Journal of Statistical Physics

, Volume 167, Issue 3–4, pp 763–776 | Cite as

Subsurface Microbial Ecosystems: A Photon Flux and a Metabolic Cascade

  • Alexander P. Petroff
  • Frank Tejera
  • Albert Libchaber


Mud is a porous medium containing a high density of diverse microorganisms. It is out of equilibrium as the energy from a photon flux is dissipated by a cascade of biochemical reactions, mediated by the metabolisms of the constituent organisms. Despite its complexity, microbes in nature self-organize into simple reproducible patterns. We present two experiments in which the dynamics of natural mud coming to steady state are observed and modeled. In the first, the oxygen gradient produced by cyanobacteria in an imposed light gradient is measured. In the second, a thin front of oxygen-consuming microbes forms at the penetration depth of oxygen and moves with the changing oxygen gradient.


Ecology Reaction-diffusion Microbial mat Oxygen Pattern formation 


  1. 1.
    Morowitz, H.J.: Energy Flow in Biology; Biological Organization as a Problem in Thermal Physics. Academic Press, New York (1968)Google Scholar
  2. 2.
    Madigan, M.T., Martinko, J.M., Parker, J., et al.: Brock Biology of Microorganisms, vol. 514. Prentice Hall, Upper Saddle River (1997)Google Scholar
  3. 3.
    Castaing, B., Gunaratne, G., Heslot, F., Kadanoff, L., Libchaber, A., Thomae, S., Wu, X.Z., Zaleski, S., Zanetti, G.: Scaling of hard thermal turbulence in rayleigh-bénard convection. J. Fluid Mech. 204, 1–30 (1989)ADSCrossRefGoogle Scholar
  4. 4.
    Fenchel, T., Blackburn, H., King, G.M.: Bacterial Biogeochemistry: The Ecophysiology of Mineral Cycling. Academic Press, San Diego (2012)Google Scholar
  5. 5.
    Watnick, P., Kolter, R.: Biofilm, city of microbes. J. Bacteriol. 182(10), 2675–2679 (2000)CrossRefGoogle Scholar
  6. 6.
    Flemming, H., Wingender, J.: The biofilm matrix. Nat. Rev. Microbiol. 8(9), 623–633 (2010)Google Scholar
  7. 7.
    Stolz, J.: Structure of microbial mats and biofilms. In: Microbial Sediments, pp. 1–8. Springer, Berlin (2000)Google Scholar
  8. 8.
    Gilbert, W.: de Magnete magneticioque coporibus, et de magneto magnete terrure. London (1600)Google Scholar
  9. 9.
    Petroff, A., Libchaber, A.: Hydrodynamics and collective behavior of the tethered bacterium thiovulum majus. Proc. Natl. Acad. Sci. 111(5), E537–E545 (2014)ADSCrossRefGoogle Scholar
  10. 10.
    Petroff, A.P., Pasulka, A.L., Soplop, N., Wu, X.L., Libchaber, A.: Biophysical basis for convergent evolution of two veil-forming microbes. R. Soc. Open Sci. 2(11), 150437 (2015)MathSciNetCrossRefGoogle Scholar
  11. 11.
    Petroff, A.P., Wu, X.L., Libchaber, A.: Fast-moving bacteria self-organize into active two-dimensional crystals of rotating cells. Phys. Rev. Lett. 114(15), 158102 (2015)ADSCrossRefGoogle Scholar
  12. 12.
    Gans, J., Wolinsky, M., Dunbar, J.: Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309(5739), 1387–1390 (2005)ADSCrossRefGoogle Scholar
  13. 13.
    Pierson, B., Oesterle, A., Murphy, G.L.: Pigments, light penetration, and photosynthetic activity in the multi-layered microbial mats of great sippewissett salt marsh, massachusetts. FEMS Microbiol. Ecol. 3(6), 365–376 (1987)CrossRefGoogle Scholar
