Skip to main content
SpringerLink
Log in

Multicellularity in Bacteria: From Division of Labor to Biofilm Formation

  • Chapter
  • First Online:
Evolutionary Transitions to Multicellular Life

Part of the book series: Advances in Marine Genomics ((AMGE,volume 2))

Abstract

Introduced nearly two decades ago, the concept of multicellularity in bacteria is currently accepted as a general trait of bacterial physiology. The view of bacteria being more than just unicellular, non-organized, selfish organisms is to a large degree based on the findings that division of labor and cell-to-cell communication within bacterial communities are ubiquitous across bacterial species. Bacteria are able to form complex communities in which cells can specialize in a spatiotemporal fashion, using extracellular signals to coordinate the expression of specific genes required for structural development. Despite the enormous progress made by researchers in the field over the past years, knowledge of the molecular mechanisms that govern bacterial multicellularity and biofilm development is scarce and remains a highly interesting field for future research.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aguilar C, Vlamakis H, Losick R, Kolter R (2007) Thinking about Bacillus subtilis as a multicellular organism. Curr Opin Microbiol 10:638–643. doi:10.1016/j.mib.2007.09.006

    Article  CAS  Google Scholar 

  • Aguilar C, Carlier A, Riedel K, Eberl L (2009) Cell-to-cell communication in biofilms of Gram-negative bacteria. In: Krämer R, Jung K (eds) Bacterial Signaling. Wiley-VCH, Weinheim, pp 23–40

    Chapter  Google Scholar 

  • Aguilar C, Vlamakis H, Guzman A et al (2010) KinD is a checkpoint protein linking spore formation to extracellular-matrix production in Bacillus subtilis biofilms. MBio 1:1–7. doi:10.1128/mBio.00035-10

    Article  Google Scholar 

  • An D, Parsek MR (2007) The promise and peril of transcriptional profiling in biofilm communities. Curr Opin Microbiol 10:292–296. doi:10.1016/j.mib.2007.05.011

    Article  CAS  Google Scholar 

  • Asally M, Kittisopikul M, Rué P et al (2012) Localized cell death focuses mechanical forces during 3D patterning in a biofilm. Proc Natl Acad Sci U S A 109:18891–18896. doi:10.1073/pnas.1212429109

    Article  CAS  Google Scholar 

  • Atkinson S, Throup JP, Stewart GS, Williams P (1999) A hierarchical quorum-sensing system in Yersinia pseudotuberculosis is involved in the regulation of motility and clumping. Mol Microbiol 33:1267–1277. doi:10510240

    Article  CAS  Google Scholar 

  • Barken KB, Pamp SJ, Yang L et al (2008) Roles of type IV pili, flagellum-mediated motility and extracellular DNA in the formation of mature multicellular structures in Pseudomonas aeruginosa biofilms. Environ Microbiol 10:2331–2343. doi:10.1111/j.1462-2920.2008.01658.x

    Article  CAS  Google Scholar 

  • Bergman B, Gallon JR, Rai AN, Stal LJ (1997) N2 Fixation by non-heterocystous cyanobacteria. FEMS Microbiol Rev 19:139–185

    Article  CAS  Google Scholar 

  • Branda SS, González-Pastor JE, Ben-Yehuda S et al (2001) Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci U S A 98:11621–11626. doi:10.1073/pnas.191384198

    Article  CAS  Google Scholar 

  • Branda SS, Vik S, Friedman L, Kolter R (2005) Biofilms: the matrix revisited. Trends Microbiol 13:20–26. doi:S0966-842X(04)00260-4

    Article  CAS  Google Scholar 

  • Branda SS, Chu F, Kearns DB et al (2006) A major protein component of the Bacillus subtilis biofilm matrix. Mol Microbiol 59:1229–1238. doi:10.1111/j.1365-2958.2005.05020.x

    Article  CAS  Google Scholar 

  • Bryers JD (2008) Medical biofilms. Biotechnol Bioeng 100:1–18. doi:10.1002/bit.21838

    Article  CAS  Google Scholar 

  • Christensen BB, Sternberg C, Andersen JB et al (1999) Molecular tools for study of biofilm physiology. Methods Enzym 310:20–42

