Synchronization of Electrical Oscillations in the Organization of Social Life of Microorganisms

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Abstract

Many microorganisms form communities whose members coordinate their actions in solving common problems. One form of such communities is a biofilm. In the experiments on recovering the integrity by a damaged biofilm, data were obtained on oscillators in relatively quiet and active loci of the film formed by cyanobacteria Oscillatoria terebriformis. To study the interaction between different parts of the biofilm, field potentials were recorded simultaneously from two loci. The presence of a functional connection between different zones of the biofilm was revealed by calculation of the cross-correlation coefficients. The level of synchronization of field potentials between areas was determined using the coefficients of frequency and frequency-time coherence. In the loci of increased and decreased activity, different values of the frequency and amplitude of electrical oscillations were revealed. A high level of synchronization was registered between the active zones, which persisted for several seconds. The registered synchronization of oscillations between the active and quiet loci was considerably lower. The results that characterize the organization of the process of problem solving by a cyanobacterial film as an integral unit can serve as a model of the processes of organization of other biosocial structures for solving problems.

General Information

Keywords: cyanobacteria, social organization, electrical oscillations, biofilms, synchronization, coherence, coordination, integration

Journal rubric: Evolutionary and Comparative Psychology

Article type: scientific article

DOI: https://doi.org/10.17759/exppsy.2020130310

Funding. The work was supported by the Ministry of Science and Higher Education, State Assns. nos. 0159-2019-0001 and 0159-2019-0009.

For citation: Grechenko T.N., Kharitonov A.N., Zhegallo A.V., Sumina E.L., Sumin D.L. Synchronization of Electrical Oscillations in the Organization of Social Life of Microorganisms. Eksperimental'naâ psihologiâ = Experimental Psychology (Russia), 2020. Vol. 13, no. 3, pp. 132–142. DOI: 10.17759/exppsy.2020130310.

