Abstract
The present work explores bacterial colonies and their individual and social behaviours under the lens of complex adaptive systems. We initially provide a background on the biology of bacteria to describe important phenomena, such as quorum-sensing, individual and collective behaviours, adaptation, evolution and self-organization over the influence of mechanical effects on bacterial systems and connecting scales. We then explore some associations between bacterial colonies and complex adaptive systems by considering components and ownerships of self-organization. The main contribution of this paper places emphasis on individual decision-making and behaviour as a cause of bacterial colonies’ actions, i.e., how self-organization and collective behaviours impact the ability of a bacterial colony to address an environmental stimulus and maintain itself as an open biological and fault-tolerant system. Finally, we conclude the work and provide some comments regarding future research.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.References
Allen RC, McNally L, Popat R, Brown SP (2016) Quorum sensing protects bacterial co-operation from exploitation by cheats. ISME J 10:1706
Ammor MS, Michaelidis C, Nychas G-JE (2008) Insights into the role of quorum sensing in food spoilage. J Food Prot 71:1510–1525
Bazurto JV, Downs DM (2016) Metabolic network structure and function in bacteria goes beyond conserved enzyme components. Microbial Cell 3:260–262
Ben-Jacob E (1997) From snowflake formation to growth of bacterial colonies II: cooperative formation of complex colonial patterns. Contemp Phys 38(3):205–241
Ben-Jacob E (2009) Learning from bacteria about natural information processing. Ann N Y Acad Sci 1178(1):78–90
Ben-Jacob E, Shmueli H, Shochet O, Tenenbaum A (1992) Adaptive self-organization during growth of bacterial colonies. Phys A 187(4):378–424
Ben-Jacob E, Shochet O, Tenenbaum A, Cohen I, Czirók A, Vicsek T (1994) Communication, regulation and control during complex patterning of bacterial colonies. Fractals 2(1):15–44
Ben-Jacob E, Shapira Y, Tauber AI (2006) Seeking the foundations of cognition in bacteria: from Schrödinger’s negative entropy to latent information. Phys A 359:495–524
Ben-Jacob E, Lu M, Schultz D, Onuchic JN (2014) The physics of bacterial decision making. Front Cell Infect Microbiol 4:154
Berk V, Fong JC, Dempsey GT, Develioglu ON, Zhuang X, Liphardt JY et al (2012) Molecular architecture and assembly principles of Vibrio cholerae biofilms. Science 337:236–239
Blair KM, Winkelman JT, Berg HC, Kearns DB (2008) A molecular clutch disables flagella in the Bacillus subtilis biofilm. Science 320:1636–1638
Blume LE, Durlauf SN (2005) The economy as an evolving complex system, III: current perspectives and future directions. Oxford University Press, Oxford
Bonabeau E (1998) Social insect colonies as complex adaptive systems. Ecosystems 5:437–443
Bowsher CG, Swain PS (2014) Environmental sensing, information transfer, and cellular decision-making. Curr Opin Biotechnol 28:149–155
Bravo JA, Forsythe P, Chew MV, Savignac HM, Dinana TG, Bienenstock J et al (2011) Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci 108:16050
Chen H, Zhu Y, Hu K (2010) Multi-colony bacteria foraging optimization with cell-to-cell communication for RFID network planning. Appl Soft Comput 10:539–547
Chew SC, Kundukad B, Seviour T, Van der Maarel JR, Yang LA, Doyle P et al (2014) Dynamic remodeling of microbial biofilms by functionally distinct exopolysaccharides. MBio 5:e01536–e015314
Choe JC, Crespi BJ (1997) The evolution of social behaviour in insects and arachnids. Cambridge University Press, Cambridge
Clark DJ (1967) DNA replication and the division cycle in Escherichia coli. J Mol Biol 99:99–112
Cornforth DM, Popat R, McNally L, Gurney J, Scott-Phillips TC, Brown SP (2014) Combinatorial quorum sensing allows bacteria to resolve their social and physical environment. Proc Natl Acad Sci 111:4280–4284