    Article  CAS  Google Scholar 

  • Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322 (80-)

    Article  CAS  Google Scholar 

  • Danhorn T, Fuqua C (2007) Biofilm formation by plant-associated bacteria. Annu Rev Microbiol 61:401–422. doi:10.1146/annurev.micro.61.080706.093316

    Article  CAS  Google Scholar 

  • Darouiche RO (2004) Treatment of infections associated with surgical implants. N Engl J Med 350:1422–1429. doi:10.1056/NEJMra035415

    Article  CAS  Google Scholar 

  • Dow JM, Crossman L, Findlay K et al (2003) Biofilm dispersal in Xanthomonas campestris is controlled by cell-cell signaling and is required for full virulence to plants. Proc Natl Acad Sci U S A 100:10995–11000. doi:12960398

    Article  CAS  Google Scholar 

  • Flores E, Herrero A (2010) Compartmentalized function through cell differentiation in filamentous cyanobacteria. Nat Rev Microbiol 8:39–50. doi:10.1038/nrmicro2242

    Article  CAS  Google Scholar 

  • Fremgen SA, Burke NS, Hartzell PL (2010) Effects of site-directed mutagenesis of mglA on motility and swarming of Myxococcus xanthus. BMC Microbiol 10:295. doi:10.1186/1471-2180-10-295

    Article  Google Scholar 

  • Fujita M, Gonza E, Losick R (2005) High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis. J Bacteriol 187:1357–1368. doi:10.1128/JB.187.4.1357

    Article  CAS  Google Scholar 

  • Funken H, Bartels K, Wilhelm S et al (2012) Specific association of lectin LecB with the surface of Pseudomonas aeruginosa: role of outer membrane protein OprF. PLoS One 7:e46857. doi:10.1371/journal.pone.0046857

    Article  CAS  Google Scholar 

  • Grosberg RK, Strathmann RR (2007) The evolution of multicellularity: a minor major transition? Annu Rev Ecol Evol Syst 38:621–654. doi:10.1146/annurev.ecolsys.36.102403.114735

    Article  Google Scholar 

  • Hu W, Li L, Sharma S et al (2012) DNA builds and strengthens the extracellular matrix in Myxococcus xanthus biofilms by interacting with exopolysaccharides. PLoS One 7:e51905. doi:10.1371/journal.pone.0051905

    Article  CAS  Google Scholar 

  • Inhülsen S, Aguilar C, Schmid N et al (2012) Identification of functions linking quorum sensing with biofilm formation in Burkholderia cenocepacia H111. Microbiologyopen 1:225–242. doi:10.1002/mbo3.24

    Article  Google Scholar 

  • Izano EA, Amarante MA, Kher WB, Kaplan JB (2008) Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. Appl Environ Microbiol 74:470–476. doi:10.1128/AEM.02073-07

    Article  CAS  Google Scholar 

  • Jurcisek JA, Bakaletz LO (2007) Biofilms formed by nontypeable Haemophilus influenzae in vivo contain both double-stranded DNA and type IV pilin protein. J Bacteriol 189:3868–3875. doi:10.1128/JB.01935-06

    Article  CAS  Google Scholar 

  • Kaiser D (2003) Coupling cell movement to multicellular development in myxobacteria. Nat Rev Microbiol 1:45–54. doi:10.1038/nrmicro733

    Article  CAS  Google Scholar 

  • Klausen M, Aaes-Jørgensen A, Molin S, Tolker-Nielsen T (2003) Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol Microbiol 50:61–68. doi:10.1046/j.1365-2958.2003.03677.x

    Article  CAS  Google Scholar 

  • Kolodkin-Gal I, Verdiger R, Shlosberg-Fedida A, Engelberg-Kulka H (2009) A differential effect of E. coli toxin-antitoxin systems on cell death in liquid media and biofilm formation. PLoS One 4:e6785. doi:10.1371/journal.pone.0006785

    Article  Google Scholar 

  • Koutsoudis M, Tsaltas D, Minogue T, von Bodman SB (2006) Quorum-sensing regulation governs bacterial adhesion, biofilm development, and host colonization in Pantoea stewartii subspecies stewartii. Proc Natl Acad Sci U S A 103:5983–5988. doi:10.1073/pnas.0509860103