References

  1. Grechenko T.N., Kharitonov A.N., Orleanskij V.K., Zhegallo A.V. Novye ob’ekty psihologicheskih issledovanij i perspektivy razvitiya nauki [New Objects of Psychological Studies]. Istoriya rossijskoj psihologii v licah. Dajdzhest = History of Russian psychology. Digest. 2017, no. 6, pp. 248—259 (in Russ.).
  2. Grechenko T.N., Kharitonov A.N., Zhegallo A.V. Social’nye struktury i kommunikacii v mire mikroorganizmov [Social Structures and Communications in the World of Microorganisms]. Eksperimental’naya psihologiya = Experimantal psychology, Russia. 2019, vol. 12, no. 4, pp. 106—119 (in Russian, abstr. Engl.).
  3. Grechenko T.N., Kharitonov A.N., Zhegallo A.V., Aleksandrov Yu.I. Psihofiziologicheskij analiz oscilljatornyh processov v povedenii biosocial’nyh system [Psychophysiological Analysis of Oscillatory Processes the Behavior of Biosocial Systems]. Psihologicheskij zhurnal =Psychological Journal (Rus.). 2015, vol. 36, no. 5, pp. 78—86 (in Russian, abstr. Engl.).
  4. Zotov M.V., Andrianova N.E. Processy koordinacii v vospriyatii kommunikativnogo vzaimodejstviya [Coordination Processes in the Perception of Communication]. Kognitivnye issledovaniya [Cognitive Studies], eds. D.V. Ushakov, A.A. Medyntsev. Publ. Institut psihologii RAN, 2017, pp. 50—67 (in Russ.).
  5. Livanov M.N. Prostranstvennaya organizaciya processov golovnogo mozga. Publ. Nauka, Moscow, 1972 (in Russ.).
  6. Magdanova L.A., Golyasnaya N.V. Geterogennost’ kak adaptivnoe svojstvo bakterial’noj populyacii [Heterogeneity as an Adaptive Property of a Bacterial Population]. Mikrobiologiya = Microbiology (Rus.). 2013, vol. 82, no. 1, p. 3. (in Russ.).
  7. Nikolaev Yu.A., Plakunov V.K. Bioplenka — gorod mikrobov ili analog mnogokletochnogo organizma [Biofilm: a City of Microbes or an Analog of a Multicellular Organism?]. Mikrobiologiya = Microbiology (Rus.), 2007, vol. 76, no. 2, pp. 149—163 (in Russ.).
  8. Novik G.I., Vysockij V.V. Arhitektonika populyacij bifidobakterij — submikroskopicheskij aspekt kogezii kletok Bifidobacterium adolescentis i Dofidobacterium bifidum [Architectonics of Bifidobacterial Population: a Submicroscopic Aspect of Cellular Cohesion of Bifidobacterium adolescentis and Dofidobacterium bifidum]. . Mikrobiologiya = Microbiology (Rus.),1995, vol. 64, no. 2, pp. 222—227 (in Russ.).
  9. Oleskin A.V. Biosocial’nost’ odnokletochnyh (na materiale issledovanij prokariot) [Biosociality of the Unicellular Organisms: Prokaryotes]. Zhurnal obshchej biologii = Journal of General Biology (Rus.), 2009, vol. 70, pp. 35—60. (in Russ.).
  10. Romanova Yu.M., Smirnova T.A., Andreev A.L., Il’ina T.S., Didenko L.V., Gincburg A.L. Obrazovanie bioplenok — primer social’nogo povedenija baktetij [Biofilm Formation as an Example of Social Behavior of Bacteria]. Mikrobiologiya = Microbiology (Rus.), 2006, vol. 75, no. 4, pp. 556—56. (in Russ.).
  11. Rybal’chenko O.V. Morfo-fiziologicheskie aspekty vzaimodejstvij mikroorganizmov v mikrobnyh soobshchestvah [Morpho-Physiological Aspects of Interactions of Microorganisms in Microbial Communities]. Diss. dokt. biol. nauk. 03.00 [Doctoral Dissertation, Biology 03.00]. Publ. S-Peterb. universitet, medicinskij f-t. [Faculty of Medicine, St.Petersburg University (Rus.)], Spb., 2003 (in Russ.).
  12. Sumina E.L. Povedenie nitchatyh cianobakterij v laboratornoj kul’ture [Behavior of Filamentous Cyanobacteria in Laboratory Culture] // Mikrobiologiya = Microbiology (Rus.), 2006, vol. 75, no 4, pp. 532—537. (in Russ.).
  13. Kharitonov A.N., Grechenko T.N., Sumina E.L., Sumin D.L., Orleanskij V.K. Social’naya zhizn’ cianobakterij [Social Life of Cyanobacteria]. Differencionno-integracionnaya teoriya razvitiya [Differentiation-Integration Theory of Development], eds. N.I. Chuprikova, E.V. Volkova. Publ. Yazyki slavyanskoj kul’tury, Moscow, 2014, Book 2, pp. 283—302 (in Russ.).
  14. Shapiro J.A. Bakterii kak mnogokletochnye organizmy [Bacteria as Multicellular Organisms]. V mire nauki = In the World of Science (Sci. Am., Rus. edition)1988, no. 8, pp. 46—55 (in Russ.).
  15. Sharova E.V. Fazovo-chastotnyj analiz v izuchenii nestabil’nosti elektroencefalogrammy [Phase and Frequency Analysis in the Studies of EEG Instability]. Fiziologiya cheloveka = Human Physiology (Rus.), 1980, vol. 6, no. 2, pp. 211—219 (in Russ.).
  16. Ahn S., Zauber E., Worth R.M., Witt Th., Rubchinsky L.L. Interaction of synchronized dynamics in cortex and basal ganglia in Parkinson’s disease. European Journal of Neuroscience, 2015, vol. 42, pp. 2164—2171.
  17. Ben-Jacob E., Cohen I., Gutnick D. Сooperative organization оf bacterial colonies: from genotype to morphotype. Annu. Rev. Microbiol., 1998, vol. 52, pp. 779—806.
  18. Bhattacharya J., Petsche H., Pereda E. Long-Range Synchrony in the Band: Role in Music Perception. Journal of Neuroscience, August 15, 2001, no. 21 (16), pp. 6329—6337.
  19. Canolty R.T., Knight R.T. The functional role of cross-frequency coupling. Trends Cogn. Sci., 2010 Nov; no. 14 (11), pp. 506—15.
  20. Czaran T., Hoekstra R. Microbial communication, cooperation and cheating: quorum sensing drives the evolution of cooperation in bacteria. PLoS ONE, 2009, vol. 4, no. 8, pp. 1—10.
  21. Dumas G., Nadel J., Soussignan R., Martinerie J., Garnero L. Inter-Brain Synchronization During Social Interaction. PLoS ONE, 2010, vol. 5, no. 8: e12166; doi.org/10.1371/journal.pone.0012166
  22. Fiegna F., Velicer G.J. Exploitative and hierarchical antagonism in a cooperative bacterium. PLoS Biol. 2005 Nov; 3 (11): e370. doi.org/10.1371/journal.pbio.0030370. Epub 2005, Nov 1.
  23. Fries P. Rhythms for cognition: communication through coherence. Neuron, 2015, vol. 88, pp. 220—235.
  24. Funane T., Kiguchi M., Atsumori H., Sato H., Kubota K., Koizumi H. Synchronous activity of two people’s prefrontal cortices during a cooperative task measured by simultaneous near-infrared spectroscopy. J. Biomed Opt., 2011, vol. 16, no. 7, 077011.
  25. Hu Yi, Hu Yi, Li X., Pan Y., Cheng X. Brain-to-brain synchronization across two persons predicts mutual prosociality. Social Cognitive and Affective Neuroscience, 2017, no. 12 (12), pp. 1835—1844; doi:10.1093/scan/nsx118
  26. Kelong Lu, Ning Hao. When do we fall in neural synchrony with others? Social Cognitive and Affective Neuroscience, 2019, vol 14, no. 3, pp. 253—261; doi.org/10.1093/scan/nsz012.
  27. Kingsbury L., Huang S., Wang J., Gu K., Golshani P., Wu Y.E., Hong W. Correlated Neural Activity and Encoding of Behavior across Brains of Socially Interacting Animals. Cell. 2019, no. 178, pp. 429—446.
  28. Liu J., Prindle A., Humphries J., Gabalda-Sagarra M., Munehiro A., Lee D.D., Ly S., Garcia-Ojalvo J., Suel G.M. Metabolic co-dependence gives rise to collective oscillations within biofilms. Nature, 2015, vol. 30, no. 523, pp. 550—554.
  29. Masi E., Ciszak M., Santopolo L., Frascella A., Giovannetti L., Marchi E., Viti C., Mancuso S. Electrical spiking in bacterial biofilms. Journal of the Royal Soc., Interface. 2015, Jan 6, no. 12 (102): 20141036. doi: 10.1098/rsif.2014.1036
  30. Nutman A.P., Bennett V.C., Friend C.R.L., van Kranendonk M.J., Chivas Allan R. Rapid emergence of life shown by discovery of 3,700-million-year-old microbial structures. Nature, 2016, no. 537 (7621), pp. 535—538. DOI:10.1038/nature19355. Epub 2016 Aug 31.
  31. Oleskin A.V., Shenderov B.A. Probiotics and Psychobiotics: the Role of Microbial Neurochemicals. Nature, 2019, no. 11 (4): 1071—1085. DOI:10.1007/s12602-019-09583-0 PMID: 31493127
  32. Shumway R.H., Stoffer D.S. Time series analysis and its applications. Springer Texts in Statistics, 2011.
  33. Shapiro J.A. The significances of bacterial colony patterns. BioEssays, 1995, vol. 17, no. 7, pp. 597—607.
  34. Snyder A.C., Issar D., Smith M.A. What Does Scalp EEG Coherence Tell Us About Long-range Cortical Networks? Eur. J. Neuroscience, 2018, no. 48 (7), pp. 2466—2481.
  35. Velicer G.J., Vos M. Sociobiology of the myxobacteria. Annu. Rev. Microbiol., 2009, no. 63, pp. 599—623.
  36. Von Bronk B., Schaffer S.A., Götz A., Opitz M. Effects of stochasticity and division of labor in toxin production on two-strain bacterial competition in Escherichia coli. PLoS Biol. 2017, May 1; 15 (5): e2001457. doi 10.1371/journal.pbio.2001457. eCollection 2017 May.
  37. Walter D.O. Coherence as a measure of relationship between EEG records // Electroencephalogr. Clin. Neurophysiol., 1968, vol. 24, no. 3, p. 282.

