Menu

Close

Spatial Self-Organization Resolves Conflicts Between Individuality and Collective Migration

Xiongfei Fu, Setsu Kato, Junjiajia Long, Henry H. Mattingly, Caiyun He, Dervis Can Vural, Steven W. Zucker, Thierry Emonet

Preprint posted on April 05, 2018 https://www.biorxiv.org/content/early/2018/04/05/295196.full

Keeping the runners and tumblers together: Spontaneous spatial organization allows for the collective migration of phenotypically diverse groups

Selected by Amanda Haage

Categories: cell biology, microbiology

Why This Is Cool – Populations of E. coli cells can migrate collectively up chemoattractant gradients and they do so with a biased random walk produced by straight “runs” and random “tumbles.” It has also been previously established that E. coli that are genetically identical present with variable swimming phenotypes i.e. some cells run more and some cells tumble more than others. What Fu et al. set out to answer was how do these groups of cells travel together despite their individual differences in chemotactic ability? To answer this, they had to observe both collective and individual behaviors, so they used the smartly designed microfluidic device pictured below. The narrow channel allowed E. coli cells to migrate in bands up a gradient, towards an open chamber where cells could disperse and individual behavior could be tracked. Using this set-up, they were able to establish that although there is some selection for less tumbling in collectively migrating bands, phenotypic diversity is definitely still present. They then expanded a classic mathematical model1 for collective chemotaxis to account for individual diversities. This expanded model allowed them to predict how different swimming phenotypes could still travel together. Spatial sorting of cells, so that high tumbling coincides with a steeper gradient, allows the group to compensate for diversity. So the less efficient, more tumbley cells get sorted to the back of the group where the gradient is steeper, because the front runner cells, which perform better with small changes in gradient, metabolize a certain amount of the attractant, leaving a steeper gradient behind them. The steeper gradient keeps the tumblers more focused and they are able to keep up to a certain cut-off point. Fu et al. were then able to confirm these predictions experimentally with mixed levels of expression of the chemotaxis regulating phosphatase CheZ. In addition, they identified a possible role for oxygen availability in controlling this spatial sorting. E. coli need oxygen to metabolize these chemoattractants, but oxygen becomes less available with more cells, such as the conditions of the middle of the band (Figure 1). More oxygen is available at the back due to lower cell density, which increases metabolism, thus increasing the local gradient steepness even more and possibly allowing even the worst tumblers to keep up.

Figure 1. Collective migration of a phenotypically diverse clonal population. A) When concentrated at the bottom of a nutrient channel, motile E. coli cells emerge from the high cell density region and travel in bands along the channel by following gradients produced by their own attractant consumption. B) Microfluidic device used to quantify the band migration. Control gates along the channel (black vertical lines) are initially open (top), and later closed to capture different bands of cells in the observation chamber (bottom), where single cells are tracked to quantify the distribution of phenotypes within the band.

 

Why I Selected It – I was looking for preprints on the collective migration of eukaryotic cells when I “tumbled” across this work from Fu et al., but I am so glad I stuck with it. I didn’t know bacteria even underwent collective migrations. This work uses an excellent and high-throughput model system for studying phenotypic diversity and I think their results are widely applicable, as they state – “For example in migrating neural crest cells and in fish shoals, many organisms may follow a few more informed individuals2.” Reading this preprint made me question the phenotypic diversity I see in my own research, a phenomenon not often addressed in eukaryotic cell biology.

Open Questions –

  • Would you expect the spatial sorting of cells to be any different based on the type of chemotactic cue? Are there any non-consumable cues that could be tested, presumably to see a disruption in this process?
  • Do you think this spatial sorting is an active process? If you reversed the direction of the gradient mid-migration, would the organization of the band change?
  • If you continually removed a certain phenotype, say removed all the cells that fell off the band over multiple cycles of migration, would you eventually get a homogenous band with no spatial sorting? Would this impede or improve collective migration?

Related References –

  1. Classic model of collective bacteria cell chemotaxis
    1. Keller EF, Segel LA. Traveling bands of chemotactic bacteria: a theoretical analysis. J Theor Biol 30, 235-248 (1971).
  2. Collective cell migration review
    1. Mayor R, Etienne-Manneville S. The front and rear of collective cell migration. Nat Rev Mol Cell Biol 17, 97-109 (2016).
  3. Similar mechanisms operating in eukaryotic collective cell migration
    1. Tweedy L, Knecht DA, Mackay GM, Insall RH. Self-Generated Chemoattractant Gradients: Attractant Depletion Extends the Range and Robustness of Chemotaxis. PLoS Biol 14, e1002404 (2016).