    Article  CAS  Google Scholar 

  • Kovács AT, van Gestel J, Kuipers OP (2012) The protective layer of biofilm: a repellent function for a new class of amphiphilic proteins. Mol Microbiol 85:8–11. doi:10.1111/j.1365-2958.2012.08101.x

    Article  Google Scholar 

  • Lasa I, Penadés J (2006) Bap: a family of surface proteins involved in biofilm formation. Res Microbiol 157:99–107. doi:10.1016/j.resmic.2005.11.003

    Article  CAS  Google Scholar 

  • Latasa C, Solano C, Penadés J, Lasa I (2006) Biofilm-associated proteins. C R Biol 329:849–857. doi:10.1016/j.crvi.2006.07.008

    Article  CAS  Google Scholar 

  • Lenz AP, Williamson KS, Pitts B et al (2008) Localized gene expression in Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 74:4463–4471. doi:10.1128/AEM.00710-08

    Article  CAS  Google Scholar 

  • Lewis K (2010) Persister cells. Annu Rev Microbiol 64:357–372. doi:10.1146/annurev.micro.112408.134306

    Article  CAS  Google Scholar 

  • López D, Kolter R (2010) Extracellular signals that define distinct and coexisting cell fates in Bacillus subtilis. FEMS Microbiol Rev 34:134–149. doi:10.1111/j.1574-6976.2009.00199.x

    Article  Google Scholar 

  • López D, Vlamakis H, Kolter R (2010) Biofilms. Cold Spring Harb Perspect Biol 2:a000398. doi:10.1101/cshperspect.a000398

    Article  Google Scholar 

  • Lynch A, Robertson G (2008) Bacterial and fungal biofilm infections. Annu Rev Med 59:415–428. doi:10.1146/annurev.med.59.110106.132000

    Article  CAS  Google Scholar 

  • McLoon AL, Guttenplan SB, Kearns DB et al (2011) Tracing the domestication of a biofilm-forming bacterium. J Bacteriol 193:2027–2034. doi:10.1128/JB.01542-10

    Article  CAS  Google Scholar 

  • Meeks JC, Elhai J (2002) Regulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states. Microbiol Mol Bio Rev 66:94–121. doi:10.1128/MMBR.66.1.94

    Article  CAS  Google Scholar 

  • Mendes-Soares H, Velicer GJ (2013) Decomposing predation: testing for parameters that correlate with predatory performance by a social bacterium. Microb Ecol 65:415–423. doi: 10.1007/s00248-012-0135-6

    Article  Google Scholar 

  • Morikawa M, Kagihiro S, Haruki M et al (2006) Biofilm formation by a Bacillus subtilis strain that produces γ-polyglutamate. Microbiology 152:2801–2807. doi:10.1099/mic.0.29060-0

    Article  CAS  Google Scholar 

  • Neu TR, Lawrence JR (2009) Extracellular polymeric substances in microbial biofilms. In: Moran AP, Holst O, Brennan PJ, von Itzstein M (eds) Microbial glycobiology. Elsevier, London, pp 735–758

    Google Scholar 

  • Ng W, Bassler B (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222. doi:10.1146/annurev-genet-102108-134304

    Article  CAS  Google Scholar 

  • O’Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54:49–79

    Article  Google Scholar 

  • Ostrowski A, Mehert A, Prescott A et al (2011) YuaB functions synergistically with the exopolysaccharide and TasA amyloid fibers to allow biofilm formation by Bacillus subtilis. J Bacteriol 193:4821–4831. doi:10.1128/JB.00223-11

    Article  CAS  Google Scholar 

  • Puskas A, Greenberg EP, Kaplan S, Schaefer AL (1997) A quorum-sensing system in the free-living photosynthetic bacterium Rhodobacter sphaeroides. J Bacteriol 179:7530–7537. doi:9393720

    CAS  Google Scholar 

  • Rani SA, Pitts B, Beyenal H et al (2007) Spatial patterns of DNA replication, protein synthesis, and oxygen concentration within bacterial biofilms reveal diverse physiological states. J Bacteriol 189:4223–4233. doi:10.1128/JB.00107-07

