Corner Flows Induced by Surfactant-Producing Bacteria Bacillus subtilis and Pseudomonas fluorescens

ABSTRACT A mechanistic understanding of bacterial spreading in soil, which has both air and water in angular pore spaces, is critical to control pathogenic contamination of soil and to design bioremediation projects. A recent study (J. Q. Yang, J. E. Sanfilippo, N. Abbasi, Z. Gitai, et al., Proc Nat...

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Main Authors: Yuan Li, Joseph E. Sanfilippo, Daniel Kearns, Judy Q. Yang
Format: Article
Language:English
Published: American Society for Microbiology 2022-10-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.03233-22
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author Yuan Li
Joseph E. Sanfilippo
Daniel Kearns
Judy Q. Yang
author_facet Yuan Li
Joseph E. Sanfilippo
Daniel Kearns
Judy Q. Yang
author_sort Yuan Li
collection DOAJ
description ABSTRACT A mechanistic understanding of bacterial spreading in soil, which has both air and water in angular pore spaces, is critical to control pathogenic contamination of soil and to design bioremediation projects. A recent study (J. Q. Yang, J. E. Sanfilippo, N. Abbasi, Z. Gitai, et al., Proc Natl Acad Sci U S A 118:e2111060118, 2021, https://doi.org/10.1073/pnas.2111060118) shows that Pseudomonas aeruginosa can self-generate flows along sharp corners by producing rhamnolipids, a type of biosurfactants that change the hydrophobicity of solid surfaces. We hypothesize that other types of biosurfactants and biosurfactant-producing bacteria can also generate corner flows. Here, we first demonstrate that rhamnolipids and surfactin, biosurfactants with different chemical structures, can generate corner flows. We identify the critical concentrations of these two biosurfactants to generate corner flow. Second, we demonstrate that two common soil bacteria, Pseudomonas fluorescens and Bacillus subtilis (which produce rhamnolipids and surfactin, respectively), can generate corner flows along sharp corners at the speed of several millimeters per hour. We further show that a surfactin-deficient mutant of B. subtilis cannot generate corner flow. Third, we show that, similar to the finding for P. aeruginosa, the critical corner angle for P. fluorescens and B. subtilis to generate corner flows can be predicted from classic corner flow theories. Finally, we show that the height of corner flows is limited by the roundness of corners. Our results suggest that biosurfactant-induced corner flows are prevalent in soil and should be considered in the modeling and prediction of bacterial spreading in soil. The critical biosurfactant concentrations we identify and the mathematical models we propose will provide a theoretical foundation for future predictions of bacterial spreading in soil. IMPORTANCE The spread of bacteria in soil is critical in soil biogeochemical cycles, soil and groundwater contamination, and the efficiency of soil-based bioremediation projects. However, the mechanistic understanding of bacterial spreading in soil remains incomplete due to a lack of direct observations. Here, we simulate confined spaces of hydrocarbon-covered soil using a transparent material with similar hydrophobicity and visualize the spread of two common soil bacteria, Pseudomonas fluorescens and Bacillus subtilis. We show that both bacteria can generate corner flows at the velocity of several millimeters per hour by producing biosurfactants, soap-like chemicals. We provide quantitative equations to predict the critical corner angle for bacterial corner flow and the maximum distance of the corner spreading. We anticipate that bacterial corner flow is prevalent because biosurfactant-producing bacteria and angular pores are common in soil. Our results will help improve predictions of bacterial spreading in soil and facilitate the design of soil-related bioremediation projects.