Tags: mathematical model, migration

Posted on: 24th April 2018

Read preprint (No Ratings Yet)




  • Author's response

    Thierry Emonet shared

    1. We expect spatial sorting to be a generic outcome when cells of different gradient-climbing abilities climb the same gradient, whether it be a gradient of consumable chemoattractant, non-consumable chemoattractant, oxygen, temperature, etc. However, spatial sorting in an attractant gradient created by consumption is special in that the fastest cells can’t run far ahead of the slower ones because they need those cells to help create the gradient; without them, there is no gradient to climb.
    2. We think this spatial sorting is active in the sense that if the gradient reversed direction (not too fast), then the direction of sorting would reverse, as well. Any fast gradient climbers located at the bottom of the new gradient would quickly catch up with and pass the slow gradient climbers ahead of them, leading to reorientation of the sorting. However, although this is an active process, it is not hard-coded in the cells; spatial sorting emerges from the differences in individual gradient-climbing capabilities.
    3. Eliminating phenotypic diversity would be very difficult because every time a cell divides it will give rise to daughter cells that are not entirely identical. If under special circumstances we managed to form a band composed of a narrow distribution of phenotypes that is nearly homogeneous, we would expect cell diffusion to smear out spatial sorting, making the band effectively well-mixed. To what extend this band might perform better than a more diverse one is unclear and  a question we are actively investigating.

     

    Have your say

    Your email address will not be published. Required fields are marked *

    This site uses Akismet to reduce spam. Learn how your comment data is processed.

    Sign up to customise the site to your preferences and to receive alerts

    Register here

    Also in the cell biology category:

    Super-resolution Molecular Map of Basal Foot Reveals Novel Cilium in Airway Multiciliated Cells

    Quynh Nguyen, Zhen Liu, Rashmi Nanjundappa, et al.



    Selected by Robert Mahen

    Single cell RNA-Seq reveals distinct stem cell populations that drive sensory hair cell regeneration in response to loss of Fgf and Notch signaling

    Mark E. Lush, Daniel C. Diaz, Nina Koenecke, et al.

    AND

    Distinct progenitor populations mediate regeneration in the zebrafish lateral line.

    Eric D Thomas, David Raible



    Selected by Rudra Nayan Das

    1

    Actomyosin-II facilitates long-range retrograde transport of large cargoes by controlling axonal radial contractility

    Tong Wang, Wei Li, Sally Martin, et al.



    Selected by Ivana Viktorinová

    Atlas of Subcellular RNA Localization Revealed by APEX-seq

    Furqan M Fazal, Shuo Han, Pornchai Kaewsapsak, et al.

    AND

    Proximity RNA labeling by APEX-Seq Reveals the Organization of Translation Initiation Complexes and Repressive RNA Granules

    Alejandro Padron, Shintaro Iwasaki, Nicholas Ingolia



    Selected by Christian Bates

    Applications, Promises, and Pitfalls of Deep Learning for Fluorescence Image Reconstruction

    Chinmay Belthangady , Loic A. Royer



    Selected by Romain F. Laine

    Stable knockout and complementation of receptor expression using in vitro cell line derived reticulocytes for dissection of host malaria invasion requirements

    Timothy J Satchwell, Katherine E Wright, Katy L Haydn-Smith, et al.



    Selected by Alyson Smith

    Maintenance of spatial gene expression by Polycomb-mediated repression after formation of a vertebrate body plan

    Julien Rougot, Naomi D Chrispijn, Marco Aben, et al.



    Selected by Yen-Chung Chen

    1

    Activation of intracellular transport by relieving KIF1C autoinhibition

    Nida Siddiqui, Alice Bachmann, Alexander J Zwetsloot, et al.



    Selected by Ben Craske, Thibault Legal and Toni McHugh

    1

    A non-canonical arm of UPRER mediates longevity through ER remodeling and lipophagy.

    Joseph R Daniele, Ryo Higuchi-Sanabria, Vidhya Ramachandran, et al.



    Selected by Sandra Franco Iborra

    1

    Basal extrusion drives cell invasion and mechanical stripping of E-cadherin

    John Fadul, Gloria M Slattum, Nadja M Redd, et al.



    Selected by William Hill

    Ribosomal DNA and the rDNA-binding protein Indra mediate non-random sister chromatid segregation in Drosophila male germline stem cells

    George Watase, Yukiko Yamashita



    Selected by Maiko Kitaoka

    An F-actin shell ruptures the nuclear envelope by sorting pore-dense and pore-free membranes in meiosis of starfish oocytes

    Natalia Wesolowska, Pedro Machado, Celina Geiss, et al.



    Selected by Maiko Kitaoka

    1

    Multi-color single molecule imaging uncovers extensive heterogeneity in mRNA decoding

    Sanne Boersma, Deepak Khuperkar, Bram M.P. Verhagen, et al.



    Selected by Lorenzo Lafranchi

    Multi-color single molecule imaging uncovers extensive heterogeneity in mRNA decoding

    Sanne Boersma, Deepak Khuperkar, Bram M.P. Verhagen, et al.

    AND

    Live-cell single RNA imaging reveals bursts of translational frameshifting

    Kenneth R Lyon Jr, Luis U Aguilera, Tatsuya Morisaki, et al.