    Article  CAS  Google Scholar 

  • Reva O, Tümmler B (2008) Think big-giant genes in bacteria. Environ Microbiol 10:768–777. doi:10.1111/j.1462-2920.2007.01500.x

    Google Scholar 

  • Rodrigues LR (2011) Inhibition of Bacterial Adhesion on Medical Devices. Adv Exp Med Biol 715:351–367. doi:10.1007/978-94-007-0940-9

    Article  CAS  Google Scholar 

  • Romero D, Aguilar C, Losick R, Kolter R (2010) Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc Natl Acad Sci U S A 107:2230–2234. doi:10.1073/pnas.0910560107

    Article  CAS  Google Scholar 

  • Romero D, Vlamakis H, Losick R, Kolter R (2011) An accessory protein required for anchoring and assembly of amyloid fibres in B. subtilis biofilms. Mol Microbiol 80:1155–1168. doi:10.1111/j.1365-2958.2011.07653.x

    Article  CAS  Google Scholar 

  • Sadykov MR, Bayles KW (2012) The control of death and lysis in staphylococcal biofilms: a coordination of physiological signals. Curr Opin Microbiol 15:211–215. doi:10.1016/j.mib.2011.12.010

    Article  CAS  Google Scholar 

  • Sakuragi Y, Kolter R (2007) Quorum-sensing regulation of the biofilm matrix genes (pel) of Pseudomonas aeruginosa. J Bacteriol 189:5383–5386. doi:10.1128/JB.00137-07

    Article  CAS  Google Scholar 

  • Schirrmeister BE, de Vos JM, Antonelli A, Bagheri HC (2013) Evolution of multicellularity coincided with increased diversification of cyanobacteria and the Great Oxidation Event. Proc Natl Acad Sci U S A. doi:10.1073/pnas.1209927110

    Google Scholar 

  • Schopf JW (2006) Fossil evidence of Archaean life. Philos Trans R Soc Lond B Biol Sci 361:869–885. doi:10.1098/rstb.2006.1834

    Article  CAS  Google Scholar 

  • Seminara A, Angelini TE, Wilking JN et al (2012) Osmotic spreading of Bacillus subtilis biofilms driven by an extracellular matrix. Proc Natl Acad Sci U S A 109:1116–1121. doi:10.1073/pnas.1109261108

    Article  CAS  Google Scholar 

  • Shank EA, Kolter R (2011) Extracellular signaling and multicellularity in Bacillus subtilis. Curr Opin Microbiol 14:741–747. doi:10.1016/j.mib.2011.09.016

    Article  CAS  Google Scholar 

  • Shapiro JA (1988) Bacteria as multicellular organisms. Sci Am 258:82–89

    Article  Google Scholar 

  • Shapiro JA (1998) Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol 52:81–104. doi:10.1146/annurev.micro.52.1.81

    Article  CAS  Google Scholar 

  • Shapiro JA, Dworkin M (1997) Bacteria as multicellular organisms. Oxford University Press, New York

    Google Scholar 

  • Stanley NR, Lazazzera BA (2005) Defining the genetic differences between wild and domestic strains of Bacillus subtilis that affect poly-γ-dl-glutamic acid production and biofilm formation. Mol Microbiol 57:1143–1158. doi:10.1111/j.1365-2958.2005.04746.x

    Article  CAS  Google Scholar 

  • Steinberger RE, Holden PA (2005) Extracellular DNA in single- and multiple-species unsaturated biofilms. Appl Environ Microbiol 71:5404–5410. doi:10.1128/AEM.71.9.5404

    Article  CAS  Google Scholar 

  • Stewart PS, Franklin MJ (2008) Physiological heterogeneity in biofilms. Nat Rev Microbiol 6:199–210. doi:10.1038/nrmicro1838

    Article  CAS  Google Scholar 

  • Tamulonis C, Postma M, Kaandorp J (2011) Modeling filamentous cyanobacteria reveals the advantages of long and fast trichomes for optimizing light exposure. PLoS One 6:e22084. doi:10.1371/journal.pone.0022084

    Article  CAS  Google Scholar 

  • Torres P, Malamud F, Rigano L et al (2007) Controlled synthesis of the DSF cell-cell signal is required for biofilm formation and virulence in Xanthomonas campestris. Environ Microbiol 9:2101–2109. doi:EMI1332