Crespi BJ (2001) The evolution of social behavior in microorganisms. Trends Ecol Evol 16:178–183
Darwin C (1859) On the origin of species: by means of natural selection, or the preservation of favoured races in the struggle for life. Bantam Classics, New York City
de Castro LN (2006) Fundamentals of natural computing: basic concepts, algorithms, and applications. CRC Press, Boca Raton
De Kievit TR, Gillis R, Marx S, Brown C, Iglewski BH (2001) Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns. Appl Environ Microbiol 67:1865–1873
de Vargas Roditi L, Boyle KE, Xavier JB (2013) Multilevel selection analysis of a microbial social trait. Mol Syst Biol 9:684
Decho AW (1994) Exopolymers in microbial mats: assessing their adaptive roles. Microb Mats Struct Dev Environ Signif 35:215–219
Del-Claro K, Tizo-Pedroso E (2009) Ecological and evolutionary pathways of social behavior in Pseudoscorpions (Arachnida: Pseudoscorpiones). Acta Ethol 12:13–22
Dessaux Y, Chapelle E, Faure D (2011) Quorum sensing and quorum quenching in soil ecosystems. Biocommun Soil Microorg 23:339–367
Dworkin M (1996) Recent advances in the social and developmental biology of the myxobacteria. Microbiol Rev 60(1):70–102
Even-Tov E, Bendori SO, Valastyan J, Ke X, Pollak S, Bareia T et al (2016) Social evolution selects for redundancy in bacterial quorum sensing. PLoS Biol 14:e1002386
Farrell FD, Gralka M, Hallatschek O, Waclaw B (2017) Mechanical interactions in bacterial colonies and the surfing probability of beneficial mutations. J R Soc Interface 14:20170073
Fick A (1855) Ueber diffusion. Ann Phys 170:59–86
Finkelshtein A, Sirota-Madi A, Roth D, Ingham CJ, Ben Jacob E (2017) Paenibacillus vortex—a bacterial guide to the wisdom of the crowd. In: Gordon R, Seckbach J (eds) BIOCOMMUNICATION: sign-mediated interactions between cells and organisms. World Scientific, Singapore, pp 257–283
Fuqua C, Parsek MR, Greenberg EP (2001) Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 35(1):439–468
Gans J, Wolinsky M, Dunbar J (2005) Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309:1387–1390
Gell-Mann M (1994) Complex Adaptive Systems. Complex Metaphor Models Real Santa Fe Inst Stud Sci Complex 19:17–45
Ghosh P, Mondal J, Ben-Jacob E, Levine H (2015) Mechanically-driven phase separation in a growing bacterial colony. Proc Natl Acad Sci 112:E2166–E2173
Giguère A, Taylor A, Myrold D, Tennigkeit B, Bottomley B (2013) Nitrification responses of ammoniaoxidizing bacteria and archaea to ammonia additions in cropped and non-cropped soils. In: Abstracts of the international conference on nitrification. Tokyo
Goo E, An JH, Kang Y, Hwang I (2015) Control of bacterial metabolism by quorum sensing. Trends Microbiol 23(9):567–576
Gram HC (1884) Ueber die isolirte Färbung der Schizomyceten: in Schnitt-und Trockenpräparaten. Fortschr Med 2:185–189
Grantham T (1994) Does science have a “global goal?”: a critique of hull’s view of conceptual progress. Biol Philos 9:85–97
Grassé P-P (1959) La reconstruction du nid et les coordinations interindividuelles chezBellicositermes natalensis etCubitermes sp. la théorie de la stigmergie: essai d’interprétation du comportement des termites constructeurs. Insectes Soc 6(1):41–80
Guespin-Michel J, Kaufman M (2001) Positive feedback circuits and adaptive regulations in bacteria. Acta Biotheor 49:207–218
Haken H (1977) Synergetics. Phys Bull 28(9):412
Harshey RM (1994) Bees aren’t the only ones: swarming in Gram-negative bacteria. Mol Microbiol 13:389–394
Heylighen F (2008) Complexity and self-organization. Encycl Libr Infor Sci 3:1215–1224
Holland JH (1992) Complex adaptive systems. Daedalus 121:17–30
Holland JH (1995) Hidden order: how adaptation builds complexity. Addison-Wesley, Boston
Holland JH (1998) Emergence: from chaos to order. Oxford University Press, Oxford
Holland JH (2006) Studying complex adaptive systems. J Syst Sci Complexity 19:1–8
