Thinking about Bacterial Populations as Multicellular Organisms
Open accessAbstract
It has been a decade since multicellularity was proposed as a general bacterial trait. Intercellular communication and multicellular coordination are now known to be widespread among prokaryotes and to affect multiple phenotypes. Many different classes of signaling molecules have been identified in both Gram-positive and Gram-negative species. Bacteria have sophisticated signal transduction networks for integrating intercellular signals with other information to make decisions about gene expression and cellular differentiation. Coordinated multicellular behavior can be observed in a variety of situations, including development of E. coli and B. subtilis colonies, swarming by Proteus and Serratia, and spatially organized interspecific metabolic cooperation in anaerobic bioreactor granules. Bacteria benefit from multicellular cooperation by using cellular division of labor, accessing resources that cannot effectively be utilized by single cells, collectively defending against antagonists, and optimizing population survival by differentiating into distinct cell types.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In prokaryotes, intercellular communication and multicellular coordination are widespread and influence the expression and intensity of multiple phenotypes.
“In procaryotes, intercellular communication and multicellular coordination are widespread and influence the expression and intensity of multiple phenotypes [6,8,9,10,11,12].”
From Microbiota of Cheese Ecosystems: A Perspective on Cheesemaking (2025) · cites this paper as [11]
Cites
Alberts, B., Johnson, A., Lewis, J. H., Morgan, D. O., RAFF, M. C., Roberts, K. J., & Walter, P. (2017) · W.W. Norton eBooks · doi:10.1201/9781315735368 · Cited by 7,937 · see citing works
Brock Biology of Microorganisms
Madigan, M. T., Bender, K. S., Buckley, D. H., Sattley, W. M., & Stahl, D. A. (1996) · Cited by 5,759 · see citing works
Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R., & Lappin-Scott, H. M. (1995) · Annual Review of Microbiology · doi:10.1146/annurev.mi.49.100195.003431 · Cited by 4,718 · see citing works
The Involvement of Cell-to-Cell Signals in the Development of a Bacterial Biofilm
Davies, D. G., Parsek, M. R., Pearson, J. P., Iglewski, B. H., Costerton, J. W., & Greenberg, E. P. (1998) · Science · doi:10.1126/science.280.5361.295 · Cited by 3,396 · see citing works
Fuqua, W. C., Winans, S. C., & Greenberg, E. P. (1994) · Journal of Bacteriology · doi:10.1128/jb.176.2.269-275.1994 · Cited by 2,941 · see citing works
Energetics of syntrophic cooperation in methanogenic degradation
Schink, B. (1997) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.61.2.262-280.1997 · Cited by 1,798 · see citing works
Common themes in microbial pathogenicity revisited
Finlay, B. B., & Falkow, S. (1997) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.61.2.136-169.1997 · Cited by 1,474 · see citing works
Fuqua, C., Winans, S. C., & Greenberg, E. P. (1996) · Annual Review of Microbiology · doi:10.1146/annurev.micro.50.1.727 · Cited by 1,217 · see citing works
Kellogg, D. S., Peacock, W. L., Deacon, W. E., Brown, L., & Pirkle, C. I. (1963) · Journal of Bacteriology · doi:10.1128/jb.85.6.1274-1279.1963 · Cited by 1,202 · see citing works
Signaling in Plant-Microbe Interactions
Baker, B., Zambryski, P., Staskawicz, B. J., & Dinesh-Kumar, S. P. (1997) · Science · doi:10.1126/science.276.5313.726 · Cited by 880 · see citing works
High Mutation Frequencies Among Escherichia coli and Salmonella Pathogens
LeClerc, J. E., Li, B., Payne, W. L., & Cebula, T. A. (1996) · Science · doi:10.1126/science.274.5290.1208 · Cited by 818 · see citing works
THE STATIONARY PHASE OF THE BACTERIAL LIFE CYCLE
Kolter, R., Siegele, D. A., & Tormo, A. (1993) · Annual Review of Microbiology · doi:10.1146/annurev.mi.47.100193.004231 · Cited by 810 · see citing works
Kleerebezem, M., Quadri, L. E. N., Kuipers, O. P., & de Vos, W. M. (1997) · Molecular Microbiology · doi:10.1046/j.1365-2958.1997.4251782.x · Cited by 791 · see citing works
Common themes in microbial pathogenicity
Finlay, B. B., & Falkow, S. (1989) · Microbiological Reviews · doi:10.1128/mr.53.2.210-230.1989 · Cited by 767 · see citing works
Signaling in Plant-Microbe Interactions
Pandey, A., & Chatterjee, S. (2013) · Cited by 766 · see citing works
Håvarstein, L. S., Coomaraswamy, G., & Morrison, D. A. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.24.11140 · Cited by 737 · see citing works
INFECTIVE HEREDITY OF MULTIPLE DRUG RESISTANCE IN BACTERIA
Watanabe, T. (1963) · Bacteriological Reviews · doi:10.1128/br.27.1.87-115.1963 · Cited by 737 · see citing works
Latifi, A., Foglino, M., Tanaka, K., et al. (1996) · Molecular Microbiology · doi:10.1046/j.1365-2958.1996.00063.x · Cited by 727 · see citing works
Methanobacillus omelianskii, a symbiotic association of two species of bacteria
Bryant, M. P., Wolin, E. A., Wolin, M. J., & WOLFE, R. S. (1967) · Archives of Microbiology · doi:10.1007/bf00406313 · Cited by 671 · see citing works
Cell density control of staphylococcal virulence mediated by an octapeptide pheromone.
