Bacterial solutions to multicellularity: A tale of biofilms, filaments and fruiting bodies

Nature Reviews Microbiology

Volumn 12, Issue 2, 2014, Pages 115-124

  Claessen, Dennis ^a   Rozen, Daniel E ^a   Kuipers, Oscar P ^b,c   Søgaard Andersen, Lotte ^d   Van Wezel, Gilles P ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c Kluyver Center for Genomics of Industrial Fermentation   (Netherlands)

^d MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANABAENA CYLINDRICA; APOPTOSIS; BACILLUS SUBTILIS; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL MULTICELLULARITY; BIOFILM; CELL DIVISION; CHLAMYDOMONAS REINHARDTII; CYANOBACTERIUM; ESCHERICHIA COLI; EXTRACELLULAR MATRIX; FRUITING BODY; GENE EXPRESSION; MORPHOGENESIS; MULTICELLULAR SPHEROID; MYCOBACTERIUM TUBERCULOSIS; MYXOCOCCALES; MYXOCOCCUS XANTHUS; NONHUMAN; PRIORITY JOURNAL; REVIEW; STREPTOMYCES COELICOLOR; STREPTOMYCETACEAE; VEGETATIVE GROWTH;

BACTERIA (MICROORGANISMS);

APOPTOSIS; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; BIOFILMS; BIOLOGICAL EVOLUTION; CELL DIVISION; CELL TRANSDIFFERENTIATION; CYTOSKELETON; SIGNAL TRANSDUCTION; SPORES, BACTERIAL;

EID: 84892677546     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro3178     Document Type: Review

References (112)

1. Shapiro, J. A. Bacteria as multicellular organisms. Sci. Am. 256, 82-89 (1988).
2. Shapiro, J. A. Thinking about bacterial populations as multicellular organisms. Annu. Rev. Microbiol. 52, 81-104 (1998).
3. Bonner, J. T. The origins of multicellularity. Int. Biol. 1, 27-36 (1998).
4. Rokas, A. The origins of multicellularity and the early history of the genetic toolkit for animal development. Annu. Rev. Genet. 42, 235-251 (2008).
5. Grosberg, R. K. & Strathmann, R. R. The evolution of multicellularity: a minor major transition? Annu. Rev. Ecol. Evol. Systemat. 38, 621-654 (2007).
6. Monds, R. D. & O'Toole, G. A. The developmental model of microbial biofilms: ten years of a paradigm up for review. Trends Microbiol. 17, 73-87 (2009).
7. Flemming, H. C., Neu, T. R. & Wozniak, D. J. The EPS matrix: the "house of biofilm cells". J. Bacteriol. 189, 7945-7947 (2007).
8. Flemming, H. C. & Wingender, J. The biofilm matrix. Nature Rev. Microbiol. 8, 623-633 (2010).
9. Gebbink, M. F., Claessen, D., Bouma, B., Dijkhuizen, L. & Wosten, H. A. Amyloids-a functional coat for microorganisms. Nature Rev. Microbiol. 3, 333-341 (2005).
10. Li, Y. et al. Extracellular polysaccharides mediate pilus retraction during social motility of Myxococcus xanthus. Proc. Natl Acad. Sci. USA 100, 5443-5448 (2003).
11. Kobayashi, K. Bacillus subtilis pellicle formation proceeds through genetically defined morphological changes. J. Bacteriol. 189, 4920-4931 (2007).
12. Perez-Nunez, D. et al. A new morphogenesis pathway in bacteria: unbalanced activity of cell wall synthesis machineries leads to coccus-to-rod transition and filamentation in ovococci. Mol. Microbiol. 79, 759-771 (2011).
13. Flores, E. et al. Septum-localized protein required for filament integrity and diazotrophy in the heterocystforming cyanobacterium Anabaena sp. strain PCC 7120. J. Bacteriol. 189, 3884-3890 (2007).
