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Bacterial colonies as complex adaptive systems

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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.

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Fig. 1
Fig. 2

Adapted from Ng and Bassler (2009)

Fig. 3
Fig. 4

Adapted from Clark (1967)

Fig. 5

Adapted from Niu et al. (2010a, b)

Fig. 6

Adapted from Reid et al. (2015)

Fig. 7

Adapted from Reid et al. (2015)

Fig. 8

Adapted from Ryan et al. (2004)

Fig. 9

Adapted from Popat et al. (2015)

Fig. 10

Adapted from Persat et al. (2015)

Fig. 11

Adapted from Persat et al. (2015)

Fig. 12

Adapted from Chen et al. (2010)

Fig. 13

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References

  • Allen RC, McNally L, Popat R, Brown SP (2016) Quorum sensing protects bacterial co-operation from exploitation by cheats. ISME J 10:1706

    Google Scholar 

  • Ammor MS, Michaelidis C, Nychas G-JE (2008) Insights into the role of quorum sensing in food spoilage. J Food Prot 71:1510–1525

    Google Scholar 

  • Bazurto JV, Downs DM (2016) Metabolic network structure and function in bacteria goes beyond conserved enzyme components. Microbial Cell 3:260–262

    Google Scholar 

  • 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

    Google Scholar 

  • Ben-Jacob E (2009) Learning from bacteria about natural information processing. Ann N Y Acad Sci 1178(1):78–90

    Google Scholar 

  • Ben-Jacob E, Shmueli H, Shochet O, Tenenbaum A (1992) Adaptive self-organization during growth of bacterial colonies. Phys A 187(4):378–424

    Google Scholar 

  • 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

    MATH  Google Scholar 

  • 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

    Google Scholar 

  • Ben-Jacob E, Lu M, Schultz D, Onuchic JN (2014) The physics of bacterial decision making. Front Cell Infect Microbiol 4:154

    Google Scholar 

  • 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

    Google Scholar 

  • Blair KM, Winkelman JT, Berg HC, Kearns DB (2008) A molecular clutch disables flagella in the Bacillus subtilis biofilm. Science 320:1636–1638

    Google Scholar 

  • Blume LE, Durlauf SN (2005) The economy as an evolving complex system, III: current perspectives and future directions. Oxford University Press, Oxford

    Google Scholar 

  • Bonabeau E (1998) Social insect colonies as complex adaptive systems. Ecosystems 5:437–443

    Google Scholar 

  • Bowsher CG, Swain PS (2014) Environmental sensing, information transfer, and cellular decision-making. Curr Opin Biotechnol 28:149–155

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Choe JC, Crespi BJ (1997) The evolution of social behaviour in insects and arachnids. Cambridge University Press, Cambridge

    Google Scholar 

  • Clark DJ (1967) DNA replication and the division cycle in Escherichia coli. J Mol Biol 99:99–112

    Google Scholar 

  • 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

    Google Scholar 

  • Crespi BJ (2001) The evolution of social behavior in microorganisms. Trends Ecol Evol 16:178–183

    Google Scholar 

  • 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

    Google Scholar 

  • de Castro LN (2006) Fundamentals of natural computing: basic concepts, algorithms, and applications. CRC Press, Boca Raton

    MATH  Google Scholar 

  • 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

    Google Scholar 

  • de Vargas Roditi L, Boyle KE, Xavier JB (2013) Multilevel selection analysis of a microbial social trait. Mol Syst Biol 9:684

    Google Scholar 

  • Decho AW (1994) Exopolymers in microbial mats: assessing their adaptive roles. Microb Mats Struct Dev Environ Signif 35:215–219

    Google Scholar 

  • Del-Claro K, Tizo-Pedroso E (2009) Ecological and evolutionary pathways of social behavior in Pseudoscorpions (Arachnida: Pseudoscorpiones). Acta Ethol 12:13–22

    Google Scholar 

  • Dessaux Y, Chapelle E, Faure D (2011) Quorum sensing and quorum quenching in soil ecosystems. Biocommun Soil Microorg 23:339–367

    Google Scholar 

  • Dworkin M (1996) Recent advances in the social and developmental biology of the myxobacteria. Microbiol Rev 60(1):70–102

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Fick A (1855) Ueber diffusion. Ann Phys 170:59–86

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Gans J, Wolinsky M, Dunbar J (2005) Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309:1387–1390

    Google Scholar 

  • Gell-Mann M (1994) Complex Adaptive Systems. Complex Metaphor Models Real Santa Fe Inst Stud Sci Complex 19:17–45

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Gram HC (1884) Ueber die isolirte Färbung der Schizomyceten: in Schnitt-und Trockenpräparaten. Fortschr Med 2:185–189

    Google Scholar 

  • Grantham T (1994) Does science have a “global goal?”: a critique of hull’s view of conceptual progress. Biol Philos 9:85–97

    Google Scholar 

  • 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

    Google Scholar 

  • Guespin-Michel J, Kaufman M (2001) Positive feedback circuits and adaptive regulations in bacteria. Acta Biotheor 49:207–218

    Google Scholar 

  • Haken H (1977) Synergetics. Phys Bull 28(9):412

    MathSciNet  MATH  Google Scholar 

  • Harshey RM (1994) Bees aren’t the only ones: swarming in Gram-negative bacteria. Mol Microbiol 13:389–394

    Google Scholar 

  • Heylighen F (2008) Complexity and self-organization. Encycl Libr Infor Sci 3:1215–1224

