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The Paracoccus denitrificans NarK-like nitrate and nitrite transporters-probing nitrate uptake and nitrate/nitrite exchange mechanisms.

ABSTRACT: Nitrate and nitrite transport across biological membranes is often facilitated by protein transporters that are members of the major facilitator superfamily. Paracoccus denitrificans contains an unusual arrangement whereby two of these transporters, NarK1 and NarK2, are fused into a single protein, NarK, which delivers nitrate to the respiratory nitrate reductase and transfers the product, nitrite, to the periplasm. Our complementation studies, using a mutant lacking the nitrate/proton symporter NasA from the assimilatory nitrate reductase pathway, support that NarK1 functions as a nitrate/proton symporter while NarK2 is a nitrate/nitrite antiporter. Through the same experimental system, we find that Escherichia coli NarK and NarU can complement deletions in both narK and nasA in P. denitrificans, suggesting that, while these proteins are most likely nitrate/nitrite antiporters, they can also act in the net uptake of nitrate. Finally, we argue that primary sequence analysis and structural modelling do not readily explain why NasA, NarK1 and NarK2, as well as other transporters from this protein family, have such different functions, ranging from net nitrate uptake to nitrate/nitrite exchange.

SUBMITTER: Goddard AD

PROVIDER: S-EPMC5217062 | biostudies-literature | 2017 Jan

REPOSITORIES: biostudies-literature

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The Paracoccus denitrificans NarK-like nitrate and nitrite transporters-probing nitrate uptake and nitrate/nitrite exchange mechanisms.

Goddard Alan D AD Bali Shilpa S Mavridou Despoina A I DA Luque-Almagro Victor M VM Gates Andrew J AJ Dolores Roldán M M Newstead Simon S Richardson David J DJ Ferguson Stuart J SJ

Molecular microbiology 20161027 1

Nitrate and nitrite transport across biological membranes is often facilitated by protein transporters that are members of the major facilitator superfamily. Paracoccus denitrificans contains an unusual arrangement whereby two of these transporters, NarK1 and NarK2, are fused into a single protein, NarK, which delivers nitrate to the respiratory nitrate reductase and transfers the product, nitrite, to the periplasm. Our complementation studies, using a mutant lacking the nitrate/proton symporter ...[more]

PMID: 27696579

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Project description:Paracoccus denitrificans is a valuable model organism due to its versatile respiration capability and bioenergetic flexibility, both of which are critical to its survival in different environments. Quorum sensing (QS) plays a crucial role in the regulation of many cell functions; however, whether QS systems play a role in P. denitrificans is unknown. In this study, we demonstrated that iron uptake systems in P. denitrificans were directly regulated by a newly identified QS system. Genes coding for TonB-dependent systems, which transport chelated iron, were transcribed at higher levels in the QS-defective mutants. In contrast, genes coding for the Fbp system, which is TonB independent and transports unchelated ferric iron, were downregulated in the mutants. In brief, QS in P. denitrificans triggers a switch in iron uptake from TonB-dependent to TonB-independent transport during biofilm formation as higher concentrations of iron accumulate in the exopolysaccharide (EPS). Switching from TonB-dependent iron uptake systems to TonB-independent systems not only prevents cells from absorbing excess iron but also conserves energy. Our data suggest that iron uptake strategies are directly regulated by QS in Paracoccus denitrificans to support their survival in available ecological niches.IMPORTANCE As iron is an important trace metal for most organisms, its absorption is highly regulated. Fur has been reported as a prevalent regulator of iron acquisition. In addition, there is a relationship between QS and iron acquisition in pathogenic microbes. However, there have been few studies on the iron uptake strategies of nonpathogenic bacteria. In this study, we demonstrated that iron uptake systems in Paracoccus denitrificans PD1222 were regulated by a newly identified PdeR/PdeI QS system during biofilm formation, and we put forward a hypothesis that QS-dependent iron uptake systems benefit the stability of biofilms. This report elaborates the correlation among QS, iron uptake, and biofilm formation and thus contributes to an understanding of the ecological behavior of environmental bacteria.

Dataset Information

The Paracoccus denitrificans NarK-like nitrate and nitrite transporters-probing nitrate uptake and nitrate/nitrite exchange mechanisms.

Publications

The Paracoccus denitrificans NarK-like nitrate and nitrite transporters-probing nitrate uptake and nitrate/nitrite exchange mechanisms.

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