¿Flujo acústico, la “pequeña invención” de las cianobacterias?

Jair Koiller; Kurt M. Ehlers; Fabio Chalub

doi:10.3989/arbor.2010.746n1256

Autores/as

Jair Koiller Centro de Matemática Aplicada, Fundação Getulio Vargas
Kurt M. Ehlers Truckee Meadows Community College
Fabio Chalub Departamento de Matemática, Universidade Nova de Lisboa

DOI:

https://doi.org/10.3989/arbor.2010.746n1256

Palabras clave:

Flujo acústico, piezolelectricidad, membranas celulares, Synechococcus, cianobacterias

Resumen

Los mecanismos de bombeo en microingeniería aparecieron al principio de la década de los 90. El principio detrás de esto es el de flujo acústico. ¿Ha descubierto la Naturaleza este invento de hace 2.700 millones de años? Algunas cianobacterias marinas de la especie Synechococcus nadan 25 diámetros por segundo sin ningún medio visible de propulsión. Especulamos en este artículo que vibraciones de amplitud de nanoescala del estrato S (una cáscara cristalina que cubre las membranas exteriores en las cepas móviles) y con frecuencias del orden de 0,5-1,5 MHz (y esto es factible por los motores moleculares), podrían producir velocidades de deslizamiento del fluido, en el exterior de la frontera de la región Stokes. Dentro de esta capa límite (que para nuestra sorpresa resulta ser relativamente ancha) el comportamiento del flujo es rotacional (y en consecuencia, ventajoso desde el punto de vista biológico). Adicionalmente a este supuesto mecanismo que se podria llamar “nadando cantando”, mostramos otros posibles ejemplos biológicos de corrientes acústicas. Sir James Lighthill ha sugerido que el flujo acústico también se da en la cóclea del oído de los mamíferos, y son muy sugerentes los nuevos hallazgos en las células ciliadas externas. Otras posibilidades son flujos acústicos producidos por vibraciones de las membranas en células de levadura, mejorando su química (¡cerveza y pan!), el contoneo de los glóbulos rojos en los tubos capilares y el bombeo de fluido producido por las diatomeas.

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[1] Adams, D.G. (2001): “How do cyanobacteria glide?”, Microbiology Today, 28, 131-133.

[2] Ashmore, J. (2008): “Cochlear Outer Hair Cell Motility”, Physiol. Rev., 88: 173-210. doi:10.1152/physrev.00044.2006 PMid:18195086

[3] Ayala, F. J. (2007): “Darwin’s greatest discovery: Design without designer”, Proc. Nat. Acad. Sci 104, suppl 1, 8567-8573. doi:10.1073/pnas.0701072104 PMid:17494753 PMCid:1876431

[4] Ayala, F. J. (2007): Darwin y el diseño inteligente. Creacionismo, cristianismo y evolucionismo, Alianza Editorial, Madrid.

[5] Bailey, S.; Melis, A.; Mackey, K. R. M.; Cardol, P.; Finazzi, G.; van Dijken, G.; Berg, G. M.; Arrigo, K.; Shrager, J. y Grossman, A. (2008): “Alternative photosynthetic electron flow to oxygen in marine Synechococcus”, Biochim. biophys. acta 1777(3), 269-76. PMid:18241667

[6] Bardy, S.; Ng, S. Y. y Jarrell, K. F. (2008): “Prokaryotic motility structures”, Microbiology 149, 295-304. doi:10.1099/mic.0.25948-0 PMid:12624192

[7] Békésy, G. von (1960): Experiments in Hearing, McGraw-Hill Inc., NY.

[8] Bell, A. y Fletcher, N. (2004): “The cochlear amplifier as a standing wave: ‘squirting’ waves between rows of outer hair cells?”, J. Acoust. Soc. Am. 116: 2, 1016-1024. doi:10.1121/1.1766053 PMid:15376668

[9] Berg, H., “Bacterial flagellar motor”, Current Biology, 18: 16, R689-R691.

[10] Beyer, R. T. (1998): Sounds of our times: two hundred years of acoustics, Springer Verlag, New York.

[11] Biello, D. From Jaw to Ear: Transition Fossil Reveals Ear Evolution in Action, Scientific American, March 14, 2007.