Ji, G., Beavis, R. C., & Novick, R. P. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.26.12055 · Cited by 668 · see citing works
Aizenman, E., Engelberg–Kulka, H., & Glaser, G. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.12.6059 · Cited by 605 · see citing works
Bacterial surface translocation: a survey and a classification
Henrichsen, J. (1972) · Bacteriological Reviews · doi:10.1128/br.36.4.478-503.1972 · Cited by 603 · see citing works
Generic modelling of cooperative growth patterns in bacterial colonies
Ben‐Jacob, E., Schochet, O., Tenenbaum, A., et al. (1994) · Nature · doi:10.1038/368046a0 · Cited by 602 · see citing works
Complex patterns formed by motile cells of Escherichia coli
Budrene, E. O., & Berg, H. C. (1991) · Nature · doi:10.1038/349630a0 · Cited by 593 · see citing works
Diffusion of autoinducer is involved in regulation of the Vibrio fischeri luminescence system
Kaplan, H. B., & Greenberg, E. P. (1985) · Journal of Bacteriology · doi:10.1128/jb.163.3.1210-1214.1985 · Cited by 572 · see citing works
Social gliding is correlated with the presence of pili in Myxococcus xanthus.
Kaiser, D. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.11.5952 · Cited by 570 · see citing works
DNA: Insertion Elements, Plasmids, and Episomes.
Bukhari, A. I., Shapiro, J. A., & Adhya, S. L. (1977) · Medical Entomology and Zoology · Cited by 558 · see citing works
Self-citationDynamics of formation of symmetrical patterns by chemotactic bacteria
Budrene, E. O., & Berg, H. C. (1995) · Nature · doi:10.1038/376049a0 · Cited by 547 · see citing works
Winson, M. K., Cámara, M., Latifi, A., et al. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.20.9427 · Cited by 539 · see citing works
Bacteria as Multicellular Organisms
Shapiro, J. A. (1988) · Scientific American · doi:10.1038/scientificamerican0688-82 · Cited by 524 · cited 2× · see citing works
“A more detailed discussion of particular aspects can be found in the recent book dedicated to this theme (148).”
BackgroundSelf-citationAdaptive reversion of a frameshift mutation in Escherichia coli.
Cairns, J., & Foster, P. L. (1991) · Genetics · doi:10.1093/genetics/128.4.695 · Cited by 491 · see citing works
Jones, S., Yu, B., Bainton, N. J., et al. (1993) · The EMBO Journal · doi:10.1002/j.1460-2075.1993.tb05902.x · Cited by 466 · see citing works
Biochemical and genetic characterization of a competence pheromone from B. subtilis
Magnuson, R. D., Solomon, J. M., & Grossman, A. D. (1994) · Cell · doi:10.1016/0092-8674(94)90313-1 · Cited by 465 · see citing works
Pirhonen, M., Flego, D., Heikinheimo, R., & Palva, E. T. (1993) · The EMBO Journal · doi:10.1002/j.1460-2075.1993.tb05901.x · Cited by 457 · see citing works
Pestova, E. V., Håvarstein, L. S., & Morrison, D. A. (1996) · Molecular Microbiology · doi:10.1046/j.1365-2958.1996.501417.x · Cited by 442 · see citing works
Grossman, A. D. (1995) · Annual Review of Genetics · doi:10.1146/annurev.ge.29.120195.002401 · Cited by 425 · see citing works
The bacterial ’enigma’: cracking the code of cell-cell communication
Salmond, G. P. C., Bycroft, B. W., Stewart, G. S. A. B., & Williams, P. (1995) · Molecular Microbiology · doi:10.1111/j.1365-2958.1995.tb02424.x · Cited by 387 · see citing works
EXOPOLYSACCHARIDES IN PLANT-BACTERIAL INTERACTIONS
Leigh, J. A., & Coplin, D. L. (1992) · Annual Review of Microbiology · doi:10.1146/annurev.mi.46.100192.001515 · Cited by 369 · see citing works
Goodman, S. D., & Scocca, J. J. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.18.6982 · Cited by 361 · see citing works
A scanning and transmission electron microscopic study of an infected endocardial pacemaker lead.
Marrie, T. J., Nelligan, J., & Costerton, J. W. (1982) · Circulation · doi:10.1161/01.cir.66.6.1339 · Cited by 347 · see citing works
Eberl, L., Winson, M. K., Sternberg, C., Stewart, G. S. A. B., Christiansen, G., Chhabra, S. R., Bycroft, B. W., Williams, P. M., Molin, S., & Givskov, M. (1996) · Molecular Microbiology · doi:10.1111/j.1365-2958.1996.tb02495.x · Cited by 347 · see citing works
Seed, P. C., Passador, L., & Iglewski, B. H. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.3.654-659.1995 · Cited by 344 · see citing works
Field, J. A., Stams, A. J. M., Kato, M. T., & Schraa, G. (1995) · Antonie van Leeuwenhoek · doi:10.1007/bf00872195 · Cited by 341 · see citing works
Programmed Cell Death in Bacterial Populations
Yarmolinsky, M. B. (1995) · Science · doi:10.1126/science.7846528 · Cited by 339 · see citing works
Spontaneous point mutations that occur more often when advantageous than when neutral.
