Microbes in Porous Environments: from Active Interactions to Emergent Feedback

Overview

Journal Biophys Rev

Publisher Springer

Specialty Biophysics

Date 2024 May 13

PMID 38737203

Authors

Chenyu Jin

Anupam Sengupta

Affiliations

Soon will be listed here.

Abstract

Microbes thrive in diverse porous environments-from soil and riverbeds to human lungs and cancer tissues-spanning multiple scales and conditions. Short- to long-term fluctuations in local factors induce spatio-temporal heterogeneities, often leading to physiologically stressful settings. How microbes respond and adapt to such biophysical constraints is an active field of research where considerable insight has been gained over the last decades. With a focus on bacteria, here we review recent advances in self-organization and dispersal in inorganic and organic porous settings, highlighting the role of active interactions and feedback that mediates microbial survival and fitness. We discuss open questions and opportunities for using integrative approaches to advance our understanding of the biophysical strategies which microbes employ at various scales to make porous settings habitable.

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References

Volpe G, Volpe G . The topography of the environment alters the optimal search strategy for active particles. Proc Natl Acad Sci U S A. 2017; 114(43):11350-11355. PMC: 5664536. DOI: 10.1073/pnas.1711371114. View

Fu X, Kato S, Long J, Mattingly H, He C, Vural D . Spatial self-organization resolves conflicts between individuality and collective migration. Nat Commun. 2018; 9(1):2177. PMC: 5988668. DOI: 10.1038/s41467-018-04539-4. View

Wang Q, Suzuki A, Mariconda S, Porwollik S, Harshey R . Sensing wetness: a new role for the bacterial flagellum. EMBO J. 2005; 24(11):2034-42. PMC: 1142604. DOI: 10.1038/sj.emboj.7600668. View

Zhao K, Tseng B, Beckerman B, Jin F, Gibiansky M, Harrison J . Psl trails guide exploration and microcolony formation in Pseudomonas aeruginosa biofilms. Nature. 2013; 497(7449):388-391. PMC: 4109411. DOI: 10.1038/nature12155. View

Bertrand T, Zhao Y, Benichou O, Tailleur J, Voituriez R . Optimized Diffusion of Run-and-Tumble Particles in Crowded Environments. Phys Rev Lett. 2018; 120(19):198103. DOI: 10.1103/PhysRevLett.120.198103. View

Cremer J, Honda T, Tang Y, Wong-Ng J, Vergassola M, Hwa T . Chemotaxis as a navigation strategy to boost range expansion. Nature. 2019; 575(7784):658-663. PMC: 6883170. DOI: 10.1038/s41586-019-1733-y. View

Bar-On Y, Phillips R, Milo R . The biomass distribution on Earth. Proc Natl Acad Sci U S A. 2018; 115(25):6506-6511. PMC: 6016768. DOI: 10.1073/pnas.1711842115. View

Zeitz M, Wolff K, Stark H . Active Brownian particles moving in a random Lorentz gas. Eur Phys J E Soft Matter. 2017; 40(2):23. DOI: 10.1140/epje/i2017-11510-0. View

Bansil R, Turner B . The biology of mucus: Composition, synthesis and organization. Adv Drug Deliv Rev. 2017; 124:3-15. DOI: 10.1016/j.addr.2017.09.023. View

10.

Smith H, Zelaya A, De Leon K, Chakraborty R, Elias D, Hazen T . Impact of hydrologic boundaries on microbial planktonic and biofilm communities in shallow terrestrial subsurface environments. FEMS Microbiol Ecol. 2018; 94(12). PMC: 6192502. DOI: 10.1093/femsec/fiy191. View

11.

Geng J, Beloin C, Ghigo J, Henry N . Bacteria hold their breath upon surface contact as shown in a strain of Escherichia coli, using dispersed surfaces and flow cytometry analysis. PLoS One. 2014; 9(7):e102049. PMC: 4108326. DOI: 10.1371/journal.pone.0102049. View

12.

Yonekura K, Maki-Yonekura S, Namba K . Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature. 2003; 424(6949):643-50. DOI: 10.1038/nature01830. View

13.

Taubert M, Stockel S, Geesink P, Girnus S, Jehmlich N, von Bergen M . Tracking active groundwater microbes with D O labelling to understand their ecosystem function. Environ Microbiol. 2017; 20(1):369-384. DOI: 10.1111/1462-2920.14010. View

14.

Vallespir Lowery N, Ursell T . Structured environments fundamentally alter dynamics and stability of ecological communities. Proc Natl Acad Sci U S A. 2018; 116(2):379-388. PMC: 6329963. DOI: 10.1073/pnas.1811887116. View

15.

Licata N, Mohari B, Fuqua C, Setayeshgar S . Diffusion of Bacterial Cells in Porous Media. Biophys J. 2016; 110(1):247-57. PMC: 4805881. DOI: 10.1016/j.bpj.2015.09.035. View

16.

Weaver W, Milisavljevic V, Miller J, Di Carlo D . Fluid flow induces biofilm formation in Staphylococcus epidermidis polysaccharide intracellular adhesin-positive clinical isolates. Appl Environ Microbiol. 2012; 78(16):5890-6. PMC: 3406141. DOI: 10.1128/AEM.01139-12. View

17.

Secchi E, Vitale A, Mino G, Kantsler V, Eberl L, Rusconi R . The effect of flow on swimming bacteria controls the initial colonization of curved surfaces. Nat Commun. 2020; 11(1):2851. PMC: 7275075. DOI: 10.1038/s41467-020-16620-y. View

18.

Ma L, Jackson K, Landry R, Parsek M, Wozniak D . Analysis of Pseudomonas aeruginosa conditional psl variants reveals roles for the psl polysaccharide in adhesion and maintaining biofilm structure postattachment. J Bacteriol. 2006; 188(23):8213-21. PMC: 1698210. DOI: 10.1128/JB.01202-06. View

19.

Neumann R, Barsi-Andreeta M, Lucas-Oliveira E, Barbalho H, Trevizan W, J Bonagamba T . High accuracy capillary network representation in digital rock reveals permeability scaling functions. Sci Rep. 2021; 11(1):11370. PMC: 8206086. DOI: 10.1038/s41598-021-90090-0. View

20.

OToole G, Wong G . Sensational biofilms: surface sensing in bacteria. Curr Opin Microbiol. 2016; 30:139-146. PMC: 4843124. DOI: 10.1016/j.mib.2016.02.004. View