[12] Cavalier-Smith, T.; Brasier, M. y Embley, T. M. (2006): Major steps in cell evolution, Discussion meeting Issue, Phil. Trans. Royal Society B, 361.

[13] Caicci, F.; Burighel, P. y Manni, L. (2007): “Hair cells in an ascidian (Tunicata) and their evolution in chordates”, Hearing Research 231 (1-2), 63-72. doi:10.1016/j.heares.2007.05.007 PMid:17611058

[14] Dallos, P.; Zheng, J. y Cheatham, M. (2006): “Prestin and the cochlear amplifier”, J. Physiol. 576: 1, 37-42. doi:10.1113/jphysiol.2006.114652 PMid:16873410 PMCid:1995634

[15] Darwin, C. (1859): The Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life, John Murray, London. online: http://www.talkorigins.org/faqs/origin.html.

[16] Davis, H. (1983): “An active process in cochlear mechanics”, Hearing Res. 9: 79-90. doi:10.1016/0378-5955(83)90136-3

[17] Desmond, A. y Moore, J. (2010): Darwin’s sacred cause: race, slavery and the quest for human origins, Penguin.

[18] Desmond, A. y Moore, J. (1991): Darwin, Michael Joseph.

[19] Drum, R. W. y Gordon, R. (2003): “Star Trek replicators and diatom nanotechnology”, Trends in Biotechnology, 21: 8, 325-328. doi:10.1016/S0167-7799(03)00169-0

[20] Ehlers, K. y Koiller, J. (2010): “Could cell membranes produce acoustic streaming? Making the case for Synechococcus self-propulsion”, Mathematical and Computer Modelling, Special Issue on Mathematical Methods and Modeling of Biophysical Phenomena, ed. by B. Perthame, P. Markowich, J. Zubelli (in press, linkinghub.elsevier.com/retrieve/pii/S089571771000172X). Preliminary version in http://arxiv.org/abs/0903.3781.

[21] Ehlers K. M.; Samuel, A. D.; Berg, H. C. y Montgomery, R. (1996): “Do cyanobacteria swim using traveling surface waves?”, Proc. Nat. Acad. Sci. 93: 16, 8340-8343. doi:10.1073/pnas.93.16.8340

[22] Fernández-Cara, E. y Zuazua, E. (2007): “Las matemáticas del control”, Arbor, 725, 383-394.

[23] Helmholtz, H. F. von (1874): “Théorie Physiologique de la Musique”, Masson G. Ed., Paris.

[24] Hoiczyk, E. y Hansel, A. (2000): “Cyanobacterial Cell Walls: News from an Unusual Prokaryotic Envelope”, J. of Bacteriology, 182: 5, 1191-1199. doi:10.1128/JB.182.5.1191-1199.2000 PMid:10671437 PMCid:94402

[25] Gallego-Jurez, J. A. (2007): “Acoustics for the 21st Century”, Plenary Lectures of the 19th International Congress on Acoustics, Revista de Acústica de la SEA, 38: 3-4, 7-15.

[26] Gallego-Jurez, J. A. (2008): “La acústica en las ciencias de la vida”, Plenary Lectures of the 19th International Congress on Acoustics, Revista de Acústica de la SEA, 39: 1-2, 5-15.

[27] García-Pichel, F.; Belnap, J.; Neuer, S. y Schanz, F. (2003): “Estimates of global cyanobacterial biomass and its distribution”, Archiv fr Hydrobiologie, 148, 213-227.

[28] Gordon, R.; Sterrenburg, F. y Sandhage, K. (2005): “Special Issue on Diatom Nanotechnology”, J. Nanoscience and Nanotechnology, 5: 1, 1-178. doi:10.1166/jnn.2005.017

[29] Guasto, J. y Breuer, K. (2008): Micro- velocimetry using time-resolved measurements of quantum dots in a microchannel, ECI International Conference on Heat Transfer and Fluid Flow in Microscale, Whistler.