Hall, B. G. (1990) · Genetics · doi:10.1093/genetics/126.1.5 · Cited by 326 · see citing works
SIGNALING AND HOST RANGE VARIATION IN NODULATION
Dénarié, J., Debellé, F., & Rosenberg, C. (1992) · Annual Review of Microbiology · doi:10.1146/annurev.mi.46.100192.002433 · Cited by 292 · see citing works
A Kinetic Study of the Mode of Growth of Surface Colonies of Bacteria and Fungi
PIRT, S. J. (1967) · Journal of General Microbiology · doi:10.1099/00221287-47-2-181 · Cited by 292 · see citing works
Wu, S., & Kaiser, D. (1995) · Molecular Microbiology · doi:10.1111/j.1365-2958.1995.mmi_18030547.x · Cited by 283 · see citing works
Torkelson, J. D., Harris, R. S., Lombardo, M., Nagendran, J., Thulin, C., & Rosenberg, S. M. (1997) · EMBO Journal · doi:10.1093/emboj/16.11.3303 · Cited by 273 · see citing works
Solomon, J. M., Lazazzera, B. A., & Grossman, A. D. (1996) · Genes & Development · doi:10.1101/gad.10.16.2014 · Cited by 268 · see citing works
ADAPTIVE MUTATION: The Uses of Adversity
Foster, P. L. (1993) · Annual Review of Microbiology · doi:10.1146/annurev.mi.47.100193.002343 · Cited by 262 · see citing works
Fractal Growth of Bacillus subtilis on Agar Plates
Fujikawa, H., & Matsushita, M. (1989) · Journal of the Physical Society of Japan · doi:10.1143/jpsj.58.3875 · Cited by 256 · see citing works
A role for bacteriophages in the evolution and transfer of bacterial virulence determinants
Cheetham, B. F., & Katz, M. E. (1995) · Molecular Microbiology · doi:10.1111/j.1365-2958.1995.mmi_18020201.x · Cited by 255 · see citing works
REGULATION OF THE TRANSFORMABILITY OF PNEUMOCOCCAL CULTURES BY MACROMOLECULAR CELL PRODUCTS
Tomasz, A., & Hotchkiss, R. D. (1964) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.51.3.480 · Cited by 254 · see citing works
Bacteria as multicellular organisms
(1997) · Choice Reviews Online · doi:10.5860/choice.35-0884 · Cited by 247 · see citing works
Spatio-temporal patterns generated by Salmonella typhimurium
Woodward, D. E., Tyson, R. C., Myerscough, M. R., et al. (1995) · Biophysical Journal · doi:10.1016/s0006-3495(95)80400-5 · Cited by 242 · see citing works
How and why bacteria talk to each other
Kaiser, D., & Losick, R. M. (1993) · Cell · doi:10.1016/0092-8674(93)90268-u · Cited by 238 · see citing works
Tomasz, A. (1965) · Nature · doi:10.1038/208155a0 · Cited by 235 · see citing works
Periodic phenomena in Proteus mirabilis swarm colony development
Rauprich, O., Matsushita, M., Weijer, C. J., et al. (1996) · Journal of Bacteriology · doi:10.1128/jb.178.22.6525-6538.1996 · Cited by 230 · see citing works
Bacterial sex pheromone-induced plasmid transfer
Clewell, D. B. (1993) · Cell · doi:10.1016/0092-8674(93)90153-h · Cited by 223 · see citing works
Sensing Starvation: a Homoserine Lactone—Dependent Signaling Pathway in Escherichia coli
Huisman, G. W., & Kolter, R. (1994) · Science · doi:10.1126/science.7545940 · Cited by 217 · see citing works
Cell density-dependent growth of Myxococcus xanthus on casein
ROSENBERG, E. B., Keller, K. H., & Dworkin, M. (1977) · Journal of Bacteriology · doi:10.1128/jb.129.2.770-777.1977 · Cited by 215 · see citing works
Selfish operons and speciation by gene transfer
Lawrence, J. G. (1997) · Trends in Microbiology · doi:10.1016/s0966-842x(97)01110-4 · Cited by 210 · see citing works
Bioremediation of organic compounds — putting microbial metabolism to work
Bouwer, E. J., & Zehnder, A. J. B. (1993) · Trends in biotechnology · doi:10.1016/0167-7799(93)90159-7 · Cited by 207 · see citing works
Hall, B. G. (1988) · Genetics · doi:10.1093/genetics/120.4.887 · Cited by 199 · see citing works
Solomon, J. M., Magnuson, R. D., Srivastava, A., & Grossman, A. D. (1995) · Genes & Development · doi:10.1101/gad.9.5.547 · Cited by 199 · see citing works
Extracellular control of spore formation in Bacillus subtilis.
