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Quantifying adsorption and transport in Gram-positive cell walls by second-harmonic light scattering.

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Τίτλος: Quantifying adsorption and transport in Gram-positive cell walls by second-harmonic light scattering.
Συγγραφείς: Hu XH; Department of Chemistry and Institute for Membranes and Interfaces, Temple University, 1901 N. 13th Street, Philadelphia, PA 19122, USA., Li Y; Department of Chemistry and Institute for Membranes and Interfaces, Temple University, 1901 N. 13th Street, Philadelphia, PA 19122, USA., Mendelsohn F; Department of Chemistry and Institute for Membranes and Interfaces, Temple University, 1901 N. 13th Street, Philadelphia, PA 19122, USA., Wu Y; Department of Chemistry and Institute for Membranes and Interfaces, Temple University, 1901 N. 13th Street, Philadelphia, PA 19122, USA., Ma J; Department of Chemistry and Institute for Membranes and Interfaces, Temple University, 1901 N. 13th Street, Philadelphia, PA 19122, USA., Dai HL; Department of Chemistry and Institute for Membranes and Interfaces, Temple University, 1901 N. 13th Street, Philadelphia, PA 19122, USA. Electronic address: hldai@temple.edu.
Πηγή: Biophysical journal [Biophys J] 2026 Sep 01; Vol. 125 (17), pp. 4635-4648. Date of Electronic Publication: 2026 Jul 09.
Τύπος έκδοσης: Journal Article; Research Support, Non-U.S. Gov't
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: Cell Press Country of Publication: United States NLM ID: 0370626 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1542-0086 (Electronic) Linking ISSN: 00063495 NLM ISO Abbreviation: Biophys J Subsets: MEDLINE
Imprint Name(s): Publication: Cambridge, MA : Cell Press
Original Publication: New York, Published by Rockefeller University Press [etc.] for the Biophysical Society.
Ιατρικοί όροι (MeSH): Cell Wall*/metabolism , Gram-Positive Bacteria*/metabolism , Gram-Positive Bacteria*/cytology , Scattering, Radiation* , Light*, Rosaniline Dyes/metabolism ; Cell Membrane/metabolism ; Adsorption ; Biological Transport ; Kinetics
Περίληψη: Elucidating molecule-membrane interactions within bacterial cell walls is essential for understanding proliferation of bacteria in the environment and developing effective therapeutics. Quantitative measurements of molecular adsorption and transport have been reported for individual membrane layers in Gram-negative bacteria, yet no analogous investigation exists for Gram-positive bacteria, which feature a substantially different cell-envelope architecture. In this work, we employed time-resolved second-harmonic light scattering to quantify the adsorption and transport kinetics of a small antimicrobial cation, malachite green, at each of the surface layer (SL), peptidoglycan mesh (PM), and cytoplasmic membrane (CM) within the cell walls of three Gram-positive organisms: Lysinibacillus sphaericus, which possesses a canonical crystalline S-layer; and Bacillus subtilis and Lacticaseibacillus rhamnosus, whose outermost cell-wall barriers are composed of surface-associated proteins and teichoic acids. The transport rates measured for all three bacteria reveal a consistent permeability hierarchy in which transport through the SL and PM is rapid, whereas translocation across the CM is two orders of magnitude slower, constituting the rate-limiting bottleneck for cytosolic entry. In comparing the adsorption and transport behaviors across the three Gram-positive strains studied here and previously reported Gram-negative bacteria, we find that despite profound differences in cell-envelope architecture, molecular uptake is regulated in a similar, hierarchical manner, with outer layers governing accessibility at similar rates and the lipid bilayer controlling cytosolic entry with a much slower rate. The SLs of Gram-positive bacteria behave similarly to the porin ion channels of Gram-negative bacteria in transporting hydrophobic molecular cations. Moreover, the adsorption free energies (approximately -9.5 to -12 kcal · mol-1) determined for the various interfaces within the Gram-positive and Gram-negative cell envelopes are remarkably similar, with the sole notable distinction being the substantially higher surface charge density of the Gram-negative outer membrane relative to the Gram-positive SL.
(Copyright © 2026 Biophysical Society. Published by Elsevier Inc. All rights reserved.)
Competing Interests: Declaration of interests The authors declare no competing interests.
Substance Nomenclature: 12058M7ORO (malachite green)
0 (Rosaniline Dyes)
Entry Date(s): Date Created: 20260710 Date Completed: 20260901 Latest Revision: 20260915
Update Code: 20260916
DOI: 10.1016/j.bpj.2026.07.007
PMID: 42427033
Βάση Δεδομένων: MEDLINE
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  Data: Quantifying adsorption and transport in Gram-positive cell walls by second-harmonic light scattering.
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  Data: <searchLink fieldCode="AU" term="%22Hu+XH%22">Hu XH</searchLink>; Department of Chemistry and Institute for Membranes and Interfaces, Temple University, 1901 N. 13th Street, Philadelphia, PA 19122, USA.<br /><searchLink fieldCode="AU" term="%22Li+Y%22">Li Y</searchLink>; Department of Chemistry and Institute for Membranes and Interfaces, Temple University, 1901 N. 13th Street, Philadelphia, PA 19122, USA.<br /><searchLink fieldCode="AU" term="%22Mendelsohn+F%22">Mendelsohn F</searchLink>; Department of Chemistry and Institute for Membranes and Interfaces, Temple University, 1901 N. 13th Street, Philadelphia, PA 19122, USA.<br /><searchLink fieldCode="AU" term="%22Wu+Y%22">Wu Y</searchLink>; Department of Chemistry and Institute for Membranes and Interfaces, Temple University, 1901 N. 13th Street, Philadelphia, PA 19122, USA.<br /><searchLink fieldCode="AU" term="%22Ma+J%22">Ma J</searchLink>; Department of Chemistry and Institute for Membranes and Interfaces, Temple University, 1901 N. 13th Street, Philadelphia, PA 19122, USA.<br /><searchLink fieldCode="AU" term="%22Dai+HL%22">Dai HL</searchLink>; Department of Chemistry and Institute for Membranes and Interfaces, Temple University, 1901 N. 13th Street, Philadelphia, PA 19122, USA. Electronic address: hldai@temple.edu.