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spelling doaj.art-57da9311ea954b7db59a26008c2c4e242022-12-22T02:40:54ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-10-0110510.1128/spectrum.03233-22Corner Flows Induced by Surfactant-Producing Bacteria Bacillus subtilis and Pseudomonas fluorescensYuan Li0Joseph E. Sanfilippo1Daniel Kearns2Judy Q. Yang3Saint Anthony Falls Laboratory, University of Minnesota, Minneapolis, Minnesota, USADepartment of Biochemistry, University of Illinois at Urbana—Champaign, Urbana, Illinois, USADepartment of Biology, Indiana University, Bloomington, Indiana, USASaint Anthony Falls Laboratory, University of Minnesota, Minneapolis, Minnesota, USAABSTRACT A mechanistic understanding of bacterial spreading in soil, which has both air and water in angular pore spaces, is critical to control pathogenic contamination of soil and to design bioremediation projects. A recent study (J. Q. Yang, J. E. Sanfilippo, N. Abbasi, Z. Gitai, et al., Proc Natl Acad Sci U S A 118:e2111060118, 2021, https://doi.org/10.1073/pnas.2111060118) shows that Pseudomonas aeruginosa can self-generate flows along sharp corners by producing rhamnolipids, a type of biosurfactants that change the hydrophobicity of solid surfaces. We hypothesize that other types of biosurfactants and biosurfactant-producing bacteria can also generate corner flows. Here, we first demonstrate that rhamnolipids and surfactin, biosurfactants with different chemical structures, can generate corner flows. We identify the critical concentrations of these two biosurfactants to generate corner flow. Second, we demonstrate that two common soil bacteria, Pseudomonas fluorescens and Bacillus subtilis (which produce rhamnolipids and surfactin, respectively), can generate corner flows along sharp corners at the speed of several millimeters per hour. We further show that a surfactin-deficient mutant of B. subtilis cannot generate corner flow. Third, we show that, similar to the finding for P. aeruginosa, the critical corner angle for P. fluorescens and B. subtilis to generate corner flows can be predicted from classic corner flow theories. Finally, we show that the height of corner flows is limited by the roundness of corners. Our results suggest that biosurfactant-induced corner flows are prevalent in soil and should be considered in the modeling and prediction of bacterial spreading in soil. The critical biosurfactant concentrations we identify and the mathematical models we propose will provide a theoretical foundation for future predictions of bacterial spreading in soil. IMPORTANCE The spread of bacteria in soil is critical in soil biogeochemical cycles, soil and groundwater contamination, and the efficiency of soil-based bioremediation projects. However, the mechanistic understanding of bacterial spreading in soil remains incomplete due to a lack of direct observations. Here, we simulate confined spaces of hydrocarbon-covered soil using a transparent material with similar hydrophobicity and visualize the spread of two common soil bacteria, Pseudomonas fluorescens and Bacillus subtilis. We show that both bacteria can generate corner flows at the velocity of several millimeters per hour by producing biosurfactants, soap-like chemicals. We provide quantitative equations to predict the critical corner angle for bacterial corner flow and the maximum distance of the corner spreading. We anticipate that bacterial corner flow is prevalent because biosurfactant-producing bacteria and angular pores are common in soil. Our results will help improve predictions of bacterial spreading in soil and facilitate the design of soil-related bioremediation projects.https://journals.asm.org/doi/10.1128/spectrum.03233-22Bacillus subtilisbacterial spreadingPseudomonas fluorescensbiosurfactantcontact anglecorners
spellingShingle Yuan Li
Joseph E. Sanfilippo
Daniel Kearns
Judy Q. Yang
Corner Flows Induced by Surfactant-Producing Bacteria Bacillus subtilis and Pseudomonas fluorescens
Microbiology Spectrum
Bacillus subtilis
bacterial spreading
Pseudomonas fluorescens
biosurfactant
contact angle
corners
title Corner Flows Induced by Surfactant-Producing Bacteria Bacillus subtilis and Pseudomonas fluorescens
title_full Corner Flows Induced by Surfactant-Producing Bacteria Bacillus subtilis and Pseudomonas fluorescens
title_fullStr Corner Flows Induced by Surfactant-Producing Bacteria Bacillus subtilis and Pseudomonas fluorescens
title_full_unstemmed Corner Flows Induced by Surfactant-Producing Bacteria Bacillus subtilis and Pseudomonas fluorescens
title_short Corner Flows Induced by Surfactant-Producing Bacteria Bacillus subtilis and Pseudomonas fluorescens
title_sort corner flows induced by surfactant producing bacteria bacillus subtilis and pseudomonas fluorescens
topic Bacillus subtilis
bacterial spreading
Pseudomonas fluorescens
biosurfactant
contact angle
corners
url https://journals.asm.org/doi/10.1128/spectrum.03233-22
work_keys_str_mv AT yuanli cornerflowsinducedbysurfactantproducingbacteriabacillussubtilisandpseudomonasfluorescens
AT josephesanfilippo cornerflowsinducedbysurfactantproducingbacteriabacillussubtilisandpseudomonasfluorescens
AT danielkearns cornerflowsinducedbysurfactantproducingbacteriabacillussubtilisandpseudomonasfluorescens
AT judyqyang cornerflowsinducedbysurfactantproducingbacteriabacillussubtilisandpseudomonasfluorescens