Iron acquisition system of Sphingobium sp. strain SYK-6, a degrader of lignin-derived aromatic compounds

Abstract Iron, an essential element for all organisms, acts as a cofactor of enzymes in bacterial degradation of recalcitrant aromatic compounds. The bacterial family, Sphingomonadaceae comprises various degraders of recalcitrant aromatic compounds; however, little is known about their iron acquisition system. Here, we investigated the iron acquisition system in a model bacterium capable of degrading lignin-derived aromatics, Sphingobium sp. strain SYK-6. Analyses of SYK-6 mutants revealed that FiuA (SLG_34550), a TonB-dependent receptor (TBDR), was the major outer membrane iron transporter. Three other TBDRs encoded by SLG_04340, SLG_04380, and SLG_10860 also participated in iron uptake, and tonB2 (SLG_34540), one of the six tonB comprising the Ton complex which enables TBDR-mediated transport was critical for iron uptake. The ferrous iron transporter FeoB (SLG_36840) played an important role in iron uptake across the inner membrane. The promoter activities of most of the iron uptake genes were induced under iron-limited conditions, and their regulation is controlled by SLG_29410 encoding the ferric uptake regulator, Fur. Although feoB, among all the iron uptake genes identified is highly conserved in Sphingomonad strains, the outer membrane transporters seem to be diversified. Elucidation of the iron acquisition system promises better understanding of the bacterial degradation mechanisms of aromatic compounds.

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Iron acquisition system of Sphingobium sp. strain SYK-6, a degrader of lignin-derived aromatic compounds

10.1101/2020.03.26.005173 ◽

2020 ◽

Author(s):

Masaya Fujita ◽

Taichi Sakumoto ◽

Kenta Tanatani ◽

Hong Yang Yu ◽

Kosuke Mori ◽

...

Keyword(s):

Outer Membrane ◽

Aromatic Compounds ◽

Iron Uptake ◽

Iron Acquisition ◽

Essential Element ◽

Acquisition System ◽

Bacterial Degradation ◽

Iron Acquisition System ◽

Iron Transporter ◽

Outer Membrane Transporters

AbstractIron, an essential element for all organisms, acts as a cofactor of enzymes in bacterial degradation of recalcitrant aromatic compounds. The bacterial family, Sphingomonadaceae comprises various degraders of recalcitrant aromatic compounds; however, little is known about their iron acquisition system. Here, we investigated the iron acquisition system in a model bacterium capable of degrading lignin-derived aromatics, Sphingobium sp. strain SYK-6. Analyses of SYK-6 mutants revealed that FiuA (SLG_34550), a TonB-dependent receptor (TBDR), was the major outer membrane iron transporter. Three other TBDRs encoded by SLG_04340, SLG_04380, and SLG_10860 also participated in iron uptake, and tonB2 (SLG_34550), one of the six tonB comprising the Ton complex which enables TBDR-mediated transport was critical for iron uptake. The ferrous iron transporter FeoB (SLG_36840) played an important role in iron uptake across the inner membrane. The promoter activities of most of the iron uptake genes were induced under iron-limited conditions, and their regulation is controlled by SLG_29410 encoding the ferric uptake regulator, Fur. Although feoB, among all the iron uptake genes identified is highly conserved in Sphingomonad strains, the outer membrane transporters seem to be diversified. Elucidation of the iron acquisition system promises better understanding of the bacterial degradation mechanisms of aromatic compounds.

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Author Correction: Iron acquisition system of Sphingobium sp. strain SYK-6, a degrader of lignin-derived aromatic compounds

Scientific Reports ◽

10.1038/s41598-020-73843-1 ◽

2020 ◽

Vol 10 (1) ◽

Author(s):

Masaya Fujita ◽

Taichi Sakumoto ◽

Kenta Tanatani ◽

HongYang Yu ◽

Kosuke Mori ◽

...

Keyword(s):

Aromatic Compounds ◽

Iron Acquisition ◽

Acquisition System ◽

Iron Acquisition System

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

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Siderophore-Mediated Iron Acquisition Enhances Resistance to Oxidative and Aromatic Compound Stress inCupriavidus necatorJMP134

Applied and Environmental Microbiology ◽

10.1128/aem.01938-18 ◽

2018 ◽

Vol 85 (1) ◽

Cited By ~ 5

Author(s):

Changfu Li ◽

Lingfang Zhu ◽

Damin Pan ◽

Shuyu Li ◽

He Xiao ◽

...

