Evaluation of the interaction between polymyxin B and  Pseudomonas aeruginosa  biofilm and planktonic cells: reactive oxygen species induction and zeta potential

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Abstract

Background

Although the most widely accepted mechanism of action for polymyxins is related to bacterial lysis via disruption, we hypothesized that this antimicrobial drug class could have other effects on Pseudomonas aeruginosa planktonic and sessile cells. Little is known regarding oxidative burst and zeta potential (ZP) data associated with the interaction between polymyxin B and P. aeruginosa cells. The present study evaluated endogenous reactive oxygen species (ROS) production and changes in the net charges of biofilm and planktonic cells in response to polymyxin B.

Results

Polymyxin B induced concentration-dependent killing at all concentrations tested in planktonic and sessile cells from P. aeruginosa strains. Sublethal concentrations of polymyxin B induced oxidative burst. ROS production was higher in resistant planktonic cells than in biofilm cells but this was not observed for susceptible cells. Moreover, no net surface charge alterations were observed in planktonic cells from a susceptible strain treated with polymyxin B, but a significant increase of ZP was noted in planktonic cells from a resistant strain.

Conclusion

Oxidative burst generated by planktonic and sessile cells from P. aeruginosa strains against polymyxin B indicates that ROS may have an important role in the mechanism of action of this drug. ZP data revealed that electrostatic interactions of the cationic peptide with the anionic surface of the cells are strain-dependent. Therefore, we suggested that the intracellular effects of polymyxin B should be further investigated to understand polymyxin B-induced stress in P. aeruginosa.

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Most cited references 33

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Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses

J.G. Scandalios (2005)

Molecular oxygen (O2) is the premier biological electron acceptor that serves vital roles in fundamental cellular functions. However, with the beneficial properties of O2 comes the inadvertent formation of reactive oxygen species (ROS) such as superoxide (O2 ·- ), hydrogen peroxide, and hydroxyl radical (OH · ). If unabated, ROS pose a serious threat to or cause the death of aerobic cells. To minimize the damaging effects of ROS, aerobic organisms evolved non-enzymatic and enzymatic antioxidant defenses. The latter include catalases, peroxidases, superoxide dismutases, and glutathione S-transferases (GST). Cellular ROS-sensing mechanisms are not well understood, but a number of transcription factors that regulate the expression of antioxidant genes are well characterized in prokaryotes and in yeast. In higher eukaryotes, oxidative stress responses are more complex and modulated by several regulators. In mammalian systems, two classes of transcription factors, nuclear factor kB and activator protein-1, are involved in the oxidative stress response. Antioxidant-specific gene induction, involved in xenobiotic metabolism, is mediated by the "antioxidant responsive element" (ARE) commonly found in the promoter region of such genes. ARE is present in mammalian GST, metallothioneine-I and MnSod genes, but has not been found in plant Gst genes. However, ARE is present in the promoter region of the three maize catalase (Cat) genes. In plants, ROS have been implicated in the damaging effects of various environmental stress conditions. Many plant defense genes are activated in response to these conditions, including the three maize Cat and some of the superoxide dismutase (Sod) genes.

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Tolerance to the antimicrobial peptide colistin in Pseudomonas aeruginosa biofilms is linked to metabolically active cells, and depends on the pmr and mexAB-oprM genes.

Tim Tolker-Nielsen, Helle Krogh Johansen, Sünje J Pamp … (2008)

Bacteria living as biofilm are frequently reported to exhibit inherent tolerance to antimicrobial compounds, and might therefore contribute to the persistence of infections. Antimicrobial peptides are attracting increasing interest as new potential antimicrobial therapeutics; however, little is known about potential mechanisms, which might contribute to resistance or tolerance development towards these compounds in biofilms. Here we provide evidence that a spatially distinct subpopulation of metabolically active cells in Pseudomonas aeruginosa biofilms is able to develop tolerance to the antimicrobial peptide colistin. On the contrary, biofilm cells exhibiting low metabolic activity were killed by colistin. We demonstrate that the subpopulation of metabolically active cells is able to adapt to colistin by inducing a specific adaptation mechanism mediated by the pmr operon, as well as an unspecific adaptation mechanism mediated by the mexAB-oprM genes. Mutants defective in either pmr-mediated lipopolysaccharide modification or in mexAB-oprM-mediated antimicrobial efflux were not able to develop a tolerant subpopulation in biofilms. In contrast to the observed pattern of colistin-mediated killing in biofilms, conventional antimicrobial compounds such as ciprofloxacin and tetracycline were found to specifically kill the subpopulation of metabolically active biofilm cells, whereas the subpopulation exhibiting low metabolic activity survived the treatment. Consequently, targeting the two physiologically distinct subpopulations by combined antimicrobial treatment with either ciprofloxacin and colistin or tetracycline and colistin almost completely eradicated all biofilm cells.

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The PmrA-regulated pmrC gene mediates phosphoethanolamine modification of lipid A and polymyxin resistance in Salmonella enterica.