14. Merino-Puerto, V. et al. FraC/FraD-dependent intercellular molecular exchange in the filaments of a heterocyst-forming cyanobacterium, Anabaena sp. Mol. Microbiol. 82, 87-98 (2011).
15. Nelson, D. E. & Young, K. D. Penicillin binding protein 5 affects cell diameter, contour, and morphology of Escherichia coli. J. Bacteriol. 182, 1714-1721 (2000).
16. Potluri, L. P., de Pedro, M. A. & Young, K. D. Escherichia coli low-molecular-weight penicillinbinding proteins help orient septal FtsZ, and their absence leads to asymmetric cell division and branching. Mol. Microbiol. 84, 203-224 (2012).
17. Ratcliff, W. C., Denison, R. F., Borrello, M. & Travisano, M. Experimental evolution of multicellularity. Proc. Natl Acad. Sci. USA 109, 1595-1600 (2012).
18. Jousset, A. Ecological and evolutive implications of bacterial defences against predators. Environ. Microbiol. 14, 1830-1843 (2012).
19. Boraas, M. E., Seale, D. B. & Boxhorn, J. E. Phagotrophy by a flagellate selects for colonial prey: a possible origin of multicellularity. Evol. Ecol. 12, 153-164 (1998).
20. Corno, G. & Jurgens, K. Direct and indirect effects of protist predation on population size structure of a bacterial strain with high phenotypic plasticity. Appl. Environ. Microbiol. 72, 78-86 (2006).
21. Blom, J. F., Zimmermann, Y. S., Ammann, T. & Pernthaler, J. Scent of danger: floc formation by a freshwater bacterium is induced by supernatants from a predator-prey coculture. Appl. Environ. Microbiol. 76, 6156-6163 (2010).
22. Chauhan, A. et al. Mycobacterium tuberculosis cells growing in macrophages are filamentous and deficient in FtsZ rings. J. Bacteriol. 188, 1856-1865 (2006).
23. Justice, S. S., Hunstad, D. A., Cegelski, L. & Hultgren, S. J. Morphological plasticity as a bacterial survival strategy. Nature Rev. Microbiol. 6, 162-168 (2008).
24. Koschwanez, J. H., Foster, K. R. & Murray, A. W. Sucrose utilization in budding yeast as a model for the origin of undifferentiated multicellularity. PLoS Biol. 8, e1001122 (2011).
25. Koschwanez, J. H., Foster, K. R. & Murray, A. W. Improved use of a public good selects for the evolution of undifferentiated multicellularity. eLife 2, e00367 (2013).
26. Rosenberg, E., Keller, K. H. & Dworkin, M. Cell density-dependent growth of Myxococcus xanthus on casein. J. Bacteriol. 129, 770-777 (1977).
27. Velicer, G. J. & Vos, M. Sociobiology of the myxobacteria. Annu. Rev. Microbiol. 63, 599-623 (2009).
28. Vlamakis, H., Chai, Y., Beauregard, P., Losick, R. & Kolter, R. Sticking together: building a biofilm the Bacillus subtilis way. Nature Rev. Microbiol. 11, 157-168 (2013).
29. Webb, J. S., Givskov, M. & Kjelleberg, S. Bacterial biofilms: prokaryotic adventures in multicellularity. Curr. Opin. Microbiol. 6, 578-585 (2003).
30. Lemon, K. P., Earl, A. M., Vlamakis, H. C., Aguilar, C. & Kolter, R. Biofilm development with an emphasis on Bacillus subtilis. Curr. Top. Microbiol. Immunol. 322, 1-16 (2008).
31. Branda, S. S., Gonzalez-Pastor, J. E., Ben-Yehuda, S., Losick, R. & Kolter, R. Fruiting body formation by Bacillus subtilis. Proc. Natl Acad. Sci. USA 98, 11621-11626 (2001).
32. Gonzalez-Pastor, J. E., Hobbs, E. C. & Losick, R. Cannibalism by sporulating bacteria. Science 301, 510-513 (2003).
33. Veening, J. W., Smits, W. K. & Kuipers, O. P. Bistability, epigenetics, and bet-hedging in bacteria. Annu. Rev. Microbiol. 62, 193-210 (2008).
