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Bacterial growth in multicellular aggregates leads to the emergence of complex lifecycles

Schwartzman, Julia A. and Ebrahimi, Ali and Chadwick, Grayson and Sato, Yuya and Orphan, Victoria and Cordero, Otto X. (2021) Bacterial growth in multicellular aggregates leads to the emergence of complex lifecycles. . (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20211103-160314501

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Abstract

In response to environmental stresses such as starvation, many bacteria facultatively aggregate into multicellular structures that can attain new metabolic functions and behaviors. Despite the ubiquity and relevance of this form of collective behavior, we lack an understanding of how the spatiotemporal dynamics of aggregate development emerge from cellular physiology. Here, we show that the coupling between growth and spatial gradient formation leads to the emergence of a complex lifecycle, akin to those known for multicellular bacteria. Under otherwise carbon-limited growth conditions, the marine bacterium Vibrio splendidus 12B01 forms multicellular groups to collectively harvest carbon from the brown-algal polysaccharide alginate. This is achieved during growth on dissolved alginate polymer through formation of spherical, clonal clusters of cells that grow up to 40 μm in radius. Clusters develop striking spatial patterning as they grow due to phenotypic differentiation of sub-populations into a 'shell' of static cells surrounding a motile 'core'. Combining in situ measurements of cell physiology with transcriptomics, we show that shell cells express adhesive type IV pili, while motile core cells express carbon storage granules. The emergence of shell and core phenotypes is cued by opposing gradients of carbon and nitrogen that form within cell clusters due to local metabolic activity. Eventually, the shell ruptures, releasing the carbon-storing core, and we show that carbon-storing cells more readily propagate on alginate than non-carbon storing cells. We propose that phenotypic differentiation promotes the resilience of 12B01 groups by enabling clonal groups to grow larger and propagate more effectively. Phenotypic differentiation may be a widespread, but overlooked, strategy among bacteria to enhance resilience in the context of resource limitation.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/2021.11.01.466752DOIDiscussion Paper
https://github.com/jaschwartzman/12B01.gitRelated ItemCode
ORCID:
AuthorORCID
Schwartzman, Julia A.0000-0003-4563-4835
Chadwick, Grayson0000-0003-0700-9350
Orphan, Victoria0000-0002-5374-6178
Cordero, Otto X.0000-0002-2695-270X
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license. This version posted November 1, 2021. We thank the Polz lab for kindly providing Vibrio splendidus 12B01. Glen D’Souza, Jan Hendrick Hehemann and Andreas Sichert provided critical advice about working with alginate. Steven Biller, Allison Coe, and members of the Chisholm lab for advice regarding RNA extraction and RNASeq data analysis. Yunbin Guan for assistance with nanoSIMS operations. We thank Terrence Hwa, Kapil Amernath, Ghita Ghessous and members of the Hwa lab, Martin Ackermann, and Ben Roller for their advice and discussions. A.E. acknowledges funding from Swiss National Science Foundation: Grants P2EZP2 175128 and P400PB_186751. Y.S. was funded through the Japan Society for the Promotion of Science KAKENHI (Grant Number 20H02291). This work was supported by Simons Foundation: Principles of Microbial Ecosystems (PriME) award number 542395. O.X.C and J.S acknowledge support from the Kavli Institute of Theoretical Physics National Science Foundation Grant No. NSF PHY-1748958, NIH Grant No. R25GM067110, the Gordon and Betty Moore Foundation Grant No. 2919.02, National Science Foundation under Grant No. NSF PHY-1748958. Author Contributions: J.S., A.E, and O.X. designed the study, with help from V.O. and G.C, about the design of stable isotope experiments. J.S, A.E., Y.S. and G.C. performed experiments. All authors contributed to data analysis and writing the paper. The authors declare no competing interests.
Funders:
Funding AgencyGrant Number
Swiss National Science Foundation (SNSF)P2EZP2_175128
Swiss National Science Foundation (SNSF)P400PB_186751
Japan Society for the Promotion of Science (JSPS)20H02291
Simons Foundation542395
Kavli Institute for Theoretical PhysicsUNSPECIFIED
NSFPHY-1748958
NIHR25GM067110
Gordon and Betty Moore Foundation2919.02
DOI:10.1101/2021.11.01.466752
Record Number:CaltechAUTHORS:20211103-160314501
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20211103-160314501
Official Citation:Bacterial growth in multicellular aggregates leads to the emergence of complex lifecycles. Julia A Schwartzman, Ali Ebrahimi, Grayson Chadwick, Yuya Sato, Victoria Orphan, Otto X Cordero. bioRxiv 2021.11.01.466752; doi: https://doi.org/10.1101/2021.11.01.466752
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:111725
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:03 Nov 2021 18:11
Last Modified:03 Nov 2021 18:11

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