Cooperatively Generated Stresslet Flows Supply Fresh Fluid to Multicellular Choanoflagellate Colonies

Roper, Marcus; Dayel, Mark J.; Pepper, Rachel E.; Koehl, M. A. R.

doi:10.1103/physrevlett.110.228104

Cited by 85 publications

(128 citation statements)

References 18 publications

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“…2(a) is similar to feeding flow that many micro-organisms use to gather food from the fluid environment near an interface [43,44]. The same flow pattern is also used to explain the formation of bound Volvox pair [49] and to explain the attractive force between thermophoretic colloids [50][51][52].…”

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confidence: 98%

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Dynamic clustering in suspension of motile bacteria

Chen

Xiang

Yang

et al. 2015

EPL

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-Bacteria suspension exhibits a wide range of collective phenomena arsing from interactions between individual cells. Here we show Serratia marcescens cells near an air-liquid interface spontaneously aggregate into dynamic clusters through surface-mediated hydrodynamic interactions. These long-lived clusters translate randomly and rotate in the counter-clockwise direction; they continuously evolve, merge with others and split into smaller ones. Measurements indicate that long-ranged hydrodynamic interactions have strong influences on cluster properties. Bacterial clusters change material and fluid transport near the interface and hence may have environmental and biological consequences.Active systems are composed of self-propelled particles that can produce motion by taking in and dissipating energy [1][2][3][4]. Examples exist at different length scales, from bacteria suspension [5][6][7][8][9][10] to flocks of birds [11][12][13]. Being far from thermal equilibrium, active systems are not subject to thermodynamic constraints, such as detailed balance or fluctuation-dissipation theorem [14][15][16]. This renders the physics of active systems much richer than that of thermal systems. For example, collective motion with extended spatio-temporal coherence has been reported in many active systems [5-9, 11-13, 17-19]. Such coherent motion can arise from local interactions that align a particle's motion with its neighbors through biological coordination [11,12] or physical interactions [17,19].Active systems without alignment interactions also exhibit interesting collective behavior. Theoretical models have shown that systems with a density-dependent motility phase separate into dense dynamic clusters and a dilute gas phase [14,15,20]. Numerical simulations of repulsive self-propelled disks confirmed the theoretical prediction of phase separation [21,22]. Effects of motility, attractive interaction, and hydrodynamic forces have been extensively explored in simulations [23][24][25][26]. On the experimental side, dynamic clusters have been observed in Janus particles (platinum-coated [27] and Carbon-coated In this letter, we report experimental results for a new type of bacterial clusters formed near an air-liquid interface in a pure suspension without depletant agents. Fluid dynamic calculation and flow visualization are used to show surface-mediated hydrodynamic interactions can explain the formation of these clusters. We further quantify the statistical and dynamic properties of bacterial clusters and show long-ranged hydrodynamic forces have important influences on cluster properties. We conclude with discussions on related research and on possible technological and environmental implications of our work.Experiments -Our experiments are carried out in drops of wild-type Serratia marcescens (ATCC 274) bacteria, which are propelled by a bundle of a few rotating flagella [32]. For cultivation, small amount of bacteria from frozen stock is put in 4 ml of Luria Broth (LB) growth p-1

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confidence: 98%

“…1(e) suggests the bacteria in clusters orient their bundles perpendicular to the interface 5 . Bacteria in such a configuration can generate fluid flow that leads to cluster formation [31,43,44]. To illustrate the mechanism, we numerically compute fluid flow around a bacterial model that is oriented perpendicular to the interface.…”

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confidence: 99%

Dynamic clustering in suspension of motile bacteria

Chen

Xiang

Yang

et al. 2015

EPL

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“…The ecological relevance of the interaction between A. machipongonensis (hereafter, Algoriphagus) and S. rosetta is evidenced by the coexistence of these organisms in nature (35) and the predator-prey relationship between choanoflagellates and bacteria (25,36). Indeed, rosettes likely have a fitness advantage over single cells in some environments, as multicellular choanoflagellates are predicted to produce increased flux of water past each cell (37), and prey capture studies reveal that rosettes collect more bacterial prey/cell/unit time than do single cells (38). However, in other environments, rosette development would likely reduce fitness as rosettes have reduced motility relative to single cells.…”