34. Wilking, J. N. et al. Liquid transport facilitated by channels in Bacillus subtilis biofilms. Proc. Natl Acad. Sci. USA 110, 848-852 (2013).
35. Nadell, C. D., Xavier, J. B. & Foster, K. R. The sociobiology of biofilms. FEMS Microbiol. Rev. 33, 206-224 (2009).
36. West, S. A., Diggle, S. P., Buckling, A., Gardner, A. & Griffins, A. S. The social lives of microbes. Annu. Rev. Ecol. Evol. Systemat. 38, 53-77 (2007).
37. Popat, R. et al. Quorum-sensing and cheating in bacterial biofilms. Proc. Biol. Sci. 279, 4765-4771 (2012).
38. Nadell, C. D., Foster, K. R. & Xavier, J. B. Emergence of spatial structure in cell groups and the evolution of cooperation. PLoS Comput. Biol. 6, e1000716 (2010).
39. Pfeiffer, T. & Bonhoeffer, S. An evolutionary scenario for the transition to undifferentiated multicellularity. Proc. Natl Acad. Sci. USA 100, 1095-1098 (2003).
40. Rossetti, V. & Bagheri, H. C. Advantages of the division of labour for the long-term population dynamics of cyanobacteria at different latitudes. Proc. Biol. Sci. 279, 3457-3466 (2012).
41. Reichenbach, H. The ecology of the myxobacteria. Environ. Microbiol. 1, 15-21 (1999).
42. Berleman, J. E., Chumley, T., Cheung, P. & Kirby, J. R. Rippling is a predatory behavior in Myxococcus xanthus. J. Bacteriol. 188, 5888-5895 (2006).
43. Jelsbak, L. & Søgaard-Andersen, L. Pattern formation by a cell surface-associated morphogen in Myxococcus xanthus. Proc. Natl Acad. Sci. USA 99, 2032-2037 (2002).
44. Whitworth, D. E. (ed.) Myxobacteria: multicellularity and differentiation (ASM, 2008).
45. O'Connor, K. A. & Zusman, D. R. Development in Myxococcus xanthus involves differentiation into two cell types, peripheral rods and spores. J. Bacteriol. 173, 3318-3333 (1991).
46. Nariya, H. & Inouye, M. MazF, an mRNA interferase, mediates programmed cell death during multicellular Myxococcus development. Cell 132, 55-66 (2008).
47. Wireman, J. W. & Dworkin, M. Developmentally induced autolysis during fruiting body formation by Myxococcus xanthus. J. Bacteriol. 129, 798-802 (1977).
48. O'Connor, K. A. & Zusman, D. R. Behaviour of peripheral rods and their role in the life cycle of Myxococcus xanthus. J. Bacteriol. 173, 3342-3355 (1991).
49. Fiegna, F. & Velicer, G. J. Exploitative and hierarchical antagonism in a cooperative bacterium. PLoS Biol. 3, e370 (2005).
50. Velicer, G. J., Kroos, L. & Lenski, R. E. Developmental cheating in the social bacterium Myxococcus xanthus. Nature 404, 598-601 (2000).
51. Kraemer, S. A. & Velicer, G. J. Endemic social diversity within natural kin groups of a cooperative bacterium. Proc. Natl Acad. Sci. USA 108, 10823-10830 (2011).
52. Velicer, G. J., Kroos, L. & Lenski, R. E. Loss of social behaviors by Myxococcus xanthus during evolution in an unstructured habitat. Proc. Natl Acad. Sci. USA 95, 12376-12380 (1998).
53. Vos, M. & Velicer, G. J. Social conflict in centimeter and global-scale populations of the bacterium Myxococcus xanthus. Curr. Biol. 19, 1763-1767 (2009).
