Scale-dependent tipping points of bacterial colonization resistance

Karita, Yuya; Limmer, David T.; Hallatschek, Oskar

doi:10.1073/pnas.2115496119

Title: Scale-dependent tipping points of bacterial colonization resistance

Journal Article · 09 February 2022 · Proceedings of the National Academy of Sciences of the United States of America

DOI: https://doi.org/10.1073/pnas.2115496119 · OSTI ID:1897633

^[1];

^[2];

^[1]

Univ. of California, Berkeley, CA (United States)
Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

The commonly observed stability of natural microbiomes is important for their function, yet the ubiquity of microbiome stability remains enigmatic. The strongest form of stability, colonization resistance, protects residents against invaders and is often associated with specific porous structures, such as skin follicles or intestinal crypts. By systematically probing the colonization of fly gut–derived bacteria in microfluidic pores of varying sizes, we revealed that colonization patterns and invasion rates strongly depend on the pore size. Mathematical modeling shows that bacteria spontaneously tend to organize into a dense colonization-resistant state in pores exceeding a critical size. The scale dependence of stability and resilience could bias ecological filtering in microbiomes and should be considered in the design of microbial ecology experiments.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1897633

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 7 Vol. 119; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

References (41)

Data from: Generic indicators for loss of resilience before a tipping point leading to population collapse Dai, Lei; Vorselen, Daan; Korolev, Kirill S. Dryad https://doi.org/10.5061/dryad.p2481134	dataset	January 2012
Fabrication of microfluidic systems in poly(dimethylsiloxane) McDonald, J. Cooper; Duffy, David C.; Anderson, Janelle R. Electrophoresis, Vol. 21, Issue 1 https://doi.org/10.1002/(SICI)1522-2683(20000101)21:1<27::AID-ELPS27>3.0.CO;2-C	journal	January 2000
A universal law of the characteristic return time near thresholds Wissel, C. Oecologia, Vol. 65, Issue 1 https://doi.org/10.1007/BF00384470	journal	December 1984
Quantitative and qualitative microscale distribution of bacteria in soil Ranjard, Lionel; Richaume, Agnès Research in Microbiology, Vol. 152, Issue 8 https://doi.org/10.1016/S0923-2508(01)01251-7	journal	October 2001
Microbial diversity and function in soil: from genes to ecosystems Torsvik, Vigdis; Øvreås, Lise Current Opinion in Microbiology, Vol. 5, Issue 3, p. 240-245 https://doi.org/10.1016/S1369-5274(02)00324-7	journal	June 2002
Physical constraints affecting bacterial habitats and activity in unsaturated porous media – a review Or, D.; Smets, B. F.; Wraith, J. M. Advances in Water Resources, Vol. 30, Issue 6-7 https://doi.org/10.1016/j.advwatres.2006.05.025	journal	June 2007
Temporal Stability of the Human Skin Microbiome Oh, Julia; Byrd, Allyson L.; Park, Morgan Cell, Vol. 165, Issue 4 https://doi.org/10.1016/j.cell.2016.04.008	journal	May 2016
Microbes Promote Amino Acid Harvest to Rescue Undernutrition in Drosophila Yamada, Ryuichi; Deshpande, Sonali A.; Bruce, Kimberley D. Cell Reports, Vol. 10, Issue 6 https://doi.org/10.1016/j.celrep.2015.01.018	journal	February 2015
The Gut Microbiome: Connecting Spatial Organization to Function Tropini, Carolina; Earle, Kristen A.; Huang, Kerwyn Casey Cell Host & Microbe, Vol. 21, Issue 4 https://doi.org/10.1016/j.chom.2017.03.010	journal	April 2017
Anatomy promotes neutral coexistence of strains in the human skin microbiome Conwill, Arolyn; Kuan, Anne C.; Damerla, Ravalika Cell Host & Microbe, Vol. 30, Issue 2 https://doi.org/10.1016/j.chom.2021.12.007	journal	February 2022
