Respiration occurs at different levels: the body, the organ, and the cells. At the cellular level, it is a molecular process that produces a high-energy molecule called adenosine triphosphate (ATP) using the biochemical energy stored in sugars, fatty acids, and other nutrients. Along with the ATP, this process also provides another source of energy to the cell: an electrochemical gradient across the membrane used for a range of processes ranging from the transport of molecules and ions to cell motility.

In order to thrive, cells need to quickly respond to cues from the environment or elsewhere in the cell. A cell must therefore have the ability to increase or decrease cellular respiration and the production of ATP to ensure it has an appropriate supply of energy. In bacteria, the protein complexes responsible for cellular respiration are embedded in the cell membrane. In the past decade, research has suggested that large molecules are arranged in a specific way throughout the bacterial cell, which directly influences how they work.

Alberge et al. tested this idea by studying the localization of a respiratory complex called nitrate reductase—which is important for generating energy in the absence of oxygen—through the introduction of a fluorescent marker tagged to the complex in the cell membrane of a rod-shaped bacterium called Escherichia coli. This allowed the complex to be tracked when the cells were viewed using a microscope. The experiments revealed that the location of the complex varies depending on how much energy the cell requires. For example, when the cells are in an oxygen-poor environment, the nitrate reductase complex moves towards the poles at each end of the bacterial cells. This allows the cells to produce ATP more efficiently through respiration of nitrate. Alberge et al. show that a ‘proton gradient’, caused by positively charged hydrogen ions moving through the cell membrane as the result of respiration, controls where the complexes are located in the membrane.

Alberge et al.'s findings provide experimental support that dynamic localization of respiratory complexes plays an important role in controlling respiration in bacteria. The next challenge will be to identify the genes that influence the distribution of respiratory complexes throughout the cell, which may help to explain how bacterial cells have adapted to specific environments.

Respiration is an essential process for most living organisms. The free energy derived from oxidation of reducing equivalents generated by cell metabolism or taken up from the environment is converted into a protonmotive force (pmf) across a membrane that is used, among many processes, to drive adenosine triphosphate synthesis. Although oxygen is the most common terminal electron acceptor of respiratory chains, prokaryotes can make use of alternative acceptors in anoxic environments, such as nitrogen oxides, elemental sulfur and sulfur oxyanions, organic N-oxides, etc. In eukaryotes, respiration is confined to a specific organelle, the mitochondrion and more specifically to its inner membrane which displays remarkably intricate ultra-structural features that impact the respiratory output (Cogliati et al., 2013). Respiration involves multimeric membrane-embedded oxidative phosphorylation (OXPHOS) complexes which bear several metal cofactors through which electrons are transported. The organization of OXPHOS complexes in the inner mitochondrial membrane has been the subject of intense debate during the last decade after the discovery of supramolecular assemblies by the landmark study of Schägger in 2000 (Schägger and Pfeiffer, 2000), later substantiated by electron microscopy studies (for a review, see Vonck and Schafer, 2009). Plasticity of the almost linear mitochondrial OXPHOS chain is ensured by a dynamic equilibrium between isolated complexes and supramolecular assemblies which is, in turn, influenced by both specific lipids and stabilizing factors (Zhang et al., 2002; Ikeda et al., 2013). Such an equilibrium is likely beneficial for the function of the mitochondrion allowing the cell to respond to cellular and environmental cues. Moreover, the extraordinarily low degradation rate of OXPHOS complexes in mitochondria (Price et al., 2010; Kim et al., 2012; Nelson et al., 2013) reinforces the idea that the dynamic association into supercomplexes adds an effective switch to control electron flows in response to environmental changes (Lapuente-Brun et al., 2013). The flexibility of energy metabolism is also critical for the adaptation of a number of prokaryotes to varying environments (Unden et al., 2014). The utilization of modular OXPHOS chains confers flexibility depending on the available energy source or terminal electron acceptor but also allows modulation of the resulting pmf. So far, the adjustment of respiration to varying environments in prokaryotes is considered to be the result of an intricate transcriptional regulation network that controls the expression of OXPHOS complexes with varying electrogenic capacities.

At the same time, there is cumulative evidence for an elaborate spatial organization of macromolecules in bacterial cells. We thus hypothesized that the OXPHOS process could be regulated through the dynamic subcellular localization of complexes in response to the metabolic demand. Here, we investigate the native localization of a major OXPHOS complex under anoxic conditions, the quinol oxidizing nitrate reductase complex from the gut bacterium Escherichia coli, and its dynamics upon changes in the environment by real-time fluorescence imaging in live cells.