54. Pathak, D. T., Wei, X., Dei, A. & Wall, D. Molecular recognition by a polymorphic cell surface receptor governs cooperative behaviors in bacteria. PLoS Genet. 9, e1003891 (2013).
55. Be'er, A. et al. Lethal protein produced in response to competition between sibling bacterial colonies. Proc. Natl Acad. Sci. USA 107, 6258-6263 (2010).
56. Gibbs, K. A. & Greenberg, E. P. Territoriality in Proteus: advertisement and aggression. Chem. Rev. 111, 188-194 (2011).
57. Schirrmeister, B. E., Antonelli, A. & Bagheri, H. C. The origin of multicellularity in cyanobacteria. BMC Evol. Biol. 11, 45 (2011).
58. Tomitani, A., Knoll, A. H., Cavanaugh, C. M. & Ohno, T. The evolutionary diversification of cyanobacteria: molecular-phylogenetic and paleontological perspectives. Proc. Natl Acad. Sci. USA 103, 5442-5447 (2006).
59. Flores, E. & Herrero, A. Compartmentalized function through cell differentiation in filamentous cyanobacteria. Nature Rev. Microbiol. 8, 39-50 (2010).
60. Kumar, K., Mella-Herrera, R. A. & Golden, J. W. Cyanobacterial heterocysts. Cold Spring Harb. Perspect. Biol. 2, a000315 (2010).
61. Yoon, H. S. & Golden, J. W. PatS and products of nitrogen fixation control heterocyst pattern. J. Bacteriol. 183, 2605-2613 (2001).
62. Golden, J. W. & Yoon, H. S. Heterocyst development in Anabaena. Curr. Opin. Microbiol. 6, 557-563 (2003).
63. Mullineaux, C. W. et al. Mechanism of intercellular molecular exchange in heterocyst-forming cyanobacteria. EMBO J. 27, 1299-1308 (2008).
64. Rossetti, V., Schirrmeister, B. E., Bernasconi, M. V. & Bagheri, H. C. The evolutionary path to terminal differentiation and division of labor in cyanobacteria. J. Theor. Biol. 262, 23-34 (2010).
65. Rodrigues, J. F. M., Rankin, D. J., Rossetti, V., Wagner, A. & Bagheri, H. C. Differences in cell division rates drive the evolution of terminal differentiation in microbes. PLoS Comput. Biol. 8, e1002468 (2012).
66. Lee, D. Y. & Rhee, G. Y. Circadian rhythm in growth and death of Anabaena flos-aquae (cyanobacteria). J. Phycol. 35, 694-699 (2002).
67. Ning, S. B., Guo, H. L., Wang, L. & Song, Y. C. Salt stress induces programmed cell death in prokaryotic organism Anabaena. J. Appl. Microbiol. 93, 15-28 (2002).
68. Berman-Frank, I. The demise of the marine cyanobacterium, Trichodesmium spp., via an autocatalyzed cell death pathway. Limnol. Oceanogr. 49, 997-1005 (2004).
69. Flärdh, K., Richards, D. M., Hempel, A. M., Howard, M. & Buttner, M. J. Regulation of apical growth and hyphal branching in Streptomyces. Curr. Opin. Microbiol. 15, 737-743 (2012).
70. Jakimowicz, D. & van Wezel, G. P. Cell division and DNA segregation in Streptomyces: how to build a septum in the middle of nowhere? Mol. Microbiol. 85, 393-404 (2012).
71. Hopwood, D. A. Streptomyces in nature and medicine: the antibiotic makers (Oxford Univ. Press, 2007).
72. van Wezel, G. P. & McDowall, K. J. The regulation of the secondary metabolism of Streptomyces: new links and experimental advances. Nature Prod. Rep. 28, 1311-1333 (2011).
73. Claessen, D., de Jong, W., Dijkhuizen, L. & Wösten, H. A. Regulation of Streptomyces development: reach for the sky!. Trends Microbiol. 14, 313-319 (2006).