    Google Scholar 

  • Holland JH (1992) Complex adaptive systems. Daedalus 121:17–30

    Google Scholar 

  • Holland JH (1995) Hidden order: how adaptation builds complexity. Addison-Wesley, Boston

    Google Scholar 

  • Holland JH (1998) Emergence: from chaos to order. Oxford University Press, Oxford

    MATH  Google Scholar 

  • Holland JH (2006) Studying complex adaptive systems. J Syst Sci Complexity 19:1–8

    MathSciNet  MATH  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Johnson S (2002) Emergence: the connected lives of ants, brains, cities, and software. Simon and Schuster, New York City

    Google Scholar 

  • Kawasaki K, Mochizuki A, Matsushita M, Umeda T, Shigesada N (1997) Modeling spatio-temporal patterns generated bybacillus subtilis. J Theor Biol 188:177–185

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Levin SA (1998) Ecosystems and the biosphere as complex adaptive systems. Ecosystems 1(5):431–436

    Google Scholar 

  • Mayr E (2007) What makes biology unique? Considerations on the autonomy of a scientific discipline. Cambridge University Press, Cambridge

    Google Scholar 

  • McCauley JL (1997) The new science of complexity. Discrete Dyn Nat Soc 1:17–30

    MATH  Google Scholar 

  • 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

    Google Scholar 

  • Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Ann Rev Microbiol 55:165–199

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Modrow S, Falke D, Truyen U, Schätzl H (2013) Molecular virology. Springer, Berlin

    Google Scholar 

  • Murshed M (2017) Social intelligence of bacteria. Bangladesh J Med Microbiol 8:1–2

    Google Scholar 

  • 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

    Google Scholar 

  • Nadell CD, Drescher K, Wingreen NS, Bassler BL (2015) Extracellular matrix structure governs invasion resistance in bacterial biofilms. ISME J 9:1700

    Google Scholar 

  • Ng W-L, Bassler BL (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222

    Google Scholar 

  • Nicolis G, Nicolis C (2012) Foundations of complex systems: emergence, information and prediction. World Scientific, Singapore

    MATH  Google Scholar 

  • Nicolis G, Prigogine I (1977) Self-organization in nonequilibrium systems (Vol. 19). Wiley, Hoboken

    MATH  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Odling-Smee FJ, Laland KN, Feldman MW (1996) Niche construction. Am Nat 147:641–648

    Google Scholar 

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

    Google Scholar 

  • Pawlowski M, Paterek T, Kaszlikowski D, Scarani V, Winter A, Zukowski M (2009) Information causality as a physical principle. Nature 461:1101–1104

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Pitz GF, Sachs NJ (1984) Judgment and decision: theory and application. Annu Rev Psychol 35(1):139–164

    Google Scholar 

  • Popat R, Cornforth DM, McNally L, Brown SP (2015) Collective sensing and collective responses in quorum-sensing bacteria. J R Soc Interface 12:20140882

    Google Scholar 

  • Prigogine I, Stengers I (1984) Order out of Chaos. Bantam Books, New York

    Google Scholar 

  • Reid CR, Garnier S, Beekman M, Latty T (2015) Information integration and multiattribute decision making in non-neuronal organisms. Anim Behav 100:44–50

    Google Scholar 

  • Ricard J (2003) What do we mean by biological complexity? C R Biol 326(2):133–140

    MathSciNet  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Ryan K, Ray CG, Ahmad N, Drew WL, Plorde J (2004) Erris medical microbiology. McGraw Hill, New York City

    Google Scholar 

  • Scharf BE, Fahrner KA, Turner L, Berg HC (1998) Control of direction of flagellar rotation in bacterial chemotaxis. Nat Acad Sci 95:201–206

    Google Scholar 

  • Schloss PD, Handelsman J (2006) Toward a census of bacteria in soil. PLoS Comput Biol 2(7):e92

    Google Scholar 

  • Shimkets LJ (1990) Social and developmental biology of the myxobacteria. Microbiol Rev 54:473–501

    Google Scholar 

  • 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

    Google Scholar 

  • Smith A (2009) The invisible hand. Penguin Books, London

    Google Scholar 

  • Spencer H (1862) First principles (Vol. 1). Williams and Norgate, London

    Google Scholar 

  • Stavropoulos T, Schultz D, Onuchic JN, Jacob E-B (2012) Breaking the code of bacteria decision making. Biophys J 102:288a

    Google Scholar 

  • Stigler GJ (1950a) The development of utility theory. I. J Polit Econ 58:307–327

    Google Scholar 

  • Stigler GJ (1950b) The development of utility theory. II. J Polit Econ 58:373–396

    Google Scholar 

  • Stubbendieck RM, Vargas-Bautista C, Straight PD (2016) Bacterial communities: interactions to scale. Front Microbiol 7:1234

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Wadhams GH, Armitage JP (2004) December). Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 5:1024–1037

    Google Scholar 

  • Wesseling P (2009) Principles of computational fluid dynamics (Vol. 29). Springer, Berlin

    MATH  Google Scholar 

  • Wilson RA, Keil FC (2001) The MIT encyclopedia of the cognitive sciences. MIT Press, Cambridge

    Google Scholar 

  • Wingender J, Neu TR, Flemming H-C (2012) Microbial extracellular polymeric substances: characterization, structure and function. Springer, Berlin

    Google Scholar 

  • 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

    Google Scholar 

  • Zaraté P (2014) Cooperative decision support systems. Agora University Editing House, Oradea

    Google Scholar 

Download references

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.

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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

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