Nutritional stress induces exchange of cell material and energetic coupling between bacterial species

Benomar, Saïda; Ranava, David; Cárdenas, Marí­a Luz; Trably, Eric; Rafrafi, Yan; Ducret, Adrien; Hamelin, Jérôme; Lojou, Élisabeth; Steyer, Jean‐Philippe; Giudici‐Orticoni, Marie‐Thérèse

doi:10.1038/ncomms7283

Cited by 143 publications

(141 citation statements)

References 57 publications

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“…Interestingly, membranous structures connect host and symbiont and N. equitans obtains its amino acids from I. hospitalis 49 , which strikingly parallels the observations of our study. Also the recent observation that a shortage of nutrients seems to trigger an exchange of cytoplasmic constituents between cocultured cells of Desulfovibrio vulgaris and Clostridium acetobutylicum 50 corroborates the interpretation that bacteria may commonly establish direct cell-cell connections to counter nutritional stress. Several other examples have been documented, in which bacteria and/or archaea engage in obligate, metabolic interactions 51,52 virtually all of which rely on close, physical associations between interacting partners.…”

Section: Greenmentioning

confidence: 53%

Metabolic cross-feeding via intercellular nanotubes among bacteria

et al. 2015

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Bacteria frequently exchange metabolites by diffusion through the extracellular environment, yet it remains generally unclear whether bacteria can also use cell-cell connections to directly exchange nutrients. Here we address this question by engineering cross-feeding interactions within and between Acinetobacter baylyi and Escherichia coli, in which two distant bacterial species reciprocally exchange essential amino acids. We establish that in a well-mixed environment E. coli, but likely not A. baylyi, can connect to other bacterial cells via membranederived nanotubes and use these to exchange cytoplasmic constituents. Intercellular connections are induced by auxotrophy-causing mutations and cease to establish when amino acids are externally supplied. Electron and fluorescence microscopy reveal a network of nanotubular structures that connects bacterial cells and enables an intercellular transfer of cytoplasmic materials. Together, our results demonstrate that bacteria can use nanotubes to exchange nutrients among connected cells and thus help to distribute metabolic functions within microbial communities.

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Section: Greenmentioning

confidence: 53%

Metabolic cross-feeding via intercellular nanotubes among bacteria

et al. 2015

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“…Cryo-electron microscopy (cryo-EM) images of the M. xanthus vesicle chains show characteristics similar to those we observed for S. oneidensis nanowires using atomic force microscopy and fluorescence microscopy (8,11,12). Recently, tube-like membrane connections have been identified between Desulfovibrio vulgaris and Clostridium acetobutylicum, as well as between Escherichia coli and Acinetobacter baylyi, for the purpose of exchanging cellular materials and cross-feeding between each pair of species (13,14). As membrane extensions and chains of vesicles are observed in increasing numbers of bacterial species, it is becoming clear that these structures are a common mechanism employed by bacteria to interact with each other and their environment.…”

mentioning

confidence: 60%

Regulation of Gene Expression in Shewanella oneidensis MR-1 during Electron Acceptor Limitation and Bacterial Nanowire Formation

Barchinger

Pirbadian

Sambles

et al. 2016

Appl Environ Microbiol

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In limiting oxygen as an electron acceptor, the dissimilatory metal-reducing bacterium Shewanella oneidensis MR-1 rapidly forms nanowires, extensions of its outer membrane containing the cytochromes MtrC and OmcA needed for extracellular electron transfer. RNA sequencing (RNA-Seq) analysis was employed to determine differential gene expression over time from triplicate chemostat cultures that were limited for oxygen. We identified 465 genes with decreased expression and 677 genes with increased expression. The coordinated increased expression of heme biosynthesis, cytochrome maturation, and transport pathways indicates that S. oneidensis MR-1 increases cytochrome production, including the transcription of genes encoding MtrA, MtrC, and OmcA, and transports these decaheme cytochromes across the cytoplasmic membrane during electron acceptor limitation and nanowire formation. In contrast, the expression of the mtrA and mtrC homologs mtrF and mtrD either remains unaffected or decreases under these conditions. The ompW gene, encoding a small outer membrane porin, has 40-fold higher expression during oxygen limitation, and it is proposed that OmpW plays a role in cation transport to maintain electrical neutrality during electron transfer. The genes encoding the anaerobic respiration regulator cyclic AMP receptor protein (CRP) and the extracytoplasmic function sigma factor RpoE are among the transcription factor genes with increased expression. RpoE might function by signaling the initial response to oxygen limitation. Our results show that RpoE activates transcription from promoters upstream of mtrC and omcA. The transcriptome and mutant analyses of S. oneidensis MR-1 nanowire production are consistent with independent regulatory mechanisms for extending the outer membrane into tubular structures and for ensuring the electron transfer function of the nanowires. IMPORTANCEShewanella oneidensis MR-1 has the capacity to transfer electrons to its external surface using extensions of the outer membrane called bacterial nanowires. These bacterial nanowires link the cell's respiratory chain to external surfaces, including oxidized metals important in bioremediation, and explain why S. oneidensis can be utilized as a component of microbial fuel cells, a form of renewable energy. In this work, we use differential gene expression analysis to focus on which genes function to produce the nanowires and promote extracellular electron transfer during oxygen limitation. Among the genes that are expressed at high levels are those encoding cytochrome proteins necessary for electron transfer. Shewanella coordinates the increased expression of regulators, metabolic pathways, and transport pathways to ensure that cytochromes efficiently transfer electrons along the nanowires.

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“…Two mechanisms are conceivable how auxotrophs obtained the AAs they required for growth: metabolites might be exchanged among genotypes via diffusion through the cell-external environment [46–48] or, alternatively, in a contact-dependent manner [49, 50]. Recently it has been described that auxotrophic cells of E .…”

Section: Discussionmentioning

confidence: 99%

Experimental Evolution of Metabolic Dependency in Bacteria

2016

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Bacteria frequently lose biosynthetic genes, thus making them dependent on an environmental uptake of the corresponding metabolite. Despite the ubiquity of this ‘genome streamlining’, it is generally unclear whether the concomitant loss of biosynthetic functions is favored by natural selection or rather caused by random genetic drift. Here we demonstrate experimentally that a loss of metabolic functions is strongly selected for when the corresponding metabolites can be derived from the environment. Serially propagating replicate populations of the bacterium Escherichia coli in amino acid-containing environments revealed that auxotrophic genotypes rapidly evolved in less than 2,000 generations in almost all replicate