[30] Guasto, J.; Leptos, K.; Gollub, J. P.; Pesci, A. y Goldstein, R. E. (2009): “Mixing by Swimming Algae”, arXiv:0910.1143v1. http://ecommons.library.cornell.edu/handle/1813/13741. Videos in: http://hdl.handle.net/1813/13741. http://physics.aps.org/articles/v3/84.

[31] Hamilton, M. F. y Blackstock, D.T. (1998): Nonlinear acoustics, Academic Press, San Diego. See http://asa.aip.org/books/nonlinearacoustics.html.

[32] Herrero, A. y Flores, E. (2008): The cyanobacteria: molecular biology, genomics and evolution, Horizon Scientific Press, Norwich, UK.

[33] Hutchinson, G. (2009): “Applying ultrasound technology to control algae and biofilm“, AALSO meeting (http://aalso.org/2009presentations=HutchinsonUltrasoundControlAlgae.pdf).

[34] Jackson, F. J. y Nyborg, W. L. (1958): “Small scale acoustic streaming near a locally excited membrane”, J. Acoust. Soc. America, 30: 7, 614-618. doi:10.1121/1.1909712

[35] Jarrell, K.F. y McBride, M. J. (2008): “The surprisingly diverse ways that prokaryotes move”, Nature Reviews: Microbiology, 6: 6, 466-476. doi:10.1038/nrmicro1900 PMid:18461074

[36] Kearns, D. B. (2007): “Bright Insight into Bacterial Gliding”, Science, 315, no. 5813, 773-774. doi:10.1126/science.1138995 PMid:17289965

[37] Kirschvink, J. L. (2005): “Red Earth, White Earth, Green Earth, Black Earth”, Engineering and Science/Caltech, 68: 4, 10-20.

[38] Koiller, J. (1999): “Movimiento de microorganismos”, La Gaceta de la Real Sociedad Matematica Española, 3: 2, 423-445.

[39] Koonin, E. (2009): “Darwinian evolution in the light of genomics”, Nucleic Acids Research, 37: 4, 1011-1034. PMid:19213802 PMCid:2651812

[40] Liberman, M. C.; Gao, J.; He, D.; Xudong Wu, X.; Jia, S. y Zuo, J. (2002): “Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier”, Nature, 419, 300-304. PMid:12239568

[41] Leptos, K. C.; Guasto, J. S.; Gollub, J. P.; Pesci, A. I. y Goldstein, R. E. (2009): “Dynamics of enhanced tracer diffusion in suspensions of swimming eukaryotic microorganisms”, Phys. Rev. Lett. 103(19), 198103. doi:10.1103/PhysRevLett.103.198103 PMid:20365957

[42] Lighthill, J. (1978): “Acoustic streaming”, J. Sound Vib., 61: 3, 391-418. doi:10.1016/0022-460X(78)90388-7

[43] Lighthill, J. (1992): “Acoustic streaming in the ear itself”, J. Fluid Mechanics, 239, 551-606. doi:10.1017/S0022112092004531

[44] Lighthill, J. (1993): “Biofluiddynamics: A Survey”, in Fluid Dynamics in Biology, Cheer, AY and van Dam, CP editors, American Mathematical Society.

[45] Lighthill, J. (1978): Waves in fluids, Cambridge University Press; 2 edition (December 3, 2001).

[46] Longuet-Higgins, M. S. (1953): “Mass transport in water waves”, Phil Trans. R. Soc. London Ser. A, 245, 535-581. doi:10.1098/rsta.1953.0006

[47] Maladen, R. D.; Ding, Y.; Li, C. y Goldman, D. I. (2009): “Undulatory Swimming in Sand: Subsurface Locomotion of the Sandfish Lizard”, Science, 325, 314-318. doi:10.1126/science.1172490 PMid:19608917

[48] Manley, G. A. (2000): “Cochlear mechanisms from a phylogenetic viewpoint”, Proc. Natl. Acad. Sci, 97: 22, 11736-11743. doi:10.1073/pnas.97.22.11736 PMid:11050203

[49] Manson, M. D.; Armitage, J. P.; Hoch, J. A. y Macnab, R. M. (1998): “Bacterial Locomotion and Signal Transduc tion” (minireview), J. Bacteriol., 180: 5, 1009-1022. PMid:9495737 PMCid:106986

