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Biophysical basis for convergent evolution of two veil-forming microbes

Petroff, Alexander P. and Pasulka, Alexis L. and Soplop, Nadine and Wu, Xiao-Lun and Libchaber, Albert (2015) Biophysical basis for convergent evolution of two veil-forming microbes. Royal Society Open Science, 2 (11). Art. No. 150437. ISSN 2054-5703.

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Microbes living in stagnant water typically rely on chemical diffusion to draw nutrients from their environment. The sulfur-oxidizing bacterium Thiovulum majus and the ciliate Uronemella have independently evolved the ability to form a ‘veil’, a centimetre-scale mucous sheet on which cells organize to produce a macroscopic flow. This flow pulls nutrients through the community an order of magnitude faster than diffusion. To understand how natural selection led these microbes to evolve this collective behaviour, we connect the physical limitations acting on individual cells to the cell traits. We show how diffusion limitation and viscous dissipation have led individual T. majus and Uronemella cells to display two similar characteristics. Both of these cells exert a force of approximately 40 pN on the water and attach to boundaries by means of a mucous stalk. We show how the diffusion coefficient of oxygen in water and the viscosity of water define the force the cells must exert. We then show how the hydrodynamics of filter-feeding orient a microbe normal to the surface to which it attaches. Finally, we combine these results with new observations of veil formation and a review of veil dynamics to compare the collective dynamics of these microbes. We conclude that this convergent evolution is a reflection of similar physical limitations imposed by diffusion and viscosity acting on individual cells.

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Additional Information:© 2015 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License, which permits unrestricted use, provided the original author and source are credited. Received: 27 August 2015; Accepted: 16 October 2015; Published 11 November 2015. Data accessibility. The 18S rRNA sequence of Uronemella was deposited in Genbank (accession number KT266872). The data for each figure are provided in the electronic supplementary material. Authors’ contributions. A.P.P. collected the organisms, designed and conducted the experiments, and wrote the manuscript with input from all authors. A.L.P. identified the ciliate. N.S. provided electron micrographs. X.L.W. provided microscope images and assisted in the analysis. A.L. helped design the experiments and provided input for the paper. Competing interests. We declare we have no competing interests. Funding. This work was supported by the Raymond and Beverly Sackler Foundation. Acknowledgements. We thank Kunihiro Uryu for his contribution to the electron microscopy. A.P.P. thanks J. Hudspeth, M. Muller, T. Bosak, O. Devauchelle, C. Modes, A. Hočevar and M. Magnasco for their comments.
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Raymond and Beverly Sackler FoundationUNSPECIFIED
Subject Keywords:convergent evolution, hydrodynamics, collective dynamics
Record Number:CaltechAUTHORS:20160104-130557365
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Official Citation:Petroff AP, Pasulka AL, Soplop N,Wu X-L, Libchaber A. 2015 Biophysical basis for convergent evolution of two veil-forming microbes. R. Soc. open sci. 2: 150437
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:63333
Deposited By: Tony Diaz
Deposited On:04 Jan 2016 23:19
Last Modified:20 Jul 2017 20:58

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