74. Manteca, A., Fernandez, M. & Sanchez, J. A death round affecting a young compartmentalized mycelium precedes aerial mycelium dismantling in confluent surface cultures of Streptomyces antibioticus. Microbiology 151, 3689-3697 (2005).
75. Chater, K. F. & Losick, R. in Bacteria as multicellular organisms (eds Shapiro, J. A. & Dworkin, M.) 149-182 (Oxford Univ. Press, 1997).
76. Colson, S. et al. Conserved cis-acting elements upstream of genes composing the chitinolytic system of streptomycetes are DasR-responsive elements. J. Mol. Microbiol. Biotechnol. 12, 60-66 (2007).
77. Nazari, B. et al. Chitin-induced gene expression involved in secondary metabolic pathways in Streptomyces coelicolor A3(2) grown in soil. Appl. Environ. Microbiol. 79, 707-713 (2012).
78. Rigali, S. et al. The sugar phosphotransferase system of Streptomyces coelicolor is regulated by the GntR-family regulator DasR and links N-acetylglucosamine metabolism to the control of development. Mol. Microbiol. 61, 1237-1251 (2006).
79. Rigali, S. et al. Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces. EMBO Rep. 9, 670-675 (2008).
80. Adams, D. W. & Errington, J. Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nature Rev. Microbiol. 7, 642-653 (2009).
81. Lutkenhaus, J. Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu. Rev. Biochem. 76, 539-562 (2007).
82. Schwedock, J., Mccormick, J. R., Angert, E. R., Nodwell, J. R. & Losick, R. Assembly of the cell division protein FtsZ into ladder like structures in the aerial hyphae of Streptomyces coelicolor. Mol. Microbiol. 25, 847-858 (1997).
83. Flärdh, K., Leibovitz, E., Buttner, M. J. & Chater, K. F. Generation of a non-sporulating strain of Streptomyces coelicolor A3(2) by the manipulation of a developmentally controlled ftsZ promoter. Mol. Microbiol. 38, 737-749 (2000).
84. Willemse, J., Mommaas, A. M. & van Wezel, G. P. Constitutive expression of ftsZ overrides the whi developmental genes to initiate sporulation of Streptomyces coelicolor. Antonie Van Leeuwenhoek 101, 619-632 (2012).
85. Willemse, J., Borst, J. W., de Waal, E., Bisseling, T. & van Wezel, G. P. Positive control of cell division: FtsZ is recruited by SsgB during sporulation of Streptomyces. Genes Dev. 25, 89-99 (2011).
86. Xu, Q. et al. Structural and functional characterizations of SsgB, a conserved activator of developmental cell division in morphologically complex actinomycetes. J. Biol. Chem. 284, 25268-25279 (2009).
87. Girard, G. et al. A novel taxonomic marker that discriminates between morphologically complex actinomycetes. Open Biol. http://dx.doi.org/10.1098/ rsob.130073 (2013).
88. Akerlund, T., Nordstrom, K. & Bernander, R. Branched Escherichia coli cells. Mol. Microbiol. 10, 849-858 (1993).
89. Gullbrand, B., Akerlund, T. & Nordstrom, K. On the origin of branches in Escherichia coli. J. Bacteriol. 181, 6607-6614 (1999).
90. Nilsen, T., Ghosh, A. S., Goldberg, M. B. & Young, K. D. Branching sites and morphological abnormalities behave as ectopic poles in shape-defective Escherichia coli. Mol. Microbiol. 52, 1045-1054 (2004).
91. Kawamoto, S., Watanabe, H., Hesketh, A., Ensign, J. C. & Ochi, K. Expression analysis of the ssgA gene product, associated with sporulation and cell division in Streptomyces griseus. Microbiology 143, 1077-1086 (1997).
92. van Wezel, G. P. et al. Unlocking Streptomyces spp. for use as sustainable industrial production platforms by morphological engineering. Appl. Environ. Microbiol. 72, 5283-5288 (2006).
93. Fisher, R. M., Cornwallis, C. K. & West, S. A. Group formation, relatedness, and the evolution of multicellularity. Curr. Biol. 23, 1120-1125 (2013).