The E. coli nitrate reductase complex is composed of three subunits (NarGHI) and likely organized in a dimer under physiological conditions (Bertero et al., 2003). A di-heme b-type cytochrome subunit, NarI, ensures quinol oxidation and membrane anchoring of the cytoplasmically oriented catalytic dimer, NarGH, where nitrate reduction takes place. The C-terminus of the catalytic subunit NarG protruding from the quaternary structure of the complex was labeled with a green fluorescent protein (GFP). The hybrid gene was expressed under the control of its native promoter activated by FNR and NarL transcriptional factors in response to anaerobiosis and nitrate, respectively and ectopically integrated into the chromosome of the nitrate reductase-deficient strain JCB4023 (Potter et al., 1999). The corresponding fusion was functional as verified by cell growth in nitrate-respiring conditions where a functional nitrate reductase complex is mandatory (Figure 1A). Fractionation studies confirmed the membrane localization of the complex (Figure 1B). The in vitro assay of the functional integrity of the NarG-gfpH catalytic module showed that the activity was only slightly affected by the fusion (Figure 1C). Thus, the GFP-labeled nitrate reductase complex is active in the cytoplasmic membrane.

Figure 1

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The subcellular localization of the anaerobic GFP-labeled OXPHOS complex was characterized by fluorescence microscopy imaging on exponentially growing E. coli cells under nitrate-respiring conditions (Figure 2A). The fluorescence signal was only detected in the cytoplasmic membrane in agreement with fractionation studies. Interestingly, the fluorescence signal appeared as clusters that predominantly concentrated at the cell poles in nearly 80% of the cells (Figure 2B–D). Furthermore, fluorescence clusters concentrate at the cell poles in nitrate-respiring cells independently of the cell length and not at the division septum (Figure 2—figure supplement 1). This suggests that there is no relationship between the position of the clusters and the cell cycle.

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We next evaluated the impact of varying electron routes on the cellular localization of the GFP-labeled nitrate reductase complex. First, fluorescence imaging was performed on exponentially growing cells under oxygen-respiring conditions. Surprisingly, the fluorescence signal was evenly distributed along the cytoplasmic membrane under those conditions (Figure 2A). As compared to nitrate-respiring cells, fewer clusters are present and evenly distributed in oxygen-respiring cells (Figure 2B–D). Second, anaerobic respiration on alternative substrates such as fumarate or trimethylamine N-oxide (TMAO) was tested. It induces a significant polar localization of the fluorescence signal albeit lower than under nitrate-respiring conditions (Figure 3). Fluorescence imaging was eventually analyzed on anoxic fermenting growing cells using glucose as sole carbon source. Strikingly, the fluorescence was evenly distributed as observed under oxygen-respiring conditions (Figure 3). Detailed analysis of the fluorescence signal distribution in all these metabolic conditions revealed that the formation of fluorescent clusters is systematically associated with polar localization (Figure 3—figure supplement 1). Thus, the nitrate reductase complex displays a dynamic subcellular localization in response to the metabolic demand.

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A major difference between the metabolic conditions studied above is the resulting pmf, based on the distinct proton transfer capabilities of the OXPHOS complexes involved. The present finding imparts particular significance to the previous reports that pmf can play a role in protein localization in bacteria (Alcock et al., 2013; Rose et al., 2013). Saliently, the dissipation of the electric component of the pmf, the transmembrane potential (ΔΨ), hampers proper localization of proteins involved in cell division, chromosome segregation or cell shape regulation (Strahl and Hamoen, 2010). However there is, to our knowledge, no report of a protein localization that would be specifically controlled by the other component of the pmf, the proton concentration gradient (ΔpH). To evaluate the participation of the pmf in the subcellular localization of the GFP-labeled nitrate reductase and analyze the contribution of its two components, we first treated nitrate-respiring cells with distinct ionophores. As shown in Figure 4A, the addition of carbonyl cyanide m-chlorophenyl hydrazone (CCCP), a specific proton-ionophore rapidly dissipating the pmf, resulted in a significant reduction of cells displaying polar clusters. Unexpectedly, depolarization of the membrane potential through the addition of the potassium-ionophore valinomycin had no effect, whereas dissipation of ΔpH by the electroneutral anion/OH⁻-exchanger trichlorocarbanilide (TCC) (Ahmed and Booth, 1983) gave rise to significant delocalization of the fluorescent signal. To substantiate the critical role of ΔpH for polar localization, we reasoned that artificial establishment of a proton concentration gradient by the light-driven proton translocation activity of the proteorhodopsin (PR) (Walter et al., 2007) should be sufficient to promote the polar recruitment of the nitrate reductase complex under anoxic fermentative conditions. Indeed, under fermenting conditions, it is considered that the ΔpH is very low as compared to respiring conditions. As shown in Figure 4B, heterologous expression of PR resulted in polar localization of the fluorescence signal in nearly 40% of cells. Thus, we conclude that the proton concentration gradient is a critical cue for polar localization of this anaerobic OXPHOS complex. We next questioned the importance of nitrate reductase activity on its subcellular localization. To this end, a catalytically inactive but stable variant was used. In particular, the H50S substitution in NarG precludes insertion of two metal centers at the active site while x-ray structural analysis of the NarG_H50SHI complex revealed the absence of structural changes at the protein surface (Magalon et al., 1998; Rothery et al., 2010). Under nitrate-respiring conditions, the fluorescence signal associated with the H50S variant is uniformly distributed likely due to its inability to generate a ΔpH (Figure 5A,B and Figure 5—figure supplement 1). In contrast, adding fumarate gives rise to a significant polar localization of the inactive GFP-labeled nitrate reductase complex reinforcing the conclusion that activity of the complex is essential for polar positioning unless a ΔpH is established (Figure 5A,B and Figure 5—figure supplement 1). Interestingly, polar localization requires both the absence of oxygen and the establishment of a proton concentration gradient to which the nitrate reductase complex may contribute fuelling the localization mechanism.

