Ciliates learn to diagnose and correct classical error syndromes in mating strategies

Preconjugal ciliates learn classical repetition error-correction codes to safeguard mating messages and replies from corruption by “rivals” and local ambient noise. Because individual cells behave as memory channels with Szilárd engine attributes, these coding schemes also might be used to limit, diagnose, and correct mating-signal errors due to noisy intracellular information processing. The present study, therefore, assessed whether heterotrich ciliates effect fault-tolerant signal planning and execution by modifying engine performance, and consequently entropy content of codes, during mock cell–cell communication. Socially meaningful serial vibrations emitted from an ambiguous artificial source initiated ciliate behavioral signaling performances known to advertise mating fitness with varying courtship strategies. Microbes, employing calcium-dependent Hebbian-like decision making, learned to diagnose then correct error syndromes by recursively matching Boltzmann entropies between signal planning and execution stages via “power” or “refrigeration” cycles. All eight serial contraction and reversal strategies incurred errors in entropy magnitude by the execution stage of processing. Absolute errors, however, subtended expected threshold values for single bit-flip errors in three-bit replies, indicating coding schemes protected information content throughout signal production. Ciliate preparedness for vibrations selectively and significantly affected the magnitude and valence of Szilárd engine performance during modal and non-modal strategy corrective cycles. But entropy fidelity for all replies mainly improved across learning trials as refinements in engine efficiency. Fidelity neared maximum levels for only modal signals coded in resilient three-bit repetition error-correction sequences. Together, these findings demonstrate microbes can elevate survival/reproductive success by learning to implement classical fault-tolerant information processing in social contexts.

[1]  Nan Hao,et al.  Dose-to-Duration Encoding and Signaling beyond Saturation in Intracellular Signaling Networks , 2008, PLoS Comput. Biol..

[2]  A. Dickson On Evolution , 1884, Science.

[3]  Lov K. Grover A fast quantum mechanical algorithm for database search , 1996, STOC '96.

[4]  R. Michod,et al.  Evolution of individuality during the transition from unicellular to multicellular life , 2007, Proceedings of the National Academy of Sciences.

[5]  Koichiro Matsuno,et al.  Forming and maintaining a heat engine for quantum biology. , 2006, Bio Systems.

[6]  B. Crespi The evolution of social behavior in microorganisms. , 2001, Trends in ecology & evolution.

[7]  E. Ben-Jacob,et al.  Coexistence of amplitude and frequency modulations in intracellular calcium dynamics. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[8]  Ginestra Bianconi Size of quantum networks. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[9]  Kevin B Clark,et al.  On classical and quantum error-correction in ciliate mate selection , 2010, Communicative & integrative biology.

[10]  L. Ryan Lesion of the subthalamic nucleus or globus pallidus does not cause chaotic firing patterns in basal ganglia neurons in rats , 2000, Brain Research.

[11]  Wouter-Jan Rappel,et al.  Compartmentalization of second messengers in neurons: a mathematical analysis. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[12]  Erio Tosatti,et al.  Optimization by quantum annealing: Lessons from simple cases , 2005, cond-mat/0502129.

[13]  E. Ben-Jacob,et al.  Social behavior of bacteria: from physics to complex organization , 2008 .

[14]  W. Gibson Sex and evolution in trypanosomes. , 2001, International journal for parasitology.

[15]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[16]  F. Banuett Signalling in the Yeasts: An Informational Cascade with Links to the Filamentous Fungi , 1998, Microbiology and Molecular Biology Reviews.

[17]  H. Levine,et al.  Bacterial linguistic communication and social intelligence. , 2004, Trends in microbiology.

[18]  D. Holberton,et al.  Myonemal contraction of spirostomum. II. Some mechanical properties of the contractile apparatus , 1975, Journal of cellular physiology.

[19]  C. Plieth,et al.  Calcium: just another regulator in the machinery of life? , 2005, Annals of botany.

[20]  P. Schlievert,et al.  In Vivo Induction of Virulence and Antibiotic Resistance Transfer in Enterococcus faecalis Mediated by the Sex Pheromone-Sensing System of pCF10 , 2002, Infection and Immunity.

[21]  K. Cunningham,et al.  Fig1p Facilitates Ca2+ Influx and Cell Fusion during Mating of Saccharomyces cerevisiae* , 2003, Journal of Biological Chemistry.

[22]  E. Dent,et al.  The dynamic cytoskeleton: backbone of dendritic spine plasticity , 2011, Current Opinion in Neurobiology.

[23]  J. Heitman,et al.  Sex and virulence of human pathogenic fungi. , 2007, Advances in genetics.