Grossman, A. D., & Losick, R. M. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.12.4369 · Cited by 196 · see citing works
The significances of bacterial colony patterns
Shapiro, J. A. (1995) · BioEssays · doi:10.1002/bies.950170706 · Cited by 195 · see citing works
Self-citationObservations on the formation of clones containing araB-lacZ cistron fusions
Shapiro, J. A. (1984) · Molecular and General Genetics MGG · doi:10.1007/bf00383501 · Cited by 194 · see citing works
Self-citationAUTOREGULATORY FACTORS AND COMMUNICATION IN ACTINOMYCETES
Horinouchi, S., & Beppu, T. (1992) · Annual Review of Microbiology · doi:10.1146/annurev.mi.46.100192.002113 · Cited by 193 · see citing works
Bacteriological composition and structure of granular sludge adapted to different substrates
Grotenhuis, J. T. C., Smit, M. P. J., Plugge, C. M., Xu, Y. S., van Lammeren, A., Stams, A. J. M., & Zehnder, A. J. B. (1991) · Applied and Environmental Microbiology · doi:10.1128/aem.57.7.1942-1949.1991 · Cited by 191 · see citing works
Adaptation of a conjugal transfer system for the export of pathogenic macromolecules
Winans, S. C., Burns, D., & Christie, P. J. (1996) · Trends in Microbiology · doi:10.1016/0966-842x(96)81513-7 · Cited by 190 · see citing works
Matsuyama, T., Kaneda, K., Nakagawa, Y., et al. (1992) · Journal of Bacteriology · doi:10.1128/jb.174.6.1769-1776.1992 · Cited by 190 · see citing works
Cell density-regulated recovery of starved biofilm populations of ammonia-oxidizing bacteria
Batchelor, S. E., Cooper, M., Chhabra, S. R., Glover, L. A., Stewart, G. S., Williams, P., & Prosser, J. I. (1997) · Applied and Environmental Microbiology · doi:10.1128/aem.63.6.2281-2286.1997 · Cited by 187 · see citing works
Who's competent and when: regulation of natural genetic competence in bacteria
Solomon, J. M., & Grossman, A. D. (1996) · Trends in Genetics · doi:10.1016/0168-9525(96)10014-7 · Cited by 184 · see citing works
McGowan, S. J., Sebaihia, M., Jones, S., et al. (1995) · Microbiology · doi:10.1099/13500872-141-3-541 · Cited by 174 · see citing works
Schripsema, J., de Rudder, K. E. E., van Vliet, T. B., et al. (1996) · Journal of Bacteriology · doi:10.1128/jb.178.2.366-371.1996 · Cited by 169 · see citing works
Intracellular signalling as a parallel distributed process
Bray, D. (1990) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(05)80268-1 · Cited by 166 · see citing works
Schmidt, J. E., & Ahring, B. K. (1993) · Applied and Environmental Microbiology · doi:10.1128/aem.59.8.2546-2551.1993 · Cited by 143 · see citing works
Foster, P. L. (1997) · Journal of Bacteriology · doi:10.1128/jb.179.5.1550-1554.1997 · Cited by 143 · see citing works
Morphological Changes in Growth Phenomena of Bacterial Colony Patterns
Ohgiwari, M., Matsushita, M., & Matsuyama, T. (1992) · Journal of the Physical Society of Japan · doi:10.1143/jpsj.61.816 · Cited by 141 · see citing works
Adaptive self-organization during growth of bacterial colonies
Ben-Jacob, E., Shmueli, H., Shochet, O., & Tenenbaum, A. (1992) · Physica A Statistical Mechanics and its Applications · doi:10.1016/0378-4371(92)90002-8 · Cited by 140 · see citing works
Intercellular C-signaling and the traveling waves of Myxococcus.Preprint
Sager, B., & Kaiser, D. (1994) · Genes & Development · doi:10.1101/gad.8.23.2793 · Cited by 138 · see citing works
Multicellular oxidant defense in unicellular organisms.
Ma, M., & Eaton, J. W. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.17.7924 · Cited by 138 · see citing works
Chapon, V., Akrim, M., Latifi, A., et al. (1997) · Molecular Microbiology · doi:10.1046/j.1365-2958.1997.4271794.x · Cited by 137 · see citing works
Evidence that F plasmid transfer replication underlies apparent adaptive mutation.
Galitski, T., & Roth, J. R. (1995) · Science · doi:10.1126/science.7716546 · Cited by 133 · see citing works
Nature of the Swarming Phenomenon in Proteus
Williams, F. D., & Schwarzhoff, R. H. (1978) · Annual Review of Microbiology · doi:10.1146/annurev.mi.32.100178.000533 · Cited by 133 · see citing works
The chain of command in Pseudomonas quorum sensing
Pesci, E. C., & Iglewski, B. H. (1997) · Trends in Microbiology · doi:10.1016/s0966-842x(97)01008-1 · Cited by 131 · see citing works
Gygi, D., Rahman, M. M., Lai, H., et al. (1995) · Molecular Microbiology · doi:10.1111/j.1365-2958.1995.mmi_17061167.x · Cited by 129 · see citing works
Cell surface properties correlated with cohesion in Myxococcus xanthus
Arnold, J. W., & Shimkets, L. J. (1988) · Journal of Bacteriology · doi:10.1128/jb.170.12.5771-5777.1988 · Cited by 126 · see citing works
Biochemical and structural analyses of the extracellular matrix fibrils of Myxococcus xanthus
Behmlander, R. M., & Dworkin, M. (1994) · Journal of Bacteriology · doi:10.1128/jb.176.20.6295-6303.1994 · Cited by 123 · see citing works
Do bacteria need to communicate with each other for growth?