Keyword(s):

Gene Cluster ◽

Aromatic Compound ◽

Stress Resistance ◽

Biofilm Formation ◽

Iron Uptake ◽

Iron Acquisition ◽

Acquisition System ◽

Content Type ◽

Swimming Motility ◽

Iron Acquisition System

ABSTRACTMany bacteria secrete siderophores to enhance iron uptake under iron-restricted conditions. In this study, we found thatCupriavidus necatorJMP134, a well-known aromatic pollutant-degrading bacterium, produces an unknown carboxylate-type siderophore named cupriabactin to overcome iron limitation. Using genome mining, targeted mutagenesis, and biochemical analysis, we discovered an operon containing six open reading frames (cubA–F) in theC. necatorJMP134 genome that encodes proteins required for the biosynthesis and uptake of cupriabactin. As the dominant siderophore ofC. necatorJMP134, cupriabactin promotes the growth ofC. necatorJMP134 under iron-limited conditions via enhanced ferric iron uptake. Furthermore, we demonstrated that the iron concentration-dependent expression of thecuboperon is mediated by the ferric uptake regulator (Fur). Physiological analyses revealed that the cupriabactin-mediated iron acquisition system influences swimming motility, biofilm formation, and resistance to oxidative and aromatic compound stress inC. necatorJMP134. In conclusion, we identified a carboxylate-type siderophore named cupriabactin, which plays important roles in iron scavenging, bacterial motility, biofilm formation, and stress resistance.IMPORTANCESince siderophores have been widely exploited for agricultural, environmental, and medical applications, the identification and characterization of new siderophores from different habitats and organisms will have great beneficial applications. Here, we identified a novel siderophore-producing gene cluster inC. necatorJMP134. This gene cluster produces a previously unknown carboxylate siderophore, cupriabactin. Physiological analyses revealed that the cupriabactin-mediated iron acquisition system influences swimming motility, biofilm formation, and oxidative stress resistance. Most notably, this system also plays important roles in increasing the resistance ofC. necatorJMP134 to stress caused by aromatic compounds, which provide a promising strategy to engineer more efficient approaches to degrade aromatic pollutants.

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Rapid evolution of a bacterial iron acquisition system

Molecular Microbiology ◽

10.1111/mmi.13918 ◽

2018 ◽

Vol 108 (1) ◽

pp. 90-100 ◽

Cited By ~ 10

Author(s):

Anushila Chatterjee ◽

Mark R. O'Brian

Keyword(s):

Iron Acquisition ◽

Rapid Evolution ◽

Acquisition System ◽

Iron Acquisition System

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Regulation of the Expression of Iron-acquisition System Genes in Pathogenic Vibrio Species

YAKUGAKU ZASSHI ◽

10.1248/yakushi.16-00192 ◽

2016 ◽

Vol 136 (11) ◽

pp. 1525-1532 ◽

Cited By ~ 1

Author(s):

Tomotaka Tanabe

Keyword(s):

Iron Acquisition ◽

Acquisition System ◽

Iron Acquisition System

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Transferrin-mediated iron acquisition by pathogenic Neisseria

Biochemical Society Transactions ◽

10.1042/bst0300705 ◽

2002 ◽

Vol 30 (4) ◽

pp. 705-707 ◽

Cited By ~ 6

Author(s):

R. W. Evans ◽

J. S. Oakhill

Keyword(s):

Bacterial Cell ◽

Iron Uptake ◽

Binding Proteins ◽

Current Knowledge ◽

Iron Acquisition ◽

Direct Interaction ◽

Acquisition System ◽

Uptake System ◽

Short Account ◽

Transferrin Binding Proteins

The pathogenic Neisseria have a siderophore-independent iron-uptake system reliant on a direct interaction between the bacterial cell and transferrin. In the meningococcus this uptake system is dependent on two surface-exposed transferrin-binding proteins. This short account will review our current knowledge of the transferrin-mediated iron-acquisition system of pathogenic Neisseria.