Holling CS, Peterson G, Marples P, Sendzimir J, Redford K, Gunderson L et al (1996) Self-organization in ecosystems: lumpy geometries, periodicities and morphologies. In: Walker BH, Steffen WL (eds) Global change and terrestrial ecosystems. Cambridge University Press, Cambridge, pp 346–384
Holmes RK, Jobling MG, Connell TD (1995) Gram-negative bacteria. In: Moss J, Iglewski B, Vaughan M, Tu AT (eds) Handbook of natural toxins: bacterial toxins and virulence factors in disease. CRC Press, Boca Raton
Johnson S (2002) Emergence: the connected lives of ants, brains, cities, and software. Simon and Schuster, New York City
Kawasaki K, Mochizuki A, Matsushita M, Umeda T, Shigesada N (1997) Modeling spatio-temporal patterns generated bybacillus subtilis. J Theor Biol 188:177–185
Krasteva PV, Fong JC, Shikuma NJ, Beyhan S, Navarro MV, Sondermann H (2010) Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science 327:866–868
Kümmerli R, Jiricny N, Clarke LS, West SA, Griffin AS (2009) Phenotypic plasticity of a cooperative behaviour in bacteria. J Evol Biol 22:589–598
Levin SA (1998) Ecosystems and the biosphere as complex adaptive systems. Ecosystems 1(5):431–436
Mayr E (2007) What makes biology unique? Considerations on the autonomy of a scientific discipline. Cambridge University Press, Cambridge
McCauley JL (1997) The new science of complexity. Discrete Dyn Nat Soc 1:17–30
McDougald D, Rice SA, Barraud N, Steinberg PD, Kjelleberg S (2012) Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal. Nat Rev Microbiol 10:39
Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Ann Rev Microbiol 55:165–199
Millet YA, Alvarez D, Ringgaard S, von Andrian UH, Davis BM, Waldor MK (2014) Insights into Vibrio cholerae intestinal colonization from monitoring fluorescently labeled bacteria. PLoS Pathog 10:e1004405
Mitchell M, Crutchfield JP, Hraber PT (1993) Dynamics, computation, and the “edge of chaos”: a re-examination. arXiv: preprint adap-org/9306003
Mitri S, Richard Foster K (2013) The genotypic view of social interactions in microbial communities. Annu Rev Genet 47:247–273
Modrow S, Falke D, Truyen U, Schätzl H (2013) Molecular virology. Springer, Berlin
Murshed M (2017) Social intelligence of bacteria. Bangladesh J Med Microbiol 8:1–2
Nadell CD, Bassler BL (2011) A fitness trade-off between local competition and dispersal in Vibrio cholerae biofilms. Proc Natl Acad Sci 108:14181–14185
Nadell CD, Drescher K, Wingreen NS, Bassler BL (2015) Extracellular matrix structure governs invasion resistance in bacterial biofilms. ISME J 9:1700
Ng W-L, Bassler BL (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222
Nicolis G, Nicolis C (2012) Foundations of complex systems: emergence, information and prediction. World Scientific, Singapore
Nicolis G, Prigogine I (1977) Self-organization in nonequilibrium systems (Vol. 19). Wiley, Hoboken
Niu BF, Tan LR, Li L (2010a) A review of bacterial foraging optimization Part II: applications and challenges. In: Huang D-S, McGinnity M, Heutte L, Zhang X-P (eds) International conference on intelligent computing. Springer, Berlin
Niu BF, Tan LR, Li L (2010b) A review of bacterial foraging optimization Part I: Background and development. In: Huang D-S, McGinnity M, Heutte L, Zhang X-P (eds) International conference on intelligent computing. Springer, Berlin
Odling-Smee FJ, Laland KN, Feldman MW (1996) Niche construction. Am Nat 147:641–648
O’Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Ann Rev Microbiol 54:49–79
Pawlowski M, Paterek T, Kaszlikowski D, Scarani V, Winter A, Zukowski M (2009) Information causality as a physical principle. Nature 461:1101–1104
Persat A, Nadell CD, Kim MK, Ingremeau F, Siryaporn A, Drescher K et al (2015) The mechanical world of bacteria. Cell 161(5):988–997
Pfeiffer T, Rutte C, Killingback T, Taborsky M, Bonhoeffer S (2005) Evolution of cooperation by generalized reciprocity. Proc R Soc Lond B Biol Sci 272:1115–1120