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Bacteria exploit the branched character of their OXPHOS chains to respond to varying environments with a great metabolic and regulatory flexibility (Unden et al 2014). The above-described modification of the localization pattern of the nitrate reductase complex in response to metabolic changes begs the question of its timeframe. First, nitrate-respiring cells were submitted to strong aeration and the fluorescent pattern was followed during the course of the anoxic–oxic transition (Figure 6A). While 80% of the bacterial cells initially displayed a pronounced polar localization of the GFP-labeled nitrate reductase complex, the signal started to change noticeably after 15 min, reaching an almost uniform distribution after one hour of aerobic transition. A similar temporal behavior has been observed under the reverse conditions using aerobically growing cells transferred to anoxic conditions (Figure 6A). In this case, more than 70% of the bacterial cells displayed a polar localization of the fluorescent signal after the transition. Thus, redistribution of the OXPHOS complex triggered by metabolic changes operates on timescales of several tens of minutes. While such timing may reflect the slow diffusion of such large membrane-embedded complexes in the crowded cytoplasmic membrane, we next questioned whether this switch is faster than the changes in nitrate reductase protein content as the result of transcriptional regulation. At first, western-blotting analyses showed nearly unchanged level of GFP-labeled nitrate reductase complex upon anoxic–oxic transition despite the rapid redistribution of the complex in the cytoplasmic membrane (Figure 6—figure supplement 1A). In comparison, an increased level of complex is observed during the oxic–anoxic transition as the result of FNR-mediated regulation. To substantiate these observations, localization upshift experiments were reproduced in cells pre-treated with chloramphenicol (Cm), a protein synthesis inhibitor (Figure 6B and Figure 6—figure supplement 1B). During the anoxic–oxic transition, Cm had nearly no impact on the delocalization kinetics with only slight diminution of the nitrate reductase content. Interestingly, during the oxic–anoxic transition, the fluorescence signal remains uniformly distributed with a concomitant decrease of nitrate reductase content. To rule out any impact on the yielded pmf value under those conditions, the oxic–anoxic upshift experiment was reproduced in presence of PR. As shown in Figure 6B, establishment of a ΔpH was not sufficient to promote polar localization. Altogether, these results support the idea that induction of the expression of at least one gene during the oxic–anoxic transition promotes polar localization of the nitrate reductase complex.

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The GFP-labeled nitrate reductase complex displays a dynamic localization pattern leading to the formation of discrete domains in the cytoplasmic membrane. At first, we reasoned that distinct subcellular localization may influence the intrinsic activity of the OXPHOS complex. The activity of the GFP-labeled complex was therefore assessed in membrane vesicles issued from cells that displayed either an even distribution (oxygen-respiring condition) or a strong polar enrichment (nitrate-respiring condition) of the complex. As shown in Figure 7A, we found no significant variation in the specific activities indicating that subcellular localization has no influence on the intrinsic activity of the OXPHOS complex.

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We next hypothesized that the formation of discrete domains through the polar recruitment of the nitrate reductase may influence the overall yield of the electron transport chain. To evaluate the impact of polar localization on the electron flux from primary dehydrogenases to GFP-labeled nitrate reductase, it was essential to ensure an identical composition of the cytoplasmic membrane in terms of OXPHOS complexes. To account for this issue, we used fermenting-growing cells expressing or not PR which have an identical OXPHOS proteome but display distinct localization patterns of the GFP-labeled complex (Figure 4B). Upon addition of nitrate in the growth medium, electron flux through the nitrate reductase complex could be kinetically resolved by quantifying nitrite in the cell culture. As seen in Figure 7B, within the first 10 min following nitrate addition, the rate of nitrite production is significantly higher in PR-expressing cells than in control cells, indicating a direct correlation between subcellular localization and electron flux through the nitrate reductase complex. After one hour, the level of nitrite produced is nearly two orders of magnitude higher in PR-expressing cells. We conclude that environmental conditions (anaerobiosis and a ΔpH) promoting polar clustering of the nitrate reductase complex result in a higher efficiency of the associated respiratory chains.

