Biophysical basis for convergent evolution of two veil-forming microbes

Abstract

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.

Transition to bound states for bacteria swimming near surfaces

“…Scanning electron microscope image of a Thiovulum majus bacterium with a slightly shrunken spherical cell body of radius a ∼ 4 µm and flagella L ∼ 2 µm long, reproduced with permission from Ref. [9] (see similar pictures in Ref. [10]).…”

Nucleation of rotating crystals byThiovulum majusbacteria

“…Thiovulum majus [1][2][3] is one of the fastest-swimming bacteria in the world, reaching speeds of up to m 600 m s −1 [4,5]. As such, the physical basis of its motion, both individually [6][7][8][9][10][11] and collectively [12][13][14][15][16][17][18], is of interest from both biological and physical perspectives. When these bacteria are confined between a glass slide and cover slip, cells localize on the glass surfaces and self organize into active crystals composed of rotating cells ( figure 1(a)), which spin and reorganize [19].…”

Candidatus Thiovulum sp. strain imperiosus: the largest free-living Epsilonproteobacteraeota Thiovulum strain lives in a marine mangrove environment

“…Ex situ measurements done in aquaria with immersed bones brought back to the laboratory 4-5 days after deployment, showed that the introduction of electrodes has not disturbed the veil structure developed around the bones. This may be due to the organization of Thiovulum communities in the bacterial veil covering the surfaces of marine sulfide deposits, in which cells are either free-swimming cells D r a f t p. 18 or cells attached to the bone surface or to neighboring cells include in a matrix constituted by a 10-100 μm long mucous stalks (Wirsen and Jannasch 1978;Fenchel 1994;Schaudinn et al 2007;Petroff et al 2015). During the experiments presented here, the water column was normally oxygenated but oxygen decreases quickly to reach zero inside the veil.…”