Pitz GF, Sachs NJ (1984) Judgment and decision: theory and application. Annu Rev Psychol 35(1):139–164
Popat R, Cornforth DM, McNally L, Brown SP (2015) Collective sensing and collective responses in quorum-sensing bacteria. J R Soc Interface 12:20140882
Prigogine I, Stengers I (1984) Order out of Chaos. Bantam Books, New York
Reid CR, Garnier S, Beekman M, Latty T (2015) Information integration and multiattribute decision making in non-neuronal organisms. Anim Behav 100:44–50
Ricard J (2003) What do we mean by biological complexity? C R Biol 326(2):133–140
Rickard AH, Gilbert P, High NJ, Kolenbrander PE, Handley PS (2003) Bacterial coaggregation: an integral process in the development of multi-species biofilms. Trends Microbiol 11:94–100
Roesch LF, Fulthorpe RR, Riva A, Casella G, Hadwin AK, Farmerie WG et al (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1:283–290
Ryan K, Ray CG, Ahmad N, Drew WL, Plorde J (2004) Erris medical microbiology. McGraw Hill, New York City
Scharf BE, Fahrner KA, Turner L, Berg HC (1998) Control of direction of flagellar rotation in bacterial chemotaxis. Nat Acad Sci 95:201–206
Schloss PD, Handelsman J (2006) Toward a census of bacteria in soil. PLoS Comput Biol 2(7):e92
Shimkets LJ (1990) Social and developmental biology of the myxobacteria. Microbiol Rev 54:473–501
Skindersoe ME, Alhede M, Phipps R, Yang L, Jensen PO, Rasmussen TB et al (2008) Effects of antibiotics on quorum sensing in Pseudomonas aeruginosa. Antimicrob Agents Chemother 52:3648–3663
Smith A (2009) The invisible hand. Penguin Books, London
Spencer H (1862) First principles (Vol. 1). Williams and Norgate, London
Stavropoulos T, Schultz D, Onuchic JN, Jacob E-B (2012) Breaking the code of bacteria decision making. Biophys J 102:288a
Stigler GJ (1950a) The development of utility theory. I. J Polit Econ 58:307–327
Stigler GJ (1950b) The development of utility theory. II. J Polit Econ 58:373–396
Stubbendieck RM, Vargas-Bautista C, Straight PD (2016) Bacterial communities: interactions to scale. Front Microbiol 7:1234
Thomson NR, Crow MA, McGowan SJ, Cox A, Salmond GP (2000) Biosynthesis of carbapenem antibiotic and prodigiosin pigment in Serratia is under quorum sensing control. Mol Microbiol 3(36):539–556
Tillisch K, Labus J, Kilpatrick L, Jiang Z, Stains J, Ebrat B et al (2013) Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology 144:1394–1401
van Helden J, Toussaint A, Thieffry D (2012) Bacterial molecular networks—methods and protocols, vol 804. Humana Press
Visick KL, Foster J, Doino J, McFall-Ngai M, Ruby EG (2000) Vibrio fischeri lux genes play an important role in colonization and development of the host light organ. J Bacteriol 182:4578–4586
Wadhams GH, Armitage JP (2004) December). Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 5:1024–1037
Wesseling P (2009) Principles of computational fluid dynamics (Vol. 29). Springer, Berlin
Wilson RA, Keil FC (2001) The MIT encyclopedia of the cognitive sciences. MIT Press, Cambridge
Wingender J, Neu TR, Flemming H-C (2012) Microbial extracellular polymeric substances: characterization, structure and function. Springer, Berlin
Woodward DE, Tyson R, Myerscough MR, Murray JD, Budrene EO, Berg HC (1995) Spatio-temporal patterns generated by Salmonella typhimurium. Biophys J 68:2181–2189
Zaraté P (2014) Cooperative decision support systems. Agora University Editing House, Oradea
Acknowledgements
The authors thank Capes, CNPq, Fapesp, and MackPesquisa for their financial support. The authors also acknowledge the support of Intel for the Natural Computing and Machine Learning Laboratory as an Intel Artificial Intelligence Center of Excellence.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Cunha, D., Xavier, R. & de Castro, L.N. Bacterial colonies as complex adaptive systems. Nat Comput 17, 781–798 (2018). https://doi.org/10.1007/s11047-018-9689-7
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11047-018-9689-7