    Selected by Nicola Stevenson

    A non-canonical arm of UPRER mediates longevity through ER remodeling and lipophagy.

    Joseph R Daniele, Ryo Higuchi-Sanabria, Vidhya Ramachandran, et al.



    Selected by Sandra Malmgren Hill

    Microtubules Gate Tau Condensation to Spatially Regulate Microtubule Functions

    Ruensern Tan, Aileen J. Lam, Tracy Tan, et al.

    AND

    Kinetically distinct phases of tau on microtubules regulate kinesin motors and severing enzymes

    Valerie Siahaan, Jochen Krattenmacher, Amayra Hernandez-Vega, et al.



    Selected by Satish Bodakuntla

    2

    Also in the microbiology category:

    Applications, Promises, and Pitfalls of Deep Learning for Fluorescence Image Reconstruction

    Chinmay Belthangady , Loic A. Royer



    Selected by Romain F. Laine

    Disrupting Transcriptional Feedback Yields an Escape-Resistant Antiviral

    Sonali Chaturvedi, Marie Wolf, Noam Vardi, et al.



    Selected by Pavithran Ravindran

    1

    Development and validation of serological markers for detecting recent exposure to Plasmodium vivax infection

    Rhea Jessica Longley, Michael T White, Eizo Takashima, et al.

    AND

    Antimalarial drug mefloquine kills both trophozoite and cyst stages of Entamoeba

    Conall Sauvey, Gretchen Ehrenkaufer, Anjan Debnath, et al.



    Selected by Zhang-He Goh

    Structure of a cytochrome-based bacterial nanowire

    David J Filman, Stephen F Marino, Joy E Ward, et al.



    Selected by Amberley Stephens

    Biofilm/Persister/Stationary Phase Bacteria Cause More Severe Disease Than Log Phase Bacteria II Infection with Persister Forms of Staphylococcus aureus Causes a Chronic Persistent Skin Infection with More Severe Lesion that Takes Longer to Heal and is not Eradicated by the Current Recommended Treatment in Mice

    Rebecca Yee, Yuting Yuan, Cory Brayton, et al.



    Selected by Snehal Kadam

    Acquired interbacterial defense systems protect against interspecies antagonism in the human gut microbiome

    Benjamin D. Ross, Adrian J. Verster, Matthew C. Radey, et al.



    Selected by Connor Rosen

    The Toll pathway inhibits tissue growth and regulates cell fitness in an infection-dependent manner

    Federico Germani, Daniel Hain, Denise Sternlicht, et al.



    Selected by Rohan Khadilkar

    The microbial basis of impaired wound healing: differential roles for pathogens, "bystanders", and strain-level diversification in clinical outcomes

    Lindsay Kalan, Jacquelyn S Meisel, Michael A Loesche, et al.



    Selected by Snehal Kadam

    CRISPR/Cas9-mediated gene deletion of the ompA gene in an Enterobacter gut symbiont impairs biofilm formation and reduces gut colonization of Aedes aegypti mosquitoes

    Shivanand Hegde, Pornjarim Nilyanimit, Elena Kozlova, et al.



    Selected by Snehal Kadam

    Agrobacterium tumefaciens divisome proteins regulate the transition from polar growth to cell division

    Matthew L Howell, Alena Aliashkevich, Kousik Sundararajan, et al.



    Selected by Hannah Behrens

    Water quality and microbial load: a double-threshold identification procedure intended for space applications

    Stefano Amalfitano, Caterina Levantesi, Laurent Garrelly, et al.



    Selected by Daphne Ng

    1

    Entomophthovirus: An insect-derived iflavirus that infects a behavior manipulating fungal pathogen of dipterans

    Maxwell C Coyle, Carolyn N Elya, Michael J Bronski, et al.



    Selected by Hiral Shah

    Soil microbial habitats in an extreme desert Mars-analogue environment

    Kimberley Warren-Rhodes, Kevin Lee, Stephen Archer, et al.



    Selected by Daphne Ng

    Ecological analyses of mycobacteria in showerhead biofilms and their relevance to human health

    Matthew Gebert, Manuel Delgado-Baquerizo, Angela Oliverio, et al.



    Selected by Hannah Behrens

    EFFECTORS OF THE SPINDLE ASSEMBLY CHECKPOINT BUT NOT THE MITOTIC EXIT NETWORK ARE CONFINED WITHIN THE NUCLEUS OF SACCHAROMYCES CEREVISIAE

    Lydia R Heasley, Jennifer G DeLuca, Steven M Markus



    Selected by Hiral Shah

    Peculiar features of the plastids of the colourless alga Euglena longa and photosynthetic euglenophytes unveiled by transcriptome analyses

    Kristina Zahonova, Zoltan Fussy, Erik Bircak, et al.



    Selected by Ellis O'Neill

    1

    Close