[50] Marmottant, P. (2006): “Microfluidics with ultrasound-driven bubbles”, J. Fluid Mech., 568, 109-118. doi:10.1017/S0022112006002746

[51] Martínez-Sala, R.; Sancho, J.; Sánchez, L. V., Gómez, V.; Llinares, J. y Meseguer, F. (1995): “Sound attenuation by sculpture”, Nature, 378, 241. doi:10.1038/378241a0

[52] Martín-Molina, A.; Moreno-Flores, S.; Pérez, E.; Pum, D.; Sleytr, U. y Toca-Herrera, J. L. (2006): “Structure, Surface Interactions, and Compressibility of Bacterial S-Layers through Scanning Force Microscopy and the Surface Force Apparatus”, Biophys J., 90: 5, 1821-1829. doi:10.1529/biophysj.105.067041 PMid:16361337 PMCid:1367331

[53] Mauriello, E. M. F.; Astlinga, D. P., Sliusarenko, O. y Zusman, D. R. (2009): “Localization of a bacterial cytoplasmic receptor is dynamic and changes with cell-cell contacts”, Proc. Natl. Acad. Sci., 106: 12, 4852-4857. doi:10.1073/pnas.0810583106 PMid:19273862 PMCid:2660758

[54] Mauriello, E. M. (2010): “Cell polarity/ motility in bacteria: closer to eukaryotes than expected?”, The EMBO Journal, 29, 2258-2259. doi:10.1038/emboj.2010.144 PMid:20648047

[55] May, R. M. (2004): “Uses and Abuses of Mathematics in Biology”, Science, 303: 5659, 790-793. doi:10.1126/science.1094442 PMid:14764866

[56] Mauriello, E. M. F.; Mignot, T.; Yang, Z. y Zusman, D. R. (2010): “Gliding Motility Revisited: How Do the Myxobacteria Move without Flagella?”, Microb. Mol. Biology Reviews, 74: 2, 229-249. doi:10.1128/MMBR.00043-09 PMid:20508248

[57] McCarren, J. (2005): “Microscopic, genetic, and biochemical characterization of non-flagellar swimming motility in marine cyanobacteria”, Ph.D. Thesis. Scripps Institution of Oceanography, Univ. of California, San Diego. download from http://openwetware.org/wiki/JayMcCarren.

[58] Mignot, T.; Shaevitz, J. W.; Hartzell, P. L. y Zusman, D. R. (2007): “Evidence That Focal Adhesion Complexes Power Bacterial Gliding Motility”, Science, 315, no. 5813, 853-856. doi:10.1126/science.1137223 PMid:17289998

[59] Moroney, R. M.; White, R. M. y Howe, R. T. (1991): “Microtransport induced by ultrasonic Lamb waves”, Applied Physics Letters, 59: 7, 774-776. doi:10.1063/1.105339

[60] Nevo, R.; Charuvi, D.; Shimoni, E.; Schwarz, R.; Kaplan, A.; Ohad, I. y Ziv Reich, Z. (2007): “Thylakoid membrane perforations and connectivity enable intracellular traffic in cyanobacteria”, EMBO Journal, 26, 1467-1473. doi:10.1038/sj.emboj.7601594 PMid:17304210 PMCid:1817639

[61] Nisbet, E.; Bendall, D.; Christopher Howe, C. y Nisbet, E. (2008): “Photosynthetic and atmospheric evolution”, (discussion meeting issue), Proc. Royal Soc. B (Biological Sciences), 363: 1504. http://rstb.royalsocietypublishing.org/content/363/1504.toc

[62] Nyborg, W. L. (1958): “Acoustic Streaming near a Boundary”, J. Ac. Soc. America, 30: 4, 329-339. doi:10.1121/1.1909587

[63] Palenik, B.; Brahamsha, B.; Larimer, F. W.; Land, M.; Hauser, L.; Chain, P.; Lamerdin, J.; Regala, W.; Allen, E. E.; McCarren, J.; Paulsen, I.; Dufresne, A.; Partensky, F.; Webb, E. A. y Waterbury, J. (2003): “The genome of a motile marine Synechococcus”, Nature, 424 (6952), 1037-1042. doi:10.1038/nature01943 PMid:12917641