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  Data: <searchLink fieldCode="JN" term="%220370626%22">Biophysical journal</searchLink> [Biophys J] 2026 Sep 01; Vol. 125 (17), pp. 4635-4648. <i>Date of Electronic Publication: </i>2026 Jul 09.
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  Data: Journal Article; Research Support, Non-U.S. Gov't
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  Data: <i>Publisher: </i><searchLink fieldCode="PB" term="%22Cell+Press%22">Cell Press </searchLink><i>Country of Publication: </i>United States <i>NLM ID: </i>0370626 <i>Publication Model: </i>Print-Electronic <i>Cited Medium: </i>Internet <i>ISSN: </i>1542-0086 (Electronic) <i>Linking ISSN: </i><searchLink fieldCode="IS" term="%2200063495%22">00063495 </searchLink><i>NLM ISO Abbreviation: </i>Biophys J <i>Subsets: </i>MEDLINE
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  Data: <searchLink fieldCode="MM" term="%22Cell+Wall%22">Cell Wall*</searchLink>/<searchLink fieldCode="MM" term="%22Cell+Wall+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Gram-Positive+Bacteria%22">Gram-Positive Bacteria*</searchLink>/<searchLink fieldCode="MM" term="%22Gram-Positive+Bacteria+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Gram-Positive+Bacteria%22">Gram-Positive Bacteria*</searchLink>/<searchLink fieldCode="MM" term="%22Gram-Positive+Bacteria+cytology%22">cytology</searchLink> <br /><searchLink fieldCode="MM" term="%22Scattering%2C+Radiation%22">Scattering, Radiation*</searchLink> <br /><searchLink fieldCode="MM" term="%22Light%22">Light*</searchLink><br /><searchLink fieldCode="MH" term="%22Rosaniline+Dyes%22">Rosaniline Dyes</searchLink>/<searchLink fieldCode="MH" term="%22Rosaniline+Dyes+metabolism%22">metabolism</searchLink> ; <searchLink fieldCode="MH" term="%22Cell+Membrane%22">Cell Membrane</searchLink>/<searchLink fieldCode="MH" term="%22Cell+Membrane+metabolism%22">metabolism</searchLink> ; <searchLink fieldCode="MH" term="%22Adsorption%22">Adsorption</searchLink> ; <searchLink fieldCode="MH" term="%22Biological+Transport%22">Biological Transport</searchLink> ; <searchLink fieldCode="MH" term="%22Kinetics%22">Kinetics</searchLink>
– Name: Abstract
  Label: Abstract
  Group: Ab
  Data: Elucidating molecule-membrane interactions within bacterial cell walls is essential for understanding proliferation of bacteria in the environment and developing effective therapeutics. Quantitative measurements of molecular adsorption and transport have been reported for individual membrane layers in Gram-negative bacteria, yet no analogous investigation exists for Gram-positive bacteria, which feature a substantially different cell-envelope architecture. In this work, we employed time-resolved second-harmonic light scattering to quantify the adsorption and transport kinetics of a small antimicrobial cation, malachite green, at each of the surface layer (SL), peptidoglycan mesh (PM), and cytoplasmic membrane (CM) within the cell walls of three Gram-positive organisms: Lysinibacillus sphaericus, which possesses a canonical crystalline S-layer; and Bacillus subtilis and Lacticaseibacillus rhamnosus, whose outermost cell-wall barriers are composed of surface-associated proteins and teichoic acids. The transport rates measured for all three bacteria reveal a consistent permeability hierarchy in which transport through the SL and PM is rapid, whereas translocation across the CM is two orders of magnitude slower, constituting the rate-limiting bottleneck for cytosolic entry. In comparing the adsorption and transport behaviors across the three Gram-positive strains studied here and previously reported Gram-negative bacteria, we find that despite profound differences in cell-envelope architecture, molecular uptake is regulated in a similar, hierarchical manner, with outer layers governing accessibility at similar rates and the lipid bilayer controlling cytosolic entry with a much slower rate. The SLs of Gram-positive bacteria behave similarly to the porin ion channels of Gram-negative bacteria in transporting hydrophobic molecular cations. Moreover, the adsorption free energies (approximately -9.5 to -12 kcal · mol<superscript>-1</superscript>) determined for the various interfaces within the Gram-positive and Gram-negative cell envelopes are remarkably similar, with the sole notable distinction being the substantially higher surface charge density of the Gram-negative outer membrane relative to the Gram-positive SL.<br /> (Copyright © 2026 Biophysical Society. Published by Elsevier Inc. All rights reserved.)
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  Data: Declaration of interests The authors declare no competing interests.
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  Data: 12058M7ORO (malachite green)<br />0 (Rosaniline Dyes)
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  Data: 10.1016/j.bpj.2026.07.007
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        Value: 10.1016/j.bpj.2026.07.007
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        Text: English
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      Pagination:
        StartPage: 4635
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      – SubjectFull: Rosaniline Dyes metabolism
        Type: general
      – SubjectFull: Cell Membrane metabolism
        Type: general
      – SubjectFull: Adsorption
        Type: general
      – SubjectFull: Biological Transport
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      – SubjectFull: Scattering, Radiation
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      – SubjectFull: Light
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      – TitleFull: Quantifying adsorption and transport in Gram-positive cell walls by second-harmonic light scattering.
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