TonB-Dependent Transporters in Sphingomonads: Unraveling Their Distribution and Function in Environmental Adaptation

Samantarrai, Devyani; Sagar, Annapoorni Lakshman; Gudla, Ramurthy; Siddavattam, Dayananda

doi:10.3390/microorganisms8030359

Cited by 20 publications

(17 citation statements)

References 71 publications

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“…16% 12 . Since the Sphingomonad strains have a large number of TBDR genes (from 39 to 153), they may play important roles not only in iron acquisition but also in other functions 13 , 54 . Five of the ten strains investigated showed the presence of TBDR-like genes, which showed 49 – 54% amino acid sequence identity with fiuA .…”

Section: Discussionmentioning

confidence: 99%

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

Fujita

Sakumoto

Tanatani

et al. 2020

Sci Rep

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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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Section: Discussionmentioning

confidence: 99%

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

Fujita

Sakumoto

Tanatani

et al. 2020

Sci Rep

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“…16% 14 . Since the Sphingomonad strains have a large number of TBDR genes (from 39 to 153), they may play important roles not only in iron acquisition but also in other functions 15,49 . Five of the ten strains investigated showed the presence of TBDR-like genes, which showed 49-54% amino acid sequence identity with fiuA .…”

Section: Resultsmentioning

confidence: 99%

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

Fujita

Sakumoto

Tanatani

et al. 2020

Preprint

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23Iron, an essential element for all organisms, acts as a cofactor of enzymes in bacterial 24 degradation of recalcitrant aromatic compounds. The bacterial family, Sphingomonadaceae 25 comprises various degraders of recalcitrant aromatic compounds; however, little is known 26 about their iron acquisition system. Here, we investigated the iron acquisition system in a 27 model bacterium capable of degrading lignin-derived aromatics, Sphingobium sp. strain 28 SYK-6. Analyses of SYK-6 mutants revealed that FiuA (SLG_34550), a TonB-dependent 29 receptor (TBDR), was the major outer membrane iron transporter. Three other TBDRs 30 encoded by SLG_04340, SLG_04380, and SLG_10860 also participated in iron uptake, and 31 tonB2 (SLG_34550), one of the six tonB comprising the Ton complex which enables 32 TBDR-mediated transport was critical for iron uptake. The ferrous iron transporter FeoB 33 (SLG_36840) played an important role in iron uptake across the inner membrane. The 34 promoter activities of most of the iron uptake genes were induced under iron-limited 35 conditions, and their regulation is controlled by SLG_29410 encoding the ferric uptake 36 regulator, Fur. Although feoB, among all the iron uptake genes identified is highly conserved 37 in Sphingomonad strains, the outer membrane transporters seem to be diversified. Elucidation 38 of the iron acquisition system promises better understanding of the bacterial degradation 39 mechanisms of aromatic compounds.40 41 42Iron is an essential nutrient utilised as a cofactor for enzymes that control various life 43 phenomena such as respiration, dissimilation, and stress response 1 . Iron exists mainly in 44 ferrous and ferric forms. Ferrous iron is soluble and highly bioavailable; however, the 45 predominant form of iron in the environment is an insoluble ferric form 2 . Ferric iron in soil 46 and water is solubilised by forming complexes with organic ligands such as siderophores, 47 humic acid, lipids, proteins, and polysaccharides 3,4 . Many bacteria secrete specific 48 high-affinity siderophores which form complexes with ferric iron and then uptake these 49 ferric-siderophore complexes to enhance iron acquisition over competitors [5][6][7] . Besides, 50 pathogenic bacteria can acquire haem and transferrin specifically from their host cells 8,9 . 51 Gram-negative bacteria need to transport iron through both the outer and inner 52 membranes. TonB-dependent receptors (TBDRs) mediate transport of ferric complexes (e.g. 53 siderophore, haem, and transferrin) across the outer membrane 1,10,11 . TBDRs utilize energy 54 derived from the proton motive force transmitted by TonB-ExbB-ExbD complex (Ton 55 complex) localised in the inner membrane (Ton system) 12 . Beside siderophores, the Ton 56 system is involved in the uptake of vitamin B12, saccharide, aromatic compounds, and metals 57 such as nickel, copper, and lanthanoid [13][14][15][16][17][18] . The uptake of the ferric complex across the inner 58 membrane is mainly achieved by ATP-binding cassette (ABC) transporters 11...

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“…The plausible biological reasoning to answer this emerges from the fact that bacterial species have an abundance of transporters such as outer membrane-associated β-barrel-containing proteins or porins, which may allow for the transport of biotic/xenobiotic molecules, and thus will facilitate their metabolism by the bacteria. One such example is the TonB-dependent transport system where the outer membrane-associated TonB-dependent transporter (TBDT), and other similar ATP-driven influx transporters, facilitate the active transport and subsequent metabolism of xenobiotic compounds by bacterial cells ( Jindal et al., 2019 ; Samantarrai et al., 2020 ). The experimental supports to these processes are provided by a few recent studies that showed the metabolism of different biotic/xenobiotic molecules such as BaP, glycoholic acid, cholesterol, glycerol, azo dyes, arginine, triglyceride lipids, propylene glycol, palmitic acid, alpha-tocopherol, uric acid, lactic acid, ethanol amine, and linolenic acid on their incubation with the bacterial species of the skin microbiome ( Sowada et al., 2014 ; Stingley et al., 2010 ; Timm et al., 2020 ).…”

Section: Discussionmentioning

confidence: 99%

SkinBug: an artificial intelligence approach to predict human skin microbiome-mediated metabolism of biotics and xenobiotics

et al. 2021

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Summary In addition to being pivotal for the host health, the skin microbiome possesses a large reservoir of metabolic enzymes, which can metabolize molecules (cosmetics, medicines, pollutants, etc.) that form a major part of the skin exposome. Therefore, to predict the complete metabolism of any molecule by skin microbiome, a curated database of metabolic enzymes (1,094,153), reactions, and substrates from ∼900 bacterial species from 19 different skin sites were used to develop “SkinBug.” It integrates machine learning, neural networks, and chemoinformatics methods, and displays a multiclass multilabel accuracy of up to 82.4% and binary accuracy of up to 90.0%. SkinBug predicts all possible metabolic reactions and associated enzymes, reaction centers, skin microbiome species harboring the enzyme, and the respective skin sites. Thus, SkinBug will be an indispensable tool to predict xenobiotic/biotic metabolism by skin microbiome and will find applications in exposome and microbiome studies, dermatology, and skin cancer research.

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TonB-Dependent Transporters in Sphingomonads: Unraveling Their Distribution and Function in Environmental Adaptation

Cited by 20 publications

References 71 publications

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

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

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

SkinBug: an artificial intelligence approach to predict human skin microbiome-mediated metabolism of biotics and xenobiotics

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