[64] Pallen, M. J. y Matzke, N. J. (2006): “From The Origin of Species to the origin of bacterial flagella”, Nature Reviews Microbiology, 4, 784-790. doi:10.1038/nrmicro1493 PMid:16953248

[65] Parker, A. R. y Townley, H. E. (2007): “Biomimetics of photonic nanostructures”, Nature Nanotechnology, 2, 347-353. doi:10.1038/nnano.2007.152 PMid:18654305

[66] Pelling, A.; Sehati, S.; Gralla, J.; Valentine, J. y Gimzewski, J. (2004): “Local Nanomechanical Motion of the Cell Wall of Saccharomyces cerevisiae”, Science, 305: 5687, 1147-115020. doi:10.1126/science.1097640 PMid:15326353

[67] Perelman, M. E. y Rubinstein, G. M. (2006): “Ultrasound vibrations of plant cells membranes: water lift in trees, electrical phenomena”, http://arxiv.org/abs/physics/0611133.

[68] Poggio, T. y Smale, S. (2003): “The Mathematics of Learning: Dealing with Data”, Notices of the Amer. Math. Soc., 50: 5, 537-544.

[69] Purcell, E. M. (1977): “Life at low Reynolds number”, Amer. J. Physics, 45, 3-11. http://jilawww.colorado.edu/perkinsgroup/Purcell_life_at_low_reynolds_number.pdf doi:10.1119/1.10903

[70] Purcell, E. M. (1997): “The efficiency of propulsion by a rotating flagellum”, Proc. Natl. Acad. Sci. USA, 94, 11307- 11311. http://www.pnas.org/content/94/21/11307.full.pdf doi:10.1073/pnas.94.21.11307

[71] Ragan, M. A.; McInerney, J. O. y Lake, J. A. (2009): “The network of life: genome beginnings and evolution”, Theme Issue, Phil. Trans. Royal Society B, 364.

[72] Lord Rayleigh (1877): The Theory of Sound, 1945 edition, Dover, New York.

[73] Lord Rayleigh (1883): “On the circulation of air observed in Kundt’s tubes, and on some allied acoustical problems”, Phil. Trans. 175, 1-21. doi:10.1098/rstl.1884.0002

[74] Lord Rayleigh (1885): “On Waves Propagated along the Plane Surface of an Elastic Solid”, Proc. London Math. Soc. s1-17, pp. 4-11.

[75] Read, N.; Connell, S. y Adams, D. G. (2007): “Nanonscale visualization of a fibrillar array in the cell wall of filamentous cyanobacteria and its implications for gliding motility”, J. Bacteriology, 189: 20, 7361-7366. doi:10.1128/JB.00706-07 PMid:17693519 PMCid:2168455

[76] Rehmeyer, J. (2009): “Darwin: The reluctant mathematician”, Science news, Web edition: Wednesday, February 11th, 2009. http://www.sciencenews.org/view/generic/id/40740/

[77] Riley, N (2001): “Steady Streaming”, Annual Review of Fluid Mechanics, 33: 43-65. doi:10.1146/annurev.fluid.33.1.43

[78] Samuel, A. D. T.; Petersen, J. D. y Reese, T. S. (2001): “Envelope structure of Synechococcus sp. WH8113, a nonflagellated swimming cyanobacterium”, BMC Microbiology, 1: 4. doi:10.1186/1471-2180-1-4 PMid:11329361 PMCid:31413

[79] Savater, F. (1986): El contenido de la felicidad, Aguilar.

[80] Serratosa, J. M. (2007): “El desarrollo de la investigación de materiales en España”, Arbor, 727, 687-704.