Kaprelyants, A. S., & Kell, D. B. (1996) · Trends in Microbiology · doi:10.1016/0966-842x(96)10035-4 · Cited by 120 · see citing works
Evolution of bacterial transformation: is sex with dead cells ever better than no sex at all?
Redfield, R. J. (1988) · Genetics · doi:10.1093/genetics/119.1.213 · Cited by 119 · see citing works
Genome organization, natural genetic engineering and adaptive mutation.
Shapiro, J. A. (1997) · Trends in Genetics · doi:10.1016/s0168-9525(97)01058-5 · Cited by 115 · see citing works
Self-citationEberl, L., Christiansen, G., Molin, S., et al. (1996) · Journal of Bacteriology · doi:10.1128/jb.178.2.554-559.1996 · Cited by 115 · see citing works
Intercellular C-signaling in Myxococcus xanthus involves a branched signal transduction pathway.Preprint
Søgaard‐Andersen, L., Slack, F. J., Kimsey, H. H., et al. (1996) · Genes & Development · doi:10.1101/gad.10.6.740 · Cited by 113 · see citing works
Intercellular communication and group behavior in bacteria
Gray, K. M. (1997) · Trends in Microbiology · doi:10.1016/s0966-842x(97)01002-0 · Cited by 109 · see citing works
Gram-negative bacterial communication by N-acyl homoserine lactones: a universal language?
Swift, S., Bainton, N. J., & Winson, M. K. (1994) · Trends in Microbiology · doi:10.1016/0966-842x(94)90110-q · Cited by 107 · see citing works
Self-Affinity for the Growing Interface of Bacterial Colonies
Wakita, J.-I., Itoh, H., Matsuyama, T., et al. (1997) · Journal of the Physical Society of Japan · doi:10.1143/jpsj.66.67 · Cited by 106 · see citing works
Chemotaxis plays a role in the social behaviour of Myxococcus xanthus
Shi, W., Köhler, T., & Zusman, D. R. (1993) · Molecular Microbiology · doi:10.1111/j.1365-2958.1993.tb01720.x · Cited by 102 · see citing works
Formation of colony patterns by a bacterial cell population
Matsushita, M., Wakita, J.-I., Itoh, H., et al. (1999) · Physica A Statistical Mechanics and its Applications · doi:10.1016/s0378-4371(99)00328-3 · Cited by 102 · see citing works
Matsuyama, T., Bhasin, A., & Harshey, R. M. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.4.987-991.1995 · Cited by 102 · see citing works
Evolution of novel metabolic pathways for the degradation of chloroaromatic compounds
van der Meer, J. R. (1997) · Antonie van Leeuwenhoek · doi:10.1023/a:1000166400935 · Cited by 101 · see citing works
Kinetic model of Proteus mirabilis swarm colony development
Esipov, S. E., & Shapiro, J. A. (1998) · Journal of Mathematical Biology · doi:10.1007/s002850050100 · Cited by 98 · see citing works
Self-citationGivskov, M., Östling, J., Eberl, L., et al. (1998) · Journal of Bacteriology · doi:10.1128/jb.180.3.742-745.1998 · Cited by 97 · see citing works
Pheromones, social behaviour and the functions of secondary metabolism in bacteria
Kell, D. B., Kaprelyants, A. S., & Grafen, A. (1995) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(00)89013-8 · Cited by 95 · see citing works
Adaptive mutation in Escherichia coli: a role for conjugation
Jp, R., Pu, P., & Ms, F. (1995) · Science · doi:10.1126/science.7716545 · Cited by 94 · see citing works
Extracellular fibrils and contact-mediated cell interactions in Myxococcus xanthus
Behmlander, R. M., & Dworkin, M. (1991) · Journal of Bacteriology · doi:10.1128/jb.173.24.7810-7820.1991 · Cited by 92 · see citing works
(1993) · Springer eBooks · doi:10.1007/978-1-4757-9357-4 · Cited by 91 · see citing works
Organization of developing Escherichia coli colonies viewed by scanning electron microscopy
Shapiro, J. A. (1987) · Journal of Bacteriology · doi:10.1128/jb.169.1.142-156.1987 · Cited by 90 · see citing works
Self-citationSøgaard‐Andersen, L., & Kaiser, D. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.7.2675 · Cited by 90 · see citing works
Escherichia coli K-12 cell-cell interactions seen by time-lapse video
Shapiro, J. A., & Hsu, C. (1989) · Journal of Bacteriology · doi:10.1128/jb.171.11.5963-5974.1989 · Cited by 89 · see citing works
Self-citationAMyxococcus xanthuscell density-sensing system required for multicellular development
Kaplan, H. B., & Plamann, L. (1996) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1996.tb08185.x · Cited by 87 · see citing works
Control of exoenzyme production, motility and cell differentiation in Serratia liquefaciens
Givskov, M., Eberl, L., & Molin, S. (2006) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1997.tb10276.x · Cited by 86 · see citing works