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confidence: 99%

Bacterial lipids activate, synergize, and inhibit a developmental switch in choanoflagellates

Woznica

Cantley

Beemelmanns

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

122

133

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In choanoflagellates, the closest living relatives of animals, multicellular rosette development is regulated by environmental bacteria. The simplicity of this evolutionarily relevant interaction provides an opportunity to identify the molecules and regulatory logic underpinning bacterial regulation of development. We find that the rosette-inducing bacterium Algoriphagus machipongonensis produces three structurally divergent classes of bioactive lipids that, together, activate, enhance, and inhibit rosette development in the choanoflagellate Salpingoeca rosetta. One class of molecules, the lysophosphatidylethanolamines (LPEs), elicits no response on its own but synergizes with activating sulfonolipid rosette-inducing factors (RIFs) to recapitulate the full bioactivity of live Algoriphagus. LPEs, although ubiquitous in bacteria and eukaryotes, have not previously been implicated in the regulation of a host-microbe interaction. This study reveals that multiple bacterially produced lipids converge to activate, enhance, and inhibit multicellular development in a choanoflagellate.choanoflagellates | bacteria | host-microbe | sulfonolipid | multicellularity

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“…Though again, this scenario predicts that multiple heterotrophic lineages would have evolved animal-like multicellularity in response to widespread eukaryotic predation in the Neoproterozoic Era -that is, a polyphyletic origin of animal multicellularity (Figure 2A,B,C). Animal monophyly and observations showing that coloniality in choanoflagellates is instigated by prey bacteria in the complete absence of flagellate-eating predators [48] suggest that alternative or additional factors, such as enhanced prey capture [49,50], might have encouraged the evolution of animal multicellularity [18].…”

Section: Animal Origins In Context: the Tonian Earth Systemmentioning

confidence: 99%

Animal origins and the Tonian Earth system

Mills

Francis

Canfield

2018

Emerging Topics in Life Sciences

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The Neoproterozoic Era (1000-541 million years ago, Ma) was characterized by dramatic environmental and evolutionary change, including at least two episodes of extensive, low-latitude glaciation, potential changes in the redox structure of the global ocean, and the origin and diversification of animal life. How these different events related to one another remains an active area of research, particularly how these environmental changes influenced, and were influenced by, the earliest evolution of animals. Animal multicellularity is estimated to have evolved in the Tonian Period (1000-720 Ma) and represents one of at least six independent acquisitions of complex multicellularity, characterized by cellular differentiation, three-dimensional body plans, and active nutrient transport. Compared with the other instances of complex multicellularity, animals represent the only clade to have evolved from wall-less, phagotrophic flagellates, which likely placed unique cytological and trophic constraints on the evolution of animal multicellularity. Here, we compare recent molecular clock estimates with compilations of the chromium isotope, micropaleontological, and organic biomarker records, suggesting that, as of now, the origin of animals was not obviously correlated to any environmental-ecological change in the Tonian Period. This lack of correlation is consistent with the idea that the evolution of animal multicellularity was primarily dictated by internal, developmental constraints and occurred independently of the known environmental-ecological changes that characterized the Neoproterozoic Era.

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Cooperatively Generated Stresslet Flows Supply Fresh Fluid to Multicellular Choanoflagellate Colonies

Cited by 85 publications

References 18 publications

Dynamic clustering in suspension of motile bacteria

Dynamic clustering in suspension of motile bacteria

Bacterial lipids activate, synergize, and inhibit a developmental switch in choanoflagellates

Animal origins and the Tonian Earth system

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