap phosphatase of virulence plasmid pXO1 inhibits Bacillus anthracis sporulation. J Bacteriol 188:487-498. http://dx.doi.org/10.1128/JB.188.2.487-498.2006.
13. Cabrera R, Rocha J, Flores V, Vázquez-Moreno L, Guarneros G, Olmedo G, Rodríguez-Romero A, de la Torre M. 2014. Regulation of sporulation initiation by NprR and its signaling peptide NprRB: molecular recognition and conformational changes. Appl Microbiol Biotechnol 98:9399-9412. http://dx.doi.org/10.1007/s00253-014-6094-8.
14. Lereclus D, Agaisse H, Grandvalet C, Salamitou S, Gominet M. 2000. Regulation of toxin and virulence gene transcription in Bacillus thuringiensis. Int J Med Microbiol 290:295-299. http://dx.doi.org/10.1016/ S1438-4221(00)80024-7.
15. Ceuppens S, Timmery S, Mahillon J, Uyttendaele M, Boon N. 2013. Small Bacillus cereus ATCC 14579 subpopulations are responsible for cytotoxin K production. J Appl Microbiol 114:899-906. http://dx.doi.org/ 10.1111/jam.12096.
16. Eijlander RT, Kuipers OP. 2013. Live-cell imaging tool optimization to study gene expression levels and dynamics in single cells of Bacillus cereus. Appl Environ Microbiol 79:5643-5651. http://dx.doi.org/10.1128/ AEM.01347-13.
17. Fagerlund A, Dubois T, Økstad OA, Verplaetse E, Gilois N, Bennaceur I, Perchat S, Gominet M, Aymerich S, Kolstø AB, Lereclus D, GoharM. 2014. SinR controls enterotoxin expression in Bacillus thuringiensis biofilms. PLoS One 9:e87532. http://dx.doi.org/10.1371/journal.pone.0087532.
18. Merrell DS, Camilli A. 2000. Detection and analysis of gene expression during infection by in vivo expression technology. Philos Trans R Soc Lond B Biol Sci 355:587-599. http://dx.doi.org/10.1098/rstb.2000.0600.
19. Fedhila S, Daou N, Lereclus D, Nielsen-LeRoux C. 2006. Identification of Bacillus cereus internalin and other candidate virulence genes specifically induced during oral infection in insects. Mol Microbiol 62:339-355. http://dx.doi.org/10.1111/j.1365-2958.2006.05362.x.
20. Slauch JM, Mahan MJ, Mekalanos JJ. 1994. In vivo expression technology for selection of bacterial genes specifically induced in host tissues. Methods Enzymol 235:481-492.
21. Nielsen AT, Dolganov NA, Rasmussen T, Otto G, Miller MC, Felt SA, Torreilles S, Schoolnik GK. 2010. A bistable switch and anatomical site control Vibrio cholerae virulence gene expression in the intestine. PLoS Pathog 6:e1001102. http://dx.doi.org/10.1371/journal.ppat.1001102.
22. Uliczka F, Pisano F, Kochut A, Opitz W, Herbst K, Stolz T, Dersch P. 2011. Monitoring of gene expression in bacteria during infections using an adaptable set of bioluminescent, fluorescent and colorigenic fusion vectors. PLoS One 6:e20425. http://dx.doi.org/10.1371/journal.pone.0020425.
23. Parker GF, Daniel RA, Errington J. 1996. Timing and genetic regulation of commitment to sporulation in Bacillus subtilis. Microbiology 142: 3445-3452. http://dx.doi.org/10.1099/13500872-142-12-3445.
24. Gohar M, Faegri K, Perchat S, Ravnum S, Økstad OA, Gominet M, Kolstø AB, LereclusD. 2008. The PlcR virulence regulon of Bacillus cereus. PLoS One 3:e2793. http://dx.doi.org/10.1371/journal.pone.0002793.
25. Bravo A, Agaisse H, Salamitou S, Lereclus D. 1996. Analysis of cryIAa expression in sigE and sigK mutants of Bacillus thuringiensis. Mol Gen Genet 250:734-741.
26. Veening JW, Stewart EJ, Berngruber TW, Taddei F, Kuipers OP, Hamoen LW. 2008. Bet-hedging and epigenetic inheritance in bacterial cell development. Proc Natl Acad Sci U S A 105:4393-4398. http:// dx.doi.org/10.1073/pnas.0700463105.
