Pore-scale hydrodynamics influence the spatial evolution of bacterial biofilms in a microfluidic porous network

Jayde A. Aufrecht; Jason D. Fowlkes; Amber N. Bible; Jennifer Morrell-Falvey; Mitchel J. Doktycz; Scott T. Retterer

doi:10.1371/journal.pone.0218316

Pore-scale hydrodynamics influence the spatial evolution of bacterial biofilms in a microfluidic porous network

Jayde A. Aufrecht, Jason D. Fowlkes, Amber N. Bible, Jennifer Morrell-Falvey, Mitchel J. Doktycz, Scott T. Retterer

Research output: Contribution to journal › Article › peer-review

53 Scopus citations

Abstract

Bacteria occupy heterogeneous environments, attaching and growing within pores in materials, living hosts, and matrices like soil. Systems that permit high-resolution visualization of dynamic bacterial processes within the physical confines of a realistic and tractable porous media environment are rare. Here we use microfluidics to replicate the grain shape and packing density of natural sands in a 2D platform to study the flow-induced spatial evolution of bacterial biofilms underground. We discover that initial bacterial dispersal and grain attachment is influenced by bacterial transport across pore space velocity gradients, a phenomenon otherwise known as rheotaxis. We find that gravity-driven flow conditions activate different bacterial cell-clustering phenotypes depending on the strain’s ability to product extracellular polymeric substances (EPS). A wildtype, biofilm-producing bacteria formed compact, multicellular patches while an EPS-defective mutant displayed a linked-cell phenotype in the presence of flow. These phenotypes subsequently influenced the overall spatial distribution of cells across the porous media network as colonies grew and altered the fluid dynamics of their microenvironment.

Original language	English
Article number	e0218316
Journal	PLoS ONE
Volume	14
Issue number	6
DOIs	https://doi.org/10.1371/journal.pone.0218316
State	Published - Oct 1 2018

Funding

This manuscript has been authored by UT-Battelle, LLC under Contract No. DE-AC05-00OR22725 with the U.S. Department of Energy. The United States Government retains and the publisher, by accepting the article for publication, acknowledges that the United States Government retains a non-exclusive, paid-up, irrevocable, world-wide license to publish or reproduce the published form of this manuscript, or allow others to do so, for United States Government purposes. The Department of Energy will provide public access to these results of federally sponsored research in accordance with the DOE Public Access Plan (http://energy.gov/downloads/doe-public-access-plan). This work was supported in part by the Genomic Science Program, U.S. Department of Energy, Office of Science, Biological and Environmental Research, as part of the Plant Microbe Interfaces Scientific Focus Area (http:// pmi.ornl.gov). The fabrication of the microfluidic platforms was carried out in the Nanofabrication Research Laboratory at the Center for Nanophase Materials Sciences, which is a DOE Office of Science User Facility. JAA is supported by an NSF graduate research fellowship DGE -1452154.

Funders	Funder number
Center for Nanophase Materials Sciences
DOE Office of Science
DOE Public Access Plan
Plant Microbe Interfaces Scientific Focus Area
United States Government
National Science Foundation	DGE -1452154
U.S. Department of Energy
Directorate for Education and Human Resources	1452154
Office of Science
Biological and Environmental Research

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title = "Pore-scale hydrodynamics influence the spatial evolution of bacterial biofilms in a microfluidic porous network",

abstract = "Bacteria occupy heterogeneous environments, attaching and growing within pores in materials, living hosts, and matrices like soil. Systems that permit high-resolution visualization of dynamic bacterial processes within the physical confines of a realistic and tractable porous media environment are rare. Here we use microfluidics to replicate the grain shape and packing density of natural sands in a 2D platform to study the flow-induced spatial evolution of bacterial biofilms underground. We discover that initial bacterial dispersal and grain attachment is influenced by bacterial transport across pore space velocity gradients, a phenomenon otherwise known as rheotaxis. We find that gravity-driven flow conditions activate different bacterial cell-clustering phenotypes depending on the strain{\textquoteright}s ability to product extracellular polymeric substances (EPS). A wildtype, biofilm-producing bacteria formed compact, multicellular patches while an EPS-defective mutant displayed a linked-cell phenotype in the presence of flow. These phenotypes subsequently influenced the overall spatial distribution of cells across the porous media network as colonies grew and altered the fluid dynamics of their microenvironment.",

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AU - Doktycz, Mitchel J.

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Pore-scale hydrodynamics influence the spatial evolution of bacterial biofilms in a microfluidic porous network

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