ROSENBERG, E. B., & Varon, M. (1984) · Springer series in molecular biology · doi:10.1007/978-1-4613-8280-5_5 · Cited by 81 · see citing works
Regulation of directed motility in Myxococcus xanthus
Ward, M. J., & Zusman, D. R. (1997) · Molecular Microbiology · doi:10.1046/j.1365-2958.1997.4261783.x · Cited by 80 · see citing works
Torres, N. V., Voit, E. O., & Gonzalez-Alcon, C. M. (2000) · Biotechnology and Bioengineering · doi:10.1002/(sici)1097-0290(19960205)49:3 · Cited by 77 · see citing works
Toal, D. R., Clifton, S. W., Roe, B. A., et al. (1995) · Molecular Microbiology · doi:10.1111/j.1365-2958.1995.tb02291.x · Cited by 74 · see citing works
CONTROL OF CELL DENSITY AND PATTERN BY INTERCELLULAR SIGNALING IN MYXOCOCCUS DEVELOPMENT
Kim, S. K., Kaiser, D., & Kuspa, A. (1992) · Annual Review of Microbiology · doi:10.1146/annurev.mi.46.100192.001001 · Cited by 74 · see citing works
Ahring, B. K., Christiansen, N., Mathrani, I. M., et al. (1992) · Applied and Environmental Microbiology · doi:10.1128/aem.58.11.3677-3682.1992 · Cited by 72 · see citing works
Two cell-density domains within the Myxococcus xanthus fruiting body.
Sager, B., & Kaiser, D. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.8.3690 · Cited by 71 · see citing works
Burnham, J. C., Collart, S. A., & Highison, B. W. (1981) · Archives of Microbiology · doi:10.1007/bf00414699 · Cited by 71 · see citing works
Holotransformations of bacterial colonies and genome cybernetics
Ben‐Jacob, E., Tenenbaum, A., Shochet, O., et al. (1994) · Physica A Statistical Mechanics and its Applications · doi:10.1016/0378-4371(94)90165-1 · Cited by 70 · see citing works
Extracellular slime associated with Proteus mirabilis during swarming
Stahl, S. J., Stewart, K. R., & Williams, F. D. (1983) · Journal of Bacteriology · doi:10.1128/jb.154.2.930-937.1983 · Cited by 69 · see citing works
Programmed cell death in bacteria
Chaloupka, J., & Vinter, V. (1996) · Folia Microbiologica · doi:10.1007/bf02814658 · Cited by 66 · see citing works
The role of pheromones in bacterial interactions
Wirth, R., Muscholl, A., & Wanner, G. (1996) · Trends in Microbiology · doi:10.1016/0966-842x(96)81525-3 · Cited by 66 · see citing works
Tar-dependent and -independent pattern formation by Salmonella typhimurium
Blat, Y., & Eisenbach, M. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.7.1683-1691.1995 · Cited by 65 · see citing works
Hauser, G. (1885) · F.C.W. Vogel eBooks · doi:10.5962/bhl.title.51536 · Cited by 64 · see citing works
The roles of starvation and selective substrates in the emergence of araB‐lacZ fusion clones.
Maenhaut-Michel, G., & Shapiro, J. A. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06854.x · Cited by 63 · see citing works
Self-citationAhring, B. K., Schmidt, J. E., Winther-Nielsen, M., et al. (1993) · Applied and Environmental Microbiology · doi:10.1128/aem.59.8.2538-2545.1993 · Cited by 62 · see citing works
Isolated fibrils rescue cohesion and development in the Dsp mutant of Myxococcus xanthus
Chang, B. Y., & Dworkin, M. (1994) · Journal of Bacteriology · doi:10.1128/jb.176.23.7190-7196.1994 · Cited by 62 · see citing works
O’Rear, J. J., Alberti, L., & Harshey, R. M. (1992) · Journal of Bacteriology · doi:10.1128/jb.174.19.6125-6137.1992 · Cited by 60 · see citing works
Programmed cell death in bacteria: translational repression by mRNA end‐pairing
Franch, T., & Gerdes, K. (1996) · Molecular Microbiology · doi:10.1046/j.1365-2958.1996.771431.x · Cited by 60 · see citing works
Localization and quantification of extracellular polymers in methanogenic granular sludge
Grotenhuis, J. T. C., Smit, M. P. J., van Lammeren, A. A. M., et al. (1991) · Applied Microbiology and Biotechnology · doi:10.1007/bf00164710 · Cited by 60 · see citing works
(1949) · The Lancet · doi:10.1016/s0140-6736(49)90098-7 · Cited by 57 · see citing works
Patterns of reporter gene expression in the phase diagram of Bacillus subtilis colony forms
Mendelson, N. H., & Salhi, B. (1996) · Journal of Bacteriology · doi:10.1128/jb.178.7.1980-1989.1996 · Cited by 57 · see citing works
Tactic behavior of Myxococcus xanthus
Dworkin, M. (1983) · Journal of Bacteriology · doi:10.1128/jb.154.1.452-459.1983 · Cited by 56 · see citing works
Molecular handles on adaptive mutation
Rosenberg, S. M., Harris, R. S., & Torkelson, J. D. (1995) · Molecular Microbiology · doi:10.1111/j.1365-2958.1995.mmi_18020185.x · Cited by 56 · see citing works