[24]  A. Barabasi,et al.  Bose-Einstein condensation in complex networks. , 2000, Physical review letters.

[25]  C. Rao,et al.  Control, exploitation and tolerance of intracellular noise , 2002, Nature.

[26]  H. Iida,et al.  Subcellular localization and oligomeric structure of the yeast putative stretch-activated Ca2+ channel component Mid1. , 2004, Experimental cell research.

[27]  J. Pearson,et al.  Fire-diffuse-fire model of dynamics of intracellular calcium waves. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[28]  T. Hamilton,et al.  Behavioral Plasticity in Protozoans , 1975 .

[29]  L. D. Partridge,et al.  The sequential-interval state space: a means of displaying temporal information in neuron firing , 1989, Journal of Neuroscience Methods.

[30]  Manuel A. S. Santos,et al.  Evolution of pathogenicity and sexual reproduction in eight Candida genomes , 2009, Nature.

[31]  D. Cronkite A suppressor gene involved in chemical induction of conjugation in Paramecium aurelia. , 1975, Genetics.

[32]  Kenneth Webb,et al.  Evolution of Communication Simulation of Adaptive Behavior – Project Report , 2004 .

[33]  A. Opstal Dynamic Patterns: The Self-Organization of Brain and Behavior , 1995 .

[34]  Kevin B. Clark,et al.  Origins of learned reciprocity in solitary ciliates searching grouped 'courting' assurances at quantum efficiencies , 2010, Biosyst..

[35]  E. Ben-Jacob,et al.  Multimodal encoding in a simplified model of intracellular calcium signaling , 2009, Cognitive Processing.

[36]  A. Bishop Memoirs: Some Observations Upon Spirostomum ambiguum (Ehrenberg) , 1923 .

[38]  N. Ricci,et al.  Cell to cell contacts mediating mating‐type dependent recognition(s) during the preconjugant cell interactions of Oxytricha bifaria (ciliata, hypotrichida) , 1980 .

[39]  G. Dunny,et al.  A paracrine peptide sex pheromone also acts as an autocrine signal to induce plasmid transfer and virulence factor expression in vivo , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[40]  Peter S. Swain,et al.  Cross-Talk between Signaling Pathways Can Generate Robust Oscillations in Calcium and cAMP , 2009, PloS one.

[41]  I. Chuang,et al.  Quantum Computation and Quantum Information: Introduction to the Tenth Anniversary Edition , 2010 .

[42]  M. Redinbo,et al.  Disrupting antibiotic resistance propagation by inhibiting the conjugative DNA relaxase , 2007, Proceedings of the National Academy of Sciences.

[43]  James Ladyman,et al.  The connection between logical and thermodynamic irreversibility , 2007 .

[44]  F. Ritort,et al.  Bias and error in estimates of equilibrium free-energy differences from nonequilibrium measurements , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[45]  Kevin Bradley Clark,et al.  Bioreaction Quantum Computing without Quantum Diffusion , 2012 .

[46]  C. Alimenti,et al.  Autocrine, Mitogenic Pheromone Receptor Loop of the Ciliate Euplotes raikovi: Pheromone-Induced Receptor Internalization , 2005, Eukaryotic Cell.

[47]  Ginestra Bianconi Quantum statistics in complex networks. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[48]  F. Takens Detecting strange attractors in turbulence , 1981 .

[49]  Anthony Trewavas,et al.  Aspects of plant intelligence. , 2003, Annals of botany.

[50]  Gavan Lintern,et al.  Dynamic patterns: The self-organization of brain and behavior , 1997, Complex.

[51]  J. Keasling,et al.  Memory in Microbes: Quantifying History-Dependent Behavior in a Bacterium , 2008, PloS one.

[52]  J A Tuszynski,et al.  "Memory bytes" - molecular match for CaMKII phosphorylation encoding of microtubule lattices. , 2010, Journal of integrative neuroscience.

[53]  Jack A. Tuszynski,et al.  Neural cytoskeleton capabilities for learning and memory , 2009, Journal of biological physics.

[54]  Y. Nishiura,et al.  Obtaining multiple separate food sources: behavioural intelligence in the Physarum plasmodium , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[55]  N. Ricci The behaviour of ciliated protozoa , 1990, Animal Behaviour.

[56]  Ginestra Bianconi,et al.  Growing Cayley trees described by a Fermi distribution. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[57]  Charles H. Bennett,et al.  Notes on Landauer's Principle, Reversible Computation, and Maxwell's Demon , 2002, physics/0210005.

[58]  J. Shapiro Thinking about bacterial populations as multicellular organisms. , 1998, Annual review of microbiology.