Robust Growth of Escherichia coli Wang, Ping; Robert, Lydia; Pelletier, James Current Biology, Vol. 20, Issue 12 https://doi.org/10.1016/j.cub.2010.04.045	journal	June 2010
Probabilistic Invasion Underlies Natural Gut Microbiome Stability Obadia, Benjamin; Güvener, Z. T.; Zhang, Vivian Current Biology, Vol. 27, Issue 13 https://doi.org/10.1016/j.cub.2017.05.034	journal	July 2017
Spatial scales of soil bacterial diversity â€“ the size of a clone Grundmann, GeneviÃ¨ve L. FEMS Microbiology Ecology, Vol. 48, Issue 2 https://doi.org/10.1016/j.femsec.2004.01.010	journal	May 2004
Control of bacterial colonization in the glands and crypts Yang, Christina; Ottemann, Karen M. Current Opinion in Microbiology, Vol. 47 https://doi.org/10.1016/j.mib.2018.11.004	journal	February 2019
Spatial, Temporal, and Phylogenetic Scales of Microbial Ecology Ladau, Joshua; Eloe-Fadrosh, Emiley A. Trends in Microbiology, Vol. 27, Issue 8 https://doi.org/10.1016/j.tim.2019.03.003	journal	August 2019
TrackMate: An open and extensible platform for single-particle tracking Tinevez, Jean-Yves; Perry, Nick; Schindelin, Johannes Methods, Vol. 115 https://doi.org/10.1016/j.ymeth.2016.09.016	journal	February 2017
Smoothing and Differentiation of Data by Simplified Least Squares Procedures. Savitzky, Abraham.; Golay, M. J. E. Analytical Chemistry, Vol. 36, Issue 8 https://doi.org/10.1021/ac60214a047	journal	July 1964
Diversity, stability and resilience of the human gut microbiota Lozupone, Catherine A.; Stombaugh, Jesse I.; Gordon, Jeffrey I. Nature, Vol. 489, Issue 7415 https://doi.org/10.1038/nature11550	journal	September 2012
Bacterial colonization factors control specificity and stability of the gut microbiota Lee, S. Melanie; Donaldson, Gregory P.; Mikulski, Zbigniew Nature, Vol. 501, Issue 7467 https://doi.org/10.1038/nature12447	journal	August 2013
Regional specialization within the intestinal immune system Mowat, Allan M.; Agace, William W. Nature Reviews Immunology, Vol. 14, Issue 10 https://doi.org/10.1038/nri3738	journal	September 2014
Gut biogeography of the bacterial microbiota Donaldson, Gregory P.; Lee, S. Melanie; Mazmanian, Sarkis K. Nature Reviews Microbiology, Vol. 14, Issue 1 https://doi.org/10.1038/nrmicro3552	journal	October 2015
Self-induced mechanical stress can trigger biofilm formation in uropathogenic Escherichia coli Chu, Eric K.; Kilic, Onur; Cho, Hojung Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-06552-z	journal	October 2018
Ecosystem tipping points in an evolving world Dakos, Vasilis; Matthews, Blake; Hendry, Andrew P. Nature Ecology & Evolution, Vol. 3, Issue 3 https://doi.org/10.1038/s41559-019-0797-2	journal	February 2019
Arrested phase separation in reproducing bacteria creates a generic route to pattern formation Cates, M. E.; Marenduzzo, D.; Pagonabarraga, I. Proceedings of the National Academy of Sciences, Vol. 107, Issue 26 https://doi.org/10.1073/pnas.1001994107	journal	May 2010
Microbial competition in porous environments can select against rapid biofilm growth Coyte, Katharine Z.; Tabuteau, Hervé; Gaffney, Eamonn A. Proceedings of the National Academy of Sciences, Vol. 114, Issue 2 https://doi.org/10.1073/pnas.1525228113	journal	December 2016
Slow Recovery from Perturbations as a Generic Indicator of a Nearby Catastrophic Shift van Nes, Egbert H.; Scheffer, Marten The American Naturalist, Vol. 169, Issue 6 https://doi.org/10.1086/516845	journal	June 2007
Development of improved versatile broad-host-range vectors for use in methylotrophs and other Gram-negative bacteria Lidstrom, Mary E.; Marx, Christopher J. Microbiology, Vol. 147, Issue 8 https://doi.org/10.1099/00221287-147-8-2065	journal	August 2001
