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Low-concentration iron promotes Klebsiella pneumoniae biofilm formation by suppressing succinic acid

BACKGROUND: Klebsiella pneumoniae is widely distributed in water and plays a major role in both human and poultry infections. Many K. pneumoniae strains form biofilms on various surfaces, enhancing their pathogenicity and resistance to antibiotics. The water supply pipeline of chicken farms has beco...

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Autores principales: Liu, Kexin, Tan, Shuang, Ye, Weiyuan, Hou, Limin, Fang, Binghu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8996614/
https://www.ncbi.nlm.nih.gov/pubmed/35410114
http://dx.doi.org/10.1186/s12866-022-02518-w
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author Liu, Kexin
Tan, Shuang
Ye, Weiyuan
Hou, Limin
Fang, Binghu
author_facet Liu, Kexin
Tan, Shuang
Ye, Weiyuan
Hou, Limin
Fang, Binghu
author_sort Liu, Kexin
collection PubMed
description BACKGROUND: Klebsiella pneumoniae is widely distributed in water and plays a major role in both human and poultry infections. Many K. pneumoniae strains form biofilms on various surfaces, enhancing their pathogenicity and resistance to antibiotics. The water supply pipeline of chicken farms has become a hotbed for the growth of K pneumoniae biofilm because of its humid environment, and because the chicken drinking water pipeline is thin, it is easily blocked by the biofilm, and the diffused cells can cause repeated and persistent infections. Iron is vital to the growth of microorganisms and the formation of biofilms. Therefore, the aim of this study was to examine the effects of iron on K. pneumoniae biofilm formation and any associated metabolic changes to provide a rationale for reducing the formation of biofilms. RESULTS: Biofilm formation was enhanced to the greatest extent by the presence of 0.16 mM FeCl(2), producing a denser structure under electron microscopy. The number of biofilm-forming and planktonic bacteria did not change, but protein and polysaccharide concentrations in the bacterial extracellular polymeric substances (EPS) were significantly increased by iron supplementation. To clarify this mechanism, intracellular metabolomic analysis was carried out, showing that the differential, down-regulated metabolites included succinic acid. The addition of 1.7 mM succinic acid counteracted the biofilm-forming effect of iron, with no bactericidal side effects. CONCLUSION: This study demonstrates the importance of succinic acid and iron in K. pneumoniae biofilms, and provides insight into the formation of K. pneumoniae biofilms and direction for the development of new antibacterial agents.
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spelling pubmed-89966142022-04-12 Low-concentration iron promotes Klebsiella pneumoniae biofilm formation by suppressing succinic acid Liu, Kexin Tan, Shuang Ye, Weiyuan Hou, Limin Fang, Binghu BMC Microbiol Research BACKGROUND: Klebsiella pneumoniae is widely distributed in water and plays a major role in both human and poultry infections. Many K. pneumoniae strains form biofilms on various surfaces, enhancing their pathogenicity and resistance to antibiotics. The water supply pipeline of chicken farms has become a hotbed for the growth of K pneumoniae biofilm because of its humid environment, and because the chicken drinking water pipeline is thin, it is easily blocked by the biofilm, and the diffused cells can cause repeated and persistent infections. Iron is vital to the growth of microorganisms and the formation of biofilms. Therefore, the aim of this study was to examine the effects of iron on K. pneumoniae biofilm formation and any associated metabolic changes to provide a rationale for reducing the formation of biofilms. RESULTS: Biofilm formation was enhanced to the greatest extent by the presence of 0.16 mM FeCl(2), producing a denser structure under electron microscopy. The number of biofilm-forming and planktonic bacteria did not change, but protein and polysaccharide concentrations in the bacterial extracellular polymeric substances (EPS) were significantly increased by iron supplementation. To clarify this mechanism, intracellular metabolomic analysis was carried out, showing that the differential, down-regulated metabolites included succinic acid. The addition of 1.7 mM succinic acid counteracted the biofilm-forming effect of iron, with no bactericidal side effects. CONCLUSION: This study demonstrates the importance of succinic acid and iron in K. pneumoniae biofilms, and provides insight into the formation of K. pneumoniae biofilms and direction for the development of new antibacterial agents. BioMed Central 2022-04-11 /pmc/articles/PMC8996614/ /pubmed/35410114 http://dx.doi.org/10.1186/s12866-022-02518-w Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Liu, Kexin
Tan, Shuang
Ye, Weiyuan
Hou, Limin
Fang, Binghu
Low-concentration iron promotes Klebsiella pneumoniae biofilm formation by suppressing succinic acid
title Low-concentration iron promotes Klebsiella pneumoniae biofilm formation by suppressing succinic acid
title_full Low-concentration iron promotes Klebsiella pneumoniae biofilm formation by suppressing succinic acid
title_fullStr Low-concentration iron promotes Klebsiella pneumoniae biofilm formation by suppressing succinic acid
title_full_unstemmed Low-concentration iron promotes Klebsiella pneumoniae biofilm formation by suppressing succinic acid
title_short Low-concentration iron promotes Klebsiella pneumoniae biofilm formation by suppressing succinic acid
title_sort low-concentration iron promotes klebsiella pneumoniae biofilm formation by suppressing succinic acid
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8996614/
https://www.ncbi.nlm.nih.gov/pubmed/35410114
http://dx.doi.org/10.1186/s12866-022-02518-w
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