[59]  T. Cavalier-smith,et al.  Origins of the machinery of recombination and sex , 2002, Heredity.

[60]  Avner Priel,et al.  Microtubule ionic conduction and its implications for higher cognitive functions. , 2010, Journal of integrative neuroscience.

[61]  X. L. Zhou,et al.  Ion channels in microbes. , 1999, Methods in enzymology.

[62]  P. Bruns,et al.  A conditional mutant having paralyzed cilia and a block in cytokinesis is rescued by cytoplasmic exchange in Tetrahymena thermophila. , 1988, Genetics.

[63]  Laura K. McKemmish,et al.  Weak, strong, and coherent regimes of Fröhlich condensation and their applications to terahertz medicine and quantum consciousness , 2009, Proceedings of the National Academy of Sciences.

[64]  D. Knecht,et al.  Mechano-chemical signaling maintains the rapid movement of Dictyostelium cells. , 2008, Experimental cell research.

[65]  Wei Ren,et al.  Determining the degree of chaos from analysis of ISI time series in the nervous system: a comparison between correlation dimension and nonlinear forecasting methods , 1998, Biological Cybernetics.

[66]  R. Johnstone SEXUAL SELECTION, HONEST ADVERTISEMENT AND THE HANDICAP PRINCIPLE: REVIEWING THE EVIDENCE , 1995, Biological reviews of the Cambridge Philosophical Society.

[67]  E. Eisenstein,et al.  A Behavioral Homeostasis Theory of Habituation and Sensitization: II. Further Developments and Predictions , 2006, Reviews in the neurosciences.

[68]  B. Bassler,et al.  Mob Psychology , 1910, The Hospital.

[69]  R. Johal Quantum heat engines and nonequilibrium temperature. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[70]  Kevin B. Clark,et al.  Social biases determine spatiotemporal sparseness of ciliate mating heuristics , 2012, Communicative & integrative biology.

[71]  S. S. Stevens On the brightness of lights and loudness of sounds , 1953 .

[72]  D. Lynn,et al.  The Ciliated Protozoa: Characterization, Classification, and Guide to the Literature , 2010 .

[73]  Key,et al.  Sexual behaviour in Euplotes raikovi is accompanied by pheromone-induced modifications of ionic currents. , 1999, The Journal of experimental biology.

[74]  Juan F. Poyatos,et al.  Trade-offs and Noise Tolerance in Signal Detection by Genetic Circuits , 2010, PloS one.

[75]  J. Knott The organization of behavior: A neuropsychological theory , 1951 .

[76]  E. Eisenstein,et al.  Habituation and sensitization in an aneural cell: Some comparative and theoretical considerations , 1982, Neuroscience & Biobehavioral Reviews.

[77]  Ben Lehner Conflict between Noise and Plasticity in Yeast , 2010, PLoS genetics.

[78]  Quantitative analysis of ciliary and contractile responses during habituation training in Spirostomum ambiguum. , 1974, Behavioral biology.

[79]  Wouter-Jan Rappel,et al.  A mathematical analysis of second messenger compartmentalization , 2008, Physical biology.

[80]  Pedro C. Marijuán,et al.  On prokaryotic intelligence: Strategies for sensing the environment , 2010, Biosyst..

[81]  N. Haga,et al.  Restoration of membrane excitability in a behavioral mutant of Paramecium caudatum during conjugation and by microinjection of wild- type cytoplasm , 1980, The Journal of cell biology.

[82]  J. Ghigo Natural conjugative plasmids induce bacterial biofilm development , 2001, Nature.

[83]  L. Katz Evolution of nuclear dualism in ciliates: a reanalysis in light of recent molecular data. , 2001, International journal of systematic and evolutionary microbiology.

[84]  R. McMahon Chemical Reactions Involving Quantum Tunneling , 2003, Science.

[85]  Kevin B. Clark,et al.  Bose-Einstein condensates form in heuristics learned by ciliates deciding to signal 'social' commitments , 2010, Biosyst..

[86]  The effects of vibratory and electrical stimulation on habituation in the ciliated protozoan, Spirostomum ambiguum. , 1973, Behavioral biology.

[87]  Sujal S. Phadke,et al.  Is Evolution of Mating Preferences Inevitable? Random Mating in the Multisex System of Tetrahymena thermophila , 2012, International journal of evolutionary biology.

[88]  Jürgen Kurths,et al.  Timing Cellular Decision Making Under Noise via Cell–Cell Communication , 2009, PloS one.

[89]  P. Freestone,et al.  Calcium signalling in bacteria , 1996, Journal of bacteriology.