Differential activity of a transposable element in Escherichia coli colonies
Shapiro, J. A., & Higgins, N. (1989) · Journal of Bacteriology · doi:10.1128/jb.171.11.5975-5986.1989 · Cited by 52 · see citing works
Self-citationMacario, A. J. L., Visser, F. A., van Lier, J. B., et al. (1991) · Journal of General Microbiology · doi:10.1099/00221287-137-9-2179 · Cited by 51 · see citing works
H-NS and RpoS regulate emergence of Lac Ara+ mutants of Escherichia coli MCS2
Gómez-Gómez, J., Blázquez, J., Baquero, F., & Martínez, J. (1997) · Journal of Bacteriology · doi:10.1128/jb.179.14.4620-4622.1997 · Cited by 49 · see citing works
CELLULAR CHANGES ACCOMPANYING THE SWARMING OF PROTEUS MIRABILIS: I. OBSERVATIONS OF LIVING CULTURES
Hoeniger, J. F. M. (1964) · Canadian Journal of Microbiology · doi:10.1139/m64-001 · Cited by 49 · see citing works
Shapiro, J. A. (1984) · Microbiology · doi:10.1099/00221287-130-5-1169 · Cited by 48 · see citing works
Self-citationPheromone produced by the myxobacterium Stigmatella aurantiaca
Stephens, K. E., Hegeman, G., & White, D. (1982) · Journal of Bacteriology · doi:10.1128/jb.149.2.739-747.1982 · Cited by 47 · see citing works
Signal transduction and secondary metabolism: prospects for controlling productivity
Beppu, T. (1995) · Trends in biotechnology · doi:10.1016/s0167-7799(00)88961-1 · Cited by 44 · see citing works
Arrangement of pili in colonies of Neisseria gonorrhoeae
Todd, W. J., Wray, G. P., & Hitchcock, P. J. (1984) · Journal of Bacteriology · doi:10.1128/jb.159.1.312-320.1984 · Cited by 39 · see citing works
Spatial restriction of cellular differentiation.Preprint
Sager, B., & Kaiser, D. (1993) · Genes & Development · doi:10.1101/gad.7.9.1645 · Cited by 39 · see citing works
Scanning electron microscope study of Pseudomonas putida colonies
Shapiro, J. A. (1985) · Journal of Bacteriology · doi:10.1128/jb.164.3.1171-1181.1985 · Cited by 37 · see citing works
Self-citationDeath and transfiguration among bacteria.
Higgins, N. (1992) · TIBS -Trends in Biochemical Sciences. Regular ed · doi:10.1016/0968-0004(92)90376-k · Cited by 36 · see citing works
Redundant transfer of F' plasmids occurs between Escherichia coli cells during nonlethal selections
Peters, J. E., & Benson, S. A. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.3.847-850.1995 · Cited by 33 · see citing works
Structure function relationship in granular sludge.
Stams, A. J. M., Grotenhuis, J. T. C., & Zehnder, A. J. B. (1989) · Socio-Environmental Systems Modeling · Cited by 32 · see citing works
Pattern and control in bacterial colony development.
Shapiro, J. A. (1992) · PubMed · Cited by 29 · see citing works
Self-citationA substance produced by competent Bacillus cereus 569 cells that affects transformability
Felkner, I. C., & Wyss, O. (1964) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(64)90217-7 · Cited by 28 · see citing works
Gene transfer in Neisseria gonorrhoeae
Biswas, G. D., Thompson, S. A., & Sparling, P. F. (1989) · Clinical Microbiology Reviews · doi:10.1128/cmr.2.suppl.s24 · Cited by 27 · see citing works
Characterization of a new sporulation factor in Bacillus subtilis
Waldburger, C. D., Gonzalez, D., & Chambliss, G. H. (1993) · Journal of Bacteriology · doi:10.1128/jb.175.19.6321-6327.1993 · Cited by 24 · see citing works
Kinniment, S., & WIMPENNY, J. W. T. (1990) · International Biodeterioration · doi:10.1016/0265-3036(90)90058-f · Cited by 22 · see citing works
Patterns of gene expression in Bacillus subtilis colonies
Salhi, B., & Mendelson, N. H. (1993) · Journal of Bacteriology · doi:10.1128/jb.175.16.5000-5008.1993 · Cited by 20 · see citing works
Microbial Biofilms and Biofilm Reactors
Peyton, B., & Characklis, W. G. (2018) · Routledge eBooks · doi:10.1201/9781315138954-6 · Cited by 19 · see citing works
Shapiro, J. A. (1992) · Journal of Bacteriology · doi:10.1128/jb.174.22.7262-7272.1992 · Cited by 18 · see citing works
Self-citationTHE ZONATION PHENOMENON AND STRUCTURE OF THE SWARM COLONY IN PROTEUS MIRABILIS
Bisset, K. A. (1973) · Journal of Medical Microbiology · doi:10.1099/00222615-6-4-429 · Cited by 15 · see citing works
Immunochemistry and localization of the enzyme disaggregatase in Methanosarcina mazei
de Macario, E. C., Macario, A. J. L., Mok, T., et al. (1993) · Journal of Bacteriology · doi:10.1128/jb.175.10.3115-3120.1993 · Cited by 14 · see citing works
The effect of streptomycin on ribosomal function.