94. Ratcliff, W. C. et al. Experimental evolution of an alternating uni-and multicellular life cycle in Chlamydomonas reinhardtii. Nature Commun. 4, 2742 (2013).
95. Giddings, T. H. & Staehelin, L. A. Observation of microplasmodesmata in both heterocyst-forming and non-heterocyst forming filamentous cyanobacteria by freeze-fracture electron microscopy. Arch. Microbiol. 129, 295-298 (1981).
96. Wilk, L. et al. Outer membrane continuity and septosome formation between vegetative cells in the filaments of Anabaena sp. PCC 7120. Cell. Microbiol. 13, 1744-1754 (2011).
97. Merino-Puerto, V., Mariscal, V., Mullineaux, C. W., Herrero, A. & Flores, E. Fra proteins influencing filament integrity, diazotrophy and localization of septal protein SepJ in the heterocyst-forming cyanobacterium Anabaena sp. Mol. Microbiol. 75, 1159-1170 (2010).
98. Kataoka, M., Seki, T. & Yoshida, T. Regulation and function of the Streptomyces plasmid pSN22 genes involved in pock formation and inviability. J. Bacteriol. 173, 7975-7981 (1991).
99. Hopwood, D. A. & Kieser, T. in Bacterial Conjugation (ed. Clewell, D. B.) 293-311 (Plenum, 1993).
100. McCormick, J. R., Su, E. P., Driks, A. & Losick, R. Growth and viability of Streptomyces coelicolor mutant for the cell division gene ftsZ. Mol. Microbiol. 14, 243-254 (1994).
101. Mistry, B. V., Del Sol, R., Wright, C., Findlay, K. & Dyson, P. FtsW is a dispensable cell division protein required for Z-ring stabilization during sporulation septation in Streptomyces coelicolor. J. Bacteriol. 190, 5555-5566 (2008).
102. Schlimpert, S. et al. General protein diffusion barriers create compartments within bacterial cells. Cell 151, 1270-1282 (2012).
103. Sonobe, S. et al. Proliferation of the hyperthermophilic archaeon Pyrobaculum islandicum by cell fission. Extremophiles 14, 403-407 (2010).
104. Letek, M. et al. DivIVA is required for polar growth in the MreB-lacking rod-shaped actinomycete Corynebacterium glutamicum. J. Bacteriol. 190, 3283-3292 (2008).
105. Kang, C. M., Nyayapathy, S., Lee, J. Y., Suh, J. W. & Husson, R. N. Wag31, a homologue of the cell division protein DivIVA, regulates growth, morphology and polar cell wall synthesis in mycobacteria. Microbiology 154, 725-735 (2008).
106. Nguyen, L. et al. Antigen 84, an effector of pleiomorphism in Mycobacterium smegmatis. J. Bacteriol. 189, 7896-7910 (2007).
107. Flärdh, K. Essential role of DivIVA in polar growth and morphogenesis in Streptomyces coelicolor A3(2). Mol. Microbiol. 49, 1523-1536 (2003).
108. Edwards, D. H. & Errington, J. The Bacillus subtilis DivIVA protein targets to the division septum and controls the site specificity of cell division. Mol. Microbiol. 24, 905-915 (1997).
109. Marston, A. L., Thomaides, H. B., Edwards, D. H., Sharpe, M. E. & Errington, J. Polar localization of the MinD protein of Bacillus subtilis and its role in selection of the mid-cell division site. Genes Dev. 12, 3419-3430 (1998).
110. Scherr, N. & Nguyen, L. Mycobacterium versus Streptomyces-we are different, we are the same. Curr. Opin. Microbiol. 12, 699-707 (2009).
111. Ghosh, J. et al. Sporulation in mycobacteria. Proc. Natl Acad. Sci. USA 106, 10781-10786 (2009).
112. Traag, B. A. et al. Do mycobacteria produce endospores? Proc. Natl Acad. Sci. USA 107, 878-881 (2010).