Hyunwoo Lee, Eduardo A. Groisman, Fu-Ning Hsu … (2004)

The PmrA/PmrB regulatory system of Salmonella enterica controls the modification of lipid A with aminoarabinose and phosphoethanolamine. The aminoarabinose modification is required for resistance to the antibiotic polymyxin B, as mutations of the PmrA-activated pbg operon or ugd gene result in strains that lack aminoarabinose in their lipid A molecules and are more susceptible to polymyxin B. Additional PmrA-regulated genes appear to participate in polymyxin B resistance, as pbgP and ugd mutants are not as sensitive to polymyxin B as a pmrA mutant. Moreover, the role that the phosphoethanolamine modification of lipid A plays in the resistance to polymyxin B has remained unknown. Here we address both of these questions by establishing that the PmrA-activated pmrC gene encodes an inner membrane protein that is required for the incorporation of phosphoethanolamine into lipid A and for polymyxin B resistance. The PmrC protein consists of an N-terminal region with five transmembrane domains followed by a large periplasmic region harboring the putative enzymatic domain. A pbgP pmrC double mutant resembled a pmrA mutant both in its lipid A profile and in its susceptibility to polymyxin B, indicating that the PmrA-dependent modification of lipid A with aminoarabinose and phosphoethanolamine is responsible for PmrA-regulated polymyxin B resistance.

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Author and article information

Contributors

Marlucy Rodrigues Lima: marlucygv@hotmail.com

Gabriella Freitas Ferreira:

ORCID: http://orcid.org/0000-0001-6842-1934

+55 33 999440070 , gabriella.freitas@ufjf.edu.br

Wallace Ribeiro Nunes Neto: wallaceneto2010@hotmail.com

Joveliane de Melo Monteiro: jovelianemello53@gmail.com

Áquila Rodrigues Costa Santos: aquila_rcs@hotmail.com

Priscila Batista Tavares: priscila4067@hotmail.com

Ângelo Márcio Leite Denadai: angelomld@gmail.com

Maria Rosa Quaresma Bomfim: mrqbomfim@yahoo.com.br

Vera Lúcia dos Santos: verabio@gmail.com

Sirlei Garcia Marques: sirleigmarques@gmail.com

Andrea de Souza Monteiro: andreasmont@gmail.com

Journal

Journal ID (nlm-ta): BMC Microbiol

Journal ID (iso-abbrev): BMC Microbiol

Title: BMC Microbiology

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2180

Publication date (Electronic): 29 May 2019

Publication date PMC-release: 29 May 2019

Publication date Collection: 2019

Volume: 19

Electronic Location Identifier: 115

Affiliations

[1 ]GRID grid.441760.0, Faculdade de Ciências da Saúde, , Universidade Vale do Rio Doce, ; Governador Valadares, MG Brazil

[2 ]ISNI 0000 0001 2170 9332, GRID grid.411198.4, Departamento de Farmácia, Programa Multicêntrico de Pós-Graduação em Bioquímica e Biologia Molecular, , Universidade Federal de Juiz de Fora, UFJF, ; Campus Governador Valadares - MG. R. Manoel Byrro, 241 - Vila Bretas, Governador Valadares, MG 35032-620 Brazil

[3 ]ISNI 0000 0004 0414 7982, GRID grid.442152.4, Universidade CEUMA, ; São Luís, MA Brazil

[4 ]ISNI 0000 0001 2181 4888, GRID grid.8430.f, Departamento de Microbiologia, Instituto de Ciência Biológicas, , Universidade Federal de Minas Gerais, ; Belo Horizonte, MG Brazil

[5 ]ISNI 0000 0004 0577 2472, GRID grid.488456.3, Hospital Universitário da Universidade Federal do Maranhão, ; São Luís, MA Brazil

[6 ]Laboratório Cedro, São Luís, MA Brazil

Author information

Gabriella Freitas Ferreira http://orcid.org/0000-0001-6842-1934

Article

Publisher ID: 1485

DOI: 10.1186/s12866-019-1485-8

PMC ID: 6542102

PubMed ID: 31142260

SO-VID: d1f85707-ac47-482f-b079-24849c1f2dba

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 8 March 2018

Date accepted : 10 May 2019

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;

Award ID: CNPq, MCT/CNPq-NANO: 550321/2012-8

Funded by: FundRef http://dx.doi.org/10.13039/501100004901, Fundação de Amparo à Pesquisa do Estado de Minas Gerais;

Award ID: APQ-00645-12

Award ID: APQ-00435-14

Funded by: Financiadora de Estudos e Pesquisas

Award ID: FINEP: 0633/13

Custom metadata

ScienceOpen disciplines: Microbiology & Virology

Keywords: p. aeruginosa,biofilm and planktonic cells,polymyxin b,reactive oxygen species,surface electrical property

Data availability:

ScienceOpen disciplines: Microbiology & Virology

Keywords: p. aeruginosa, biofilm and planktonic cells, polymyxin b, reactive oxygen species, surface electrical property

Evaluation of the interaction between polymyxin B and Pseudomonas aeruginosa biofilm and planktonic cells: reactive oxygen species induction and zeta potential

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Abstract

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Bacterial vaginosis and biofilm

Most cited references 33

Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses

Tolerance to the antimicrobial peptide colistin in Pseudomonas aeruginosa biofilms is linked to metabolically active cells, and depends on the pmr and mexAB-oprM genes.

The PmrA-regulated pmrC gene mediates phosphoethanolamine modification of lipid A and polymyxin resistance in Salmonella enterica.

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