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Molecular mechanisms of iron uptake in eukaryotes

Physiological Reviews ◽

10.1152/physrev.1996.76.1.31 ◽

1996 ◽

Vol 76 (1) ◽

pp. 31-47 ◽

Cited By ~ 130

Author(s):

D. M. de Silva ◽

C. C. Askwith ◽

J. Kaplan

Keyword(s):

Iron Uptake ◽

Mammalian Cells ◽

Iron Homeostasis ◽

Molecular Mechanisms ◽

Iron Acquisition ◽

Genetic Disorders ◽

Essential Element ◽

Recent Developments

Iron serves essential functions in both prokaryotes and eukaryotes, and cells have highly specialized mechanisms for acquiring and handling this metal. The primary mechanism by which the concentration of iron in biologic systems is controlled is through the regulation of iron uptake. Although the role of transferrin in mammalian iron homeostasis has been well characterized, the study of genetic disorders of iron metabolism has revealed other, transferrin-independent, mechanisms by which cells can acquire iron. In an attempt to understand how eukaryotic systems take up this essential element, investigators have begun studying the simple eukaryote Saccharomyces cerevisiae. Several genes have been identified and cloned that act in concert to allow iron acquisition from the environment. Some of these genes appear to have functional homologues in human systems. This review focuses on the recent developments in understanding eukaryotic iron uptake with an emphasis on the genetic and molecular characterization of these systems in both cultured mammalian cells and S. cerevisiae. An unexpected connection between iron and copper homeostasis has been revealed by recent genetic studies, which confirm biologic observations made several decades ago.

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Growth characteristics and expression of iron-regulated outer-membrane proteins of chemostat-grown biofilm cells of Pseudomonas aeruginosa

Canadian Journal of Microbiology ◽

10.1139/m91-127 ◽

1991 ◽

Vol 37 (10) ◽

pp. 737-743 ◽

Cited By ~ 8

Author(s):

H. Anwar ◽

J. L. Strap ◽

J. W. Costerton

Keyword(s):

Pseudomonas Aeruginosa ◽

Membrane Proteins ◽

Dilution Rate ◽

Outer Membrane ◽

Iron Uptake ◽

Iron Acquisition ◽

Outer Membrane Proteins ◽

Uptake System ◽

Planktonic Cells

An in vitro chemostat system was used to study the growth and the expression of iron-regulated outer-membrane proteins (IROMPs) by biofilm cells of Pseudomonas aeruginosa cultivated under conditions of iron limitation. The population of the planktonic cells decreased when the dilution rate was increased. At a dilution rate of 0.05 h−1 the populations of planktonic cells of both mucoid and nonmucoid P. aeruginosa were 3 × 109 cells/mL. This value dropped to 5 × 106 cells/mL when the dilution rate was increased to 1.0 h−1. The reverse was observed for the biofilm cells. The number of biofilm cells colonising the silicone tubing increased when the dilution rate was increased. The number of biofilm cells of the mucoid strain at steady state was 2 × 108 cells/cm (length) when the dilution rate was fixed at 0.05 h−1. The figure increased to 8 × 109 cells/cm when the dilution rate was increased to 1.0 h−1. The population of biofilm cells of the nonmucoid strain was 9 × 107 cells/cm (length) when the dilution rate was 0.05 h−1. It increased to 2 × 109 cells/cm when the dilution rate was set at 1.0 h−1. The expression of IROMPs was induced in the biofilm cells of both mucoid and nonmucoid strains when the dilution rates were 0.05 and 0.2 h−1. IROMPs were reduced but still detectable at the dilution rate of 0.5 h−1. However, the expression of IROMPs was repressed when the dilution rate was increased to 1.0 h−1. The data suggest that the biofilm cells of P. aeruginosa switch on the expression of IROMPs to assist iron acquisition when the dilution rate used for the chemostat run is below 0.5 h−1. The high affinity iron uptake system is not required by the biofilm cells when the dilution rate is increased because the trace amount of iron present in the chemostat is sufficient for the growth of adherent biofilm cells. Key words: Pseudomonas aeruginosa, chemostat, iron, outer-membrane proteins, biofilm.

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