Information About the Authors

Tatyala N. Grechenko, Doctor of Psychology, Leading Research, Institute of Psychology, Russian Academy of Sciences, Moscow, Russia, ORCID: https://orcid.org/0000-0001-7361-4714, e-mail: grecht@mail.ru

Alexandr N. Kharitonov, PhD in Psychology, Senior Researcher, Institute of Psychology, Russian Academy of Sciences, Scientific and Educational Center for Biopsychological Research, Moscow Institute of Psychoanalysis (NOCHU VO “Moscow Institute of Psychoanalysis”); Leading Researcher at the Center for Experimental Psychology, Moscow State Psychological and Pedagogical University (FSBEI HE MGPPU), Deputy editor-in-chief of the scientific journal "Experimental Psychology", Moscow, Russia, ORCID: https://orcid.org/0000-0002-4801-9937, e-mail: ankhome47@list.ru

Alexander V. Zhegallo, PhD in Psychology, Senior Researcher at the Laboratory of Systems Research of the Psyche, Institute of Psychology of the Russian Academy of Sciences, Researcher at the Center for Experimental Psychology of MSUPE, Moscow, Russia, ORCID: https://orcid.org/0000-0002-5307-0083, e-mail: zhegalloav@ipran.ru

Evgeniya L. Sumina, PhD in Biology, Researcher, Faculty of Geology, Lomonosov Moscow State University, Moscow, Russia, ORCID: https://orcid.org/0000-0002-8848-2379, e-mail: stromatolit@list.ru

Dmitry L. Sumin, Paleontologist, Network Community of Researchers NISEEB, Moscow, Russia, ORCID: https://orcid.org/0000-0002-4455-0819, e-mail: stromatolit@list.ru

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