Hydrodynamics of soft active matter Marchetti, M. C.; Joanny, J. F.; Ramaswamy, S. Reviews of Modern Physics, Vol. 85, Issue 3 https://doi.org/10.1103/RevModPhys.85.1143	journal	July 2013
Illuminating the intrinsic and extrinsic drivers of ecological stability across scales Ross, Samuel R. P. ‐J.; Suzuki, Yuka; Kondoh, Michio Ecological Research, Vol. 36, Issue 3 https://doi.org/10.1111/1440-1703.12214	journal	February 2021
Intestinal colonization resistance Lawley, Trevor D.; Walker, Alan W. Immunology, Vol. 138, Issue 1 https://doi.org/10.1111/j.1365-2567.2012.03616.x	journal	December 2012
Insights into the resistance and resilience of the soil microbial community Griffiths, Bryan S.; Philippot, Laurent FEMS Microbiology Reviews, Vol. 37, Issue 2 https://doi.org/10.1111/j.1574-6976.2012.00343.x	journal	March 2013
Generic Indicators for Loss of Resilience Before a Tipping Point Leading to Population Collapse Dai, L.; Vorselen, D.; Korolev, K. S. Science, Vol. 336, Issue 6085 https://doi.org/10.1126/science.1219805	journal	May 2012
The ecology of the microbiome: Networks, competition, and stability Coyte, K. Z.; Schluter, J.; Foster, K. R. Science, Vol. 350, Issue 6261 https://doi.org/10.1126/science.aad2602	journal	November 2015
A Crypt-Specific Core Microbiota Resides in the Mouse Colon Pédron, Thierry; Mulet, Céline; Dauga, Catherine mBio, Vol. 3, Issue 3 https://doi.org/10.1128/mBio.00116-12	journal	July 2012
Crypt- and Mucosa-Associated Core Microbiotas in Humans and Their Alteration in Colon Cancer Patients Saffarian, Azadeh; Mulet, Céline; Regnault, Béatrice mBio, Vol. 10, Issue 4 https://doi.org/10.1128/mBio.01315-19	journal	July 2019
Motility-Induced Phase Separation Cates, Michael E.; Tailleur, Julien Annual Review of Condensed Matter Physics, Vol. 6, Issue 1 https://doi.org/10.1146/annurev-conmatphys-031214-014710	journal	March 2015
The Mechanics and Statistics of Active Matter Ramaswamy, Sriram Annual Review of Condensed Matter Physics, Vol. 1, Issue 1 https://doi.org/10.1146/annurev-conmatphys-070909-104101	journal	August 2010
Memory and Fitness Optimization of Bacteria under Fluctuating Environments Lambert, Guillaume; Kussell, Edo PLoS Genetics, Vol. 10, Issue 9 https://doi.org/10.1371/journal.pgen.1004556	journal	September 2014
The Problem of Pattern and Scale in Ecology: The Robert H. MacArthur Award Lecture Levin, Simon A. Ecology, Vol. 73, Issue 6 https://doi.org/10.2307/1941447	journal	December 1992
Spatial Scaling in Ecology Wiens, J. A. Functional Ecology, Vol. 3, Issue 4 https://doi.org/10.2307/2389612	journal	January 1989
Experimental evaluation of the importance of colonization history in early-life gut microbiota assembly Martínez, Inés; Maldonado-Gomez, Maria X.; Gomes-Neto, João Carlos eLife, Vol. 7 https://doi.org/10.7554/eLife.36521	journal	September 2018

Similar Records

A symbiotic physical niche in Drosophila melanogaster regulates stable association of a multi-species gut microbiota

Journal Article · 2023 · Nature Communications · OSTI ID:2229065

Dodge, Ren; Jones, Eric W.; Zhu, Haolong; +13 more

Hospitalized Premature Infants Are Colonized by Related Bacterial Strains with Distinct Proteomic Profiles

Journal Article · 2018 · mBio (Online) · OSTI ID:1474619

Brown, Christopher T.; Xiong, Weili; Olm, Matthew R.; +6 more

Identical bacterial populations colonize premature infant gut, skin, and oral microbiomes and exhibit different in situ growth rates

Journal Article · 2017 · Genome Research · OSTI ID:1625635

Olm, Matthew R.; Brown, Christopher T.; Brooks, Brandon; +7 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
active matter
colonization resistance
microbiome stability
microfluidics
phase separation

Title: Scale-dependent tipping points of bacterial colonization resistance

Citation Formats

References (41)

Similar Records

Related Subjects