[81] Shapiro, L. (1995): “The Bacterial Flagellum: From Genetic Network to Complex Architecture”, Cell, 80, 525-527. doi:10.1016/0092-8674(95)90505-7

[82] Schuster, B.; Pum, D. y Sleytr, U. (2008): “S-layer stabilized lipid membranes (Review)”, Biointerphases, 3: 2, FA3-FA11. doi:10.1116/1.2889067 PMid:20408666 PMCid:2876325

[83] Smale, S. (1998): “Finding a horseshoe on the beaches of Rio”, The Mathematical Intelligencer, 20: 1, 39-44. doi:10.1007/BF03024399

[84] Smarda, J.; Smajs, D.; Komrska, J. y Krzyzanek, V. (2002): “S-layers on cell walls of cyanobacteria”, Micron, 33: 3, 257-277. doi:10.1016/S0968-4328(01)00031-2

[85] Smit, J. (2008): “Heads Up S-Layer Display: The Power of Many” Structure, 16: 8, 1151-1153. doi:10.1016/j.str.2008.07.003 PMid:18682215

[86] Sznitman, J. y Rösgen, T. (2008): “Acoustic Streaming Visualization in Elastic Spherical Cavities”, Journal of Visualization, 11: 4, 347-355. doi:10.1007/BF03182203

[87] Tanaka, S.; Kerfeld, C. A.; Sawaya, M. R.; Cai, F.; Heinhorst, S.; Cannon G. C. y Yeates, T. O. (2008): “Atomic-level models of the bacterial carboxysome shell”, Science, 319 (5866): 1083-1086. doi:10.1126/science.1151458 PMid:18292340

[88] Tang, J. W.; Qu, Q. Y.; Hao, H. W.; Chen, Y. y Wu, M. (2004): “Effect of 1.7 MHz ultrasound on a gas-vacuolate cyanobacterium and a gas-vacuole negative cyanobacterium”, Colloids and Surfaces B: Biointerfaces, 36: 2, 115-121. doi:10.1016/j.colsurfb.2004.06.003 PMid:15261016

[89] Thiffeault, J. L. and Childress, S. (2010): “Stirring by swimming bodies”, Physics Letters A, 374: 34, 3487-3490. doi:10.1016/j.physleta.2010.06.043

[90] Ueha, S. (2002): “Phenomena, theory and applications of near-fileld acoustic levitation”, Revista de Acústica, 33: 3-4, 21-25.

[91] van de Meent, J. W.; Tuval, I. y Goldstein, R. E. (2008): “Natures Microfluidic Transporter: Rotational Cytoplasmic Streaming at High Péclet Numbers”, Phys. Rev. Lett., 101, 178102. doi:10.1103/PhysRevLett.101.178102 PMid:18999789

[92] Vermeij, G. J. (2006): “Historical contingency and the purported uniqueness of evolutionary innovations”, Proc. Nat. Acad. Sci., 103: 6, 1804-1809. doi:10.1073/pnas.0508724103 PMid:16443685 PMCid:1413639

[93] Walsby, A. E. (1994): “Gas vesicles”, Microbiol. Mol. Biol. Rev., 58: 1, 94- 144.

[94] Waterbury, J. B.; Wiley, J. M.; Franks, D. G.; Valois, F. W. y Watson, S. W. (1985): “A Cyanobacterium Capable of Swimming Motility”, Science, 230: 4721, 74-76. doi:10.1126/science.230.4721.74 PMid:17817167

[95] Waterbury, J. B. (2004): “Little things matter a lot”, Oceanus, 43(2), 1-5. http://www.whoi.edu/oceanus/viewArticle. do?id = 3808

[96] White, R.M . (1997): “Acoustic interactions from Faraday’s crispations to MEMS”, Faraday Discuss., 107, 1-13. doi:10.1039/a707747e

[97] Wingreen, N. S. y Levin, S. A. (2006): “Cooperation among Microorganisms”, PLoS Biology, 4: 9, 1486-1488. http://www.plosbiology.org/article/info. doi/10.1371/ journal.pbio.0040299.

[98] Wolgemuth, C. W.; Igoshin, O. y Oster, G. (2003): “The motility of mollicutes”, Biophys. J., 85, 828-842.

[99] Wu, J. y Nyborg, W. (2008): “Ultrasound, cavitation bubbles and their interaction with cells”, Advanced drug delivery reviews, 60 (10), 1103-1116.

[100] Zhang, L.; Peyer, K. E. y Nelson, B. J. (2010): “Artificial bacterial flagella for micromanipulation”, Lab on a Chip, 10, 2203-2215. doi:10.1039/c004450b PMid:20567752