Gorini, L., & Davies, J. (1968) · PubMed · Cited by 13 · see citing works
Recent notes on the mechanism of the Proteus swarming phenomenon. A review.
Sturdza, S. A. (1979) · PubMed · Cited by 3 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Sies, H., Berndt, C., & Jones, D. P. (2017) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-061516-045037 · Cited by 3,520 · see citing works
Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection.
WEST, S. A., GRIFFIN, A. S., & GARDNER, A. (2007) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2006.01258.x · Cited by 1,889 · see citing works
Gene Regulation at the Single-Cell Level
Rosenfeld, N., Young, J. W., Alon, U., Swain, P. S., & Elowitz, M. B. (2005) · Science · doi:10.1126/science.1106914 · Cited by 1,104 · see citing works
The Evolution of Multicellularity: A Minor Major Transition?
Grosberg, R. K., & Strathmann, R. R. (2007) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev.ecolsys.36.102403.114735 · Cited by 732 · see citing works
Dental Plaque as a Microbial Biofilm
Marsh, P. D. (2004) · Caries Research · doi:10.1159/000077756 · Cited by 763 · see citing works
Lamont, I. L., Beare, P. A., Ochsner, U., Vasil, A. I., & Vasil, M. L. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.092016999 · Cited by 584 · see citing works
Alverdy, J., Holbrook, C., Rocha, F., Seiden, L., Licheng, R., Wu, Musch, M., Chang, E., Ohman, D., & Suh, S. (2000) · Annals of Surgery · doi:10.1097/00000658-200010000-00003 · Cited by 207 · see citing works
Ryall, B., Eydallin, G., & Ferenci, T. (2012) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.05028-11 · Cited by 160 · see citing works
Transcriptional regulatory networks in bacteria: from input signals to output responses
Seshasayee, A. S., Bertone, P., Fraser, G. M., & Luscombe, N. M. (2006) · Current Opinion in Microbiology · doi:10.1016/j.mib.2006.08.007 · Cited by 140 · see citing works
Defining Division of Labor in Microbial Communities
Giri, S., Waschina, S., Kaleta, C., & Kost, C. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.06.023 · Cited by 89 · see citing works
Microbiota of Cheese Ecosystems: A Perspective on Cheesemaking
Neviani, E., Gatti, M., Gardini, F., & Levante, A. (2025) · Foods · doi:10.3390/foods14050830 · Cited by 39 · see citing works
“This kind of super-organism activity reflects the multicellularity concept proposed by Shapiro [11,20], which is crucial for understanding the growth and development of complex prokaryotic ecosystems, where individual components interact and influence each other.”
Neviani, E., Levante, A., & Gatti, M. (2024) · Fermentation · doi:10.3390/fermentation10040186 · Cited by 17 · see citing works
Neviani, E. (2024) · Microorganisms · doi:10.3390/microorganisms12122443 · Cited by 5 · see citing works
Integrated information as a measure of cognitive processes in coupled genetic repressilators
Abrego, L., & Zaikin, A. (2019) · Entropy · doi:10.3390/e21040382 · Cited by 5 · see citing works
Erasmo, N. (2024) · International Journal of Clinical Microbiology and Biochemical Technology · doi:10.29328/journal.ijcmbt.1001029 · Cited by 1 · see citing works
- Authors
- Shapiro, J. A.
- Affiliations
- University of Chicago (US)
- Corresponding author
- Shapiro, James A.
- ORCID
- Shapiro, James A.
- Venue
- Annual Review of Microbiology
- Publisher
- Annual Reviews
- Published
- 1998-10
- Volume
- 52
- Issue
- 1
- Pages
- 81-104
- ISSN
- 0066-4227 (ISSN-L)
- 1545-3251
- OpenAlex
- W2149134207
- Cited by
- 876
- References
- 163
- Citations by year
- 2026: 12 · 2025: 12 · 2024: 29 · 2023: 16 · 2022: 26 · 2021: 34 · 2020: 29 · 2019: 45 · 2018: 27 · 2017: 39 · 2016: 34 · 2015: 34 · 2014: 40 · 2013: 35 · 2012: 38
- FWCI
- 1.57
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by
- Locations
- Annual Review of Microbiology (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
- Keywords
- bacterial multicellularity, intercellular communication, quorum sensing, signal transduction, bacterial differentiation, colony development, swarming, division of labor, Escherichia coli, Bacillus subtilis, Proteus, Serratia
- MeSH terms
- Bacillus subtilis, Bacteria, Bacterial Adhesion, Cell Division, Escherichia coli, Proteus, Serratia, Spores, Bacterial, Signal Transduction, Bacterial Physiological Phenomena, Biofilms
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review