    Article  Google Scholar 

  • Van Acker H, Sass A, Bazzini S et al (2013) Biofilm-grown Burkholderia cepacia complex cells survive antibiotic treatment by avoiding production of reactive oxygen species. PLoS One 8:e58943. doi:10.1371/journal.pone.0058943

    Article  CAS  Google Scholar 

  • Veening J, Kuipers OP, Brul S et al (2006) Effects of phosphorelay perturbations on architecture, sporulation, and spore resistance in biofilms of Bacillus subtilis. J Bacteriol 188:3099–3109. doi:10.1128/JB.188.8.3099

    Article  CAS  Google Scholar 

  • Velicer GJ, Vos M (2009) Sociobiology of the myxobacteria. Annu Rev Microbiol 63:599–623. doi:10.1146/annurev.micro.091208.073158

    Article  CAS  Google Scholar 

  • Velicer GJ, Kroos L, Lenski RE (1998) Loss of social behaviors by Myxococcus xanthus during evolution in an unstructured habitat. Proc Natl Acad Sci U S A 95:12376–12380

    Article  CAS  Google Scholar 

  • Vilain S, Pretorius JM, Theron J, Brözel VS (2009) DNA as an adhesin: Bacillus cereus requires extracellular DNA to form biofilms. Appl Environ Microbiol 75:2861–2868. doi:10.1128/AEM.01317-08

    Article  CAS  Google Scholar 

  • 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. doi:10.1101/gad.1645008

    Article  CAS  Google Scholar 

  • Vlamakis H, Chai Y, Beauregard P et al (2013) Sticking together: building a biofilm the Bacillus subtilis way. Nat Rev Microbiol 11:157–168. doi:10.1038/nrmicro2960

    Article  CAS  Google Scholar 

  • Von Bodman SB Majerczak DR Coplin DL (1998) A negative regulator mediates quorum-sensing control of exopolysaccharide production in Pantoea stewartii subsp. stewartii. Proc Natl Acad Sci U S A 95:7687–7692

    Article  CAS  Google Scholar 

  • Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS (2002) Extracellular DNA required for bacterial biofilm formation. Science 295:1487. doi:11859186 (80-)

    Article  CAS  Google Scholar 

  • Yousef F, Espinosa-Urgel M (2007) In silico analysis of large microbial surface proteins. Res Microbiol 158:545–550. doi:10.1016/j.resmic.2007.04.006

    Google Scholar 

  • Zafra O, Lamprecht-Grandío M, González de Figueras C, González-Pastor JE (2012) Extracellular DNA release by undomesticated Bacillus subtilis is regulated by early competence. PLoS One 7:e48716. doi:10.1371/journal.pone.0048716

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Hera Vlamakis for critical reading of the manuscript. Financial support from the Swiss National Fund (Project 31003A_122013 to LE) and EU (grant 265862/Paravac to CE) is gratefully acknowledged.

Author information

Authors and Affiliations

  1. Department of Microbiology, Institute of Plant Biology, University of Zurich, Zollikerstrasse 107, 8008, Zurich, Switzerland

    Claudio Aguilar & Leo Eberl

  2. Institute of Virology, University of Zurich, Winterthurerstrasse 266a, 8057, Zurich, Switzerland

    Catherine Eichwald

Authors
  1. Claudio Aguilar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Catherine Eichwald
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Leo Eberl
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Claudio Aguilar .

Editor information

Editors and Affiliations

  1. Institut de Biologia Evolutiva (UPF-CSIC), Barcelona, Spain

    Iñaki Ruiz-Trillo

  2. Department of Biology, University of New Brunswick, Fredericton, New Brunswick, Canada

    Aurora M. Nedelcu

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Aguilar, C., Eichwald, C., Eberl, L. (2015). Multicellularity in Bacteria: From Division of Labor to Biofilm Formation. In: Ruiz-Trillo, I., Nedelcu, A. (eds) Evolutionary Transitions to Multicellular Life. Advances in Marine Genomics, vol 2. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9642-2_4

Download citation

Publish with us

Policies and ethics

Search

Navigation