27. de Jong IG, Beilharz K, Kuipers OP, Veening JW. 2011. Live cell imaging of Bacillus subtilis and Streptococcus pneumoniae using automated timelapse microscopy. J Vis Exp 53:3145. http://dx.doi.org/10.3791/3145.
28. Lereclus D, Agaisse H, Gominet M, Salamitou S, Sanchis V. 1996. Identification of a Bacillus thuringiensis gene that positively regulates transcription of the phosphatidylinositol-specific phospholipase C gene at the onset of the stationary phase. J Bacteriol 178:2749-2756.
29. Rani SA, Pitts B, Beyenal H, Veluchamy RA, Lewandowski Z, Davison WM, Buckingham-Meyer K, Stewart PS. 2007. Spatial patterns of DNA replication, protein synthesis, and oxygen concentration within bacterial biofilms reveal diverse physiological states. J Bacteriol 189:4223-4233. http://dx.doi.org/10.1128/JB.00107-07.
30. López D, Kolter R. 2010. Extracellular signals that define distinct and coexisting cell fates in Bacillus subtilis. FEMS Microbiol. Rev. 34:134-149. http://dx.doi.org/10.1111/j.1574-6976.2009.00199.x.
31. Stoodley P, Sauer K, Davies DG, Costerton JW. 2002. Biofilms as complex differentiated communities. Annu Rev Microbiol 56:187-209. http:// dx.doi.org/10.1146/annurev.micro.56.012302.160705.
32. Horswill AR, Stoodley P, Stewart PS, Parsek MR. 2007. The effect of the chemical, biological, and physical environment on quorum sensing in structured microbial communities. Anal. Bioanal. Chem. 387:371-380. http://dx.doi.org/10.1007/s00216-006-0720-y.
33. Auger S, Krin E, Aymerich S, Gohar M. 2006. Autoinducer 2 affects biofilm formation by Bacillus cereus. Appl Environ Microbiol 72:937-941. http://dx.doi.org/10.1128/AEM.72.1.937-941.2006.
34. 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 19:1151-1157. http://dx.doi.org/10.1111/j.1365-2958.1996.tb02460.x.
35. Chastanet A, Vitkup D, Yuan GC, Norman TM, Liu JS, Losick RM. 2010. Broadly heterogeneous activation of the master regulator for sporulation in Bacillus subtilis. Proc. Natl Acad SciUSA107:8486-8491. http:// dx.doi.org/10.1073/pnas.1002499107.
36. Veening JW, Hamoen LW, Kuipers OP. 2005. Phosphatases modulate the bistable sporulation gene expression pattern in Bacillus subtilis.MolMicrobiol 56:1481-1494. http://dx.doi.org/10.1111/j.1365-2958.2005.04659.x.
37. Perchat S, Zouhir S, Poncet S, Gohar M, Nessler S, Lereclus D. 2013. NprR is a bifunctional quorum sensor that couples necrotrophism and cell development in bacteria of the Bacillus cereus group, abstr 76. Abstr. 7th International Conference on Gram-positive Microorganisms-17th International Conference on Bacilli. Montecatini Terme, Tuscany, Italy.
38. Lereclus D, Arantès O, Chaufaux J, Lecadet M. 1989. Transformation and expression of a cloned delta-endotoxin gene in Bacillus thuringiensis. FEMS Microbiol Lett 51:211-217. http://dx.doi.org/10.1016/0378-1097(89)90511-9.
39. Walhout AJ, Temple GF, Brasch MA, Hartley JL, Lorson MA, van den Heuvel S, Vidal M. 2000. GATEWAY recombinational cloning: application to the cloning of large numbers of open reading frames or ORFeomes. Methods Enzymol 328:575-592. http://dx.doi.org/10.1016/S0076-6879(00)28419-X.
40. Boles BR, Horswill AR. 2008. Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog. 4:e1000052. http://dx.doi.org/10.1371/ journal.ppat.1000052.
41. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, Tsien RY. 2004. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22:1567-1572. http://dx.doi.org/10.1038/nbt1037.
42. Branda SS, Chu F, Kearns DB, Losick R, Kolter R. 2006. A major protein component of the Bacillus subtilis biofilm matrix. Mol Microbiol 59: 1229-1238. http://dx.doi.org/10.1111/j.1365-2958.2005.05020.x.