  14. 14.
    Pedrós-Alió, C.: Marine microbial diversity: can it be determined? Trends Microbiol. 14(6), 257–263 (2003)CrossRefGoogle Scholar
  15. 15.
    Pedrós-Alió, Carlos: The rare bacterial biosphere. Ann. Rev. Mar. Sci. 4, 449–466 (2012)CrossRefGoogle Scholar
  16. 16.
    Lynch, M., Neufeld, J.: Ecology and exploration of the rare biosphere. Nat. Rev. Microbiol. 13(4), 217–229 (2015)CrossRefGoogle Scholar
  17. 17.
    Fenchel, T.: Biogeography for bacteria. Science 301(5635), 925–926 (2003)CrossRefGoogle Scholar
  18. 18.
    De Wit, R., Bouvier, T.: Everything is everywhere, but, the environment selects; what did Baas Becking and Beijerinck really say? Environ. Microbiol. 8(4), 755–758 (2006)CrossRefGoogle Scholar
  19. 19.
    Lennon, J., Jones, S.: Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat. Rev. Microbiol. 9(2), 119–130 (2011)CrossRefGoogle Scholar
  20. 20.
    Martiny, J., et al.: Microbial biogeography: putting microorganisms on the map. Nat. Rev. Microbiol. 4(2), 102–112 (2006)CrossRefGoogle Scholar
  21. 21.
    Baas-Becking, L.: Geobiologie; of inleiding tot de milieukunde. The Hague (1934)Google Scholar
  22. 22.
    Howes, B., Howarth, R., Teal, J., Valiela, I.: Oxidation-reduction potentials in a salt marsh: spatial patterns and interactions with primary production. Limnol. Oceanogr. 26(2), 350–360 (1981)CrossRefGoogle Scholar
  23. 23.
    Nicholson, J., Stolz, J., Pierson, B.: Structure of a microbiol mat at Great Sippewissett Marsh, Cape Cod, Massachusetts. FEMS Microbiol. Ecol. 3(6), 343–364 (1987)CrossRefGoogle Scholar
  24. 24.
    Seitz, A., Nielsen, T., Overmann, J.: Physiology of purple sulfur bacteria forming macroscopic aggregates in Great Sippewissett Salt Marsh, Massachusetts. FEMS Microbiol. Ecol. 12(4), 225–235 (1993)CrossRefGoogle Scholar
  25. 25.
    Buckley, D., Baumgartner, L., Visscher, P.: Vertical distribution of methane metabolism in microbial mats of the Great Sippewissett Salt Marsh. Environ. Microbiol. 10(4), 967–977 (2008)CrossRefGoogle Scholar
  26. 26.
    Goldman, J., McCarthy, J.: Steady state growth and ammonium uptake of a fast-growing marine diatom. Limnol. Oceanogr. 23(4), 695–703 (1978)CrossRefGoogle Scholar
  27. 27.
    Falkovich, G.: Fluid Mechanics: A Short Course for Physicists. Cambridge University Press, Cambridge (2011)CrossRefMATHGoogle Scholar
  28. 28.
    Reynolds, C.S.: The Ecology of Phytoplankton. Cambridge University Press, Cambridge (2006)CrossRefGoogle Scholar
  29. 29.
    Redfield, A.C.: On the proportions of organic derivatives in sea water and their relation to the composition of plankton. University Press of Liverpool James Johnstone memorial volume (1934)Google Scholar
  30. 30.
    Catling, D.C., Claire, M.W.: How earth’s atmosphere evolved to an oxic state: a status report. Earth Planet. Sci. Lett. 237(1), 1–20 (2005)ADSCrossRefGoogle Scholar
  31. 31.
    Glud, R.N., Kühl, M., Kohls, O., Ramsing, N.B.: Heterogeneity of oxygen production and consumption in a photosynthetic microbial mat as studied by planar optodes. J. Phycol. 35(2), 270–279 (1999)CrossRefGoogle Scholar
  32. 32.
    Stewart, P.: Diffusion in biofilms. J. Bacteriol. 185(5), 1485–1491 (2003)CrossRefGoogle Scholar
  33. 33.
    Canfield, D.E., Jørgensen, B.B., Fossing, H., Glud, R., Gundersen, J., Ramsing, N.B., Thamdrup, B., Hansen, J.W., Nielsen, L.P., Hall, P.O.: Pathways of organic carbon oxidation in three continental margin sediments. Mar. Geol. 113(1–2), 27–40 (1993)CrossRefGoogle Scholar
  34. 34.
    Robertson, L.A., Kuenen, J.G., Balows, A., Truper, H., Dworkin, M., Harder, W., Schleifer, K., et al.: The colorless sulfur bacteria. The prokaryotes: a handbook on the biology of bacteria: ecophysiology, isolation, identification, applications, vol. I. (Ed. 2), pp. 385–413 (1992)Google Scholar
  35. 35.
    Garcia-Pichel, F., Mechling, M., Castenholz, R.W.: Diel migrations of microorganisms within a benthic, hypersaline mat community. Appl. Environ. Microbiol. 60(5), 1500–1511 (1994)Google Scholar
  36. 36.
    Fenchel, T., Bernard, C.: Behavioural responses in oxygen gradients of ciliates from microbial mats. Eur. J. Protistol. 32(1), 55–63 (1996)CrossRefGoogle Scholar
  37. 37.
    Jørgensen, B.B., Revsbech, N.P.: Colorless sulfur bacteria, Beggiatoa spp. and Thiovulum spp., in o2 and h2s microgradients. Appl. Environ. Microbiol. 45(4), 1261–1270 (1983)Google Scholar
  38. 38.
    Rothman, D.: Earths carbon cycle: a mathematical perspective. Bull. Am. Math. Soc. 52(1), 47–64 (2015)MathSciNetCrossRefMATHGoogle Scholar
  39. 39.
    Sasakura, K., Hanaoka, K., Shibuya, N., Mikami, Y., Kimura, Y., Komatsu, T., Ueno, T., Terai, T., Kimura, H., Nagano, T.: Development of a highly selective fluorescence probe for hydrogen sulfide. J. Am. Chem. Soc. 133(45), 18003–18005 (2011)CrossRefGoogle Scholar
  40. 40.
    Revsbech, N., Jørgensen, B.: Microelectrodes: their use in microbial ecology. In: Advances in Microbial Ecology, pp. 293–352. Springer, Berlin (1986)Google Scholar
  41. 41.
    Boschker, H., Middelburg, J.: Stable isotopes and biomarkers in microbial ecology. FEMS Microbiol. Ecol. 40(2), 85–95 (2002)CrossRefGoogle Scholar
  42. 42.
    Kunin, V., et al.: Millimeter-scale genetic gradients and community-level molecular convergence in a hypersaline microbial mat. Mol. Syst. Biol. 4(1), 198–204 (2008)Google Scholar
  43. 43.
    Knoll, A.H.: Life on a Young Planet: The First Three Billion Years of Evolution on Earth. Princeton University Press, Princeton (2015)CrossRefGoogle Scholar
  44. 44.
    Kump, L.R.: The rise of atmospheric oxygen. Nature 451(7176), 277–278 (2008)ADSCrossRefGoogle Scholar
  45. 45.
    Davidson, E.A., Janssens, I.A.: Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440(7081), 165–173 (2006)ADSCrossRefGoogle Scholar
  46. 46.
    Fenchel, T.: Microbial behavior in a heterogeneous world. Science 296(5570), 1068–1071 (2002)ADSCrossRefGoogle Scholar
  47. 47.
    Stocker, R., Seymour, J.R., Samadani, A., Hunt, D.E., Polz, M.F.: Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches. Proc. Natl. Acad. Sci. 105(11), 4209–4214 (2008)ADSCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Alexander P. Petroff
    • 1
  • Frank Tejera
    • 1
  • Albert Libchaber
    • 1
  1. 1.Rockefeller UniversityNew YorkUSA

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