In the past decade, the emerging field of bacterial cell biology has underscored the fact that dynamic subcellular localization is intimately linked to the biological function allowing control of fundamental processes, such as cell division, virulence, motility, or signal transduction (for reviews, see Kiekebusch and Thanbichler, 2014; Laloux and Jacobs-Wagner, 2014; Nevo-Dinur et al., 2012; Shapiro et al., 2009). Similarly, we have shown that the nitrate reductase respiratory complex is submitted to a spatiotemporal regulation in response to environmental conditions which, in turns, potentiates the electron flux through the associated respiratory chain. Nitrate respiration in E. coli is thus controlled by specific subcellular localization of its terminal reductase. Segregation of respiratory complexes within the cytoplasmic membrane has also been reported for components of bacterial aerobic chains (Johnson et al., 2004; Lenn et al., 2008; Werner et al., 2009; Rexroth et al., 2011; Llorente-Garcia et al., 2014). The actual view is that functional consequences are associated with a high level of structural organization of respiratory complexes within bioenergetic membranes (for a review, see Genova and Lenaz, 2014). Interestingly enough, recent studies have evidenced the existence of functional microdomains in bacterial membranes organizing a specific subset of proteins in space and time surmising a gain-of-function (Lopez and Kolter, 2010). In the same line of thought, it has recently been shown that clustering of multiple enzymes belonging to the same metabolic pathway into agglomerates accelerates the processing of intermediates (Castellana et al., 2014). Clearly, several alternatives can be found for the reported enhanced electron flux in the nitrate reductase-associated respiratory chains such as physical association into supercomplexes or segregating respiratory complexes into microdomains. In both cases, one would hypothesize that the probability of the quinone molecules to encounter the nitrate reductase is higher. Evidences have been provided for such quinone channeling within supercomplexes while the exact mechanism of channeling is not yet understood (for a review, see Genova and Lenaz, 2014).

By providing the first evidence for a spatiotemporal regulation of a respiratory complex in response to environmental conditions, this work establishes a basis for a deeper analysis on how environmental signals are translated into subcellular localization of respiratory complexes to adjust the respiration output.

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Author details

1. François Alberge

   Laboratoire de Chimie Bactérienne UMR7283, Institut de Microbiologie de la Méditerranée, Centre national de la recherche scientifique, Aix Marseille Université, Marseille, France

   Contribution

   FA, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

2. Leon Espinosa

   Laboratoire de Chimie Bactérienne UMR7283, Institut de Microbiologie de la Méditerranée, Centre national de la recherche scientifique, Aix Marseille Université, Marseille, France

   Contribution

   LE, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

3. Farida Seduk

   Laboratoire de Chimie Bactérienne UMR7283, Institut de Microbiologie de la Méditerranée, Centre national de la recherche scientifique, Aix Marseille Université, Marseille, France

   Contribution

   FS, Conception and design, Acquisition of data, Analysis and interpretation of data

   Competing interests

   The authors declare that no competing interests exist.

4. Léa Sylvi

   Laboratoire de Chimie Bactérienne UMR7283, Institut de Microbiologie de la Méditerranée, Centre national de la recherche scientifique, Aix Marseille Université, Marseille, France

   Present address

   MIO, Aix Marseille Université, Marseille, France

   Contribution

   LS, Conception and design, Acquisition of data, Analysis and interpretation of data

   Competing interests

   The authors declare that no competing interests exist.

5. René Toci

   Laboratoire de Chimie Bactérienne UMR7283, Institut de Microbiologie de la Méditerranée, Centre national de la recherche scientifique, Aix Marseille Université, Marseille, France

   Contribution

   RT, Conception and design, Acquisition of data, Analysis and interpretation of data

   Competing interests

   The authors declare that no competing interests exist.

6. Anne Walburger

   Laboratoire de Chimie Bactérienne UMR7283, Institut de Microbiologie de la Méditerranée, Centre national de la recherche scientifique, Aix Marseille Université, Marseille, France

   Contribution

   AW, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

7. Axel Magalon

   Laboratoire de Chimie Bactérienne UMR7283, Institut de Microbiologie de la Méditerranée, Centre national de la recherche scientifique, Aix Marseille Université, Marseille, France

   Contribution

   AM, Conception and design, Analysis and interpretation of data, Drafting or revising the article

   For correspondence

   magalon@imm.cnrs.fr

   Competing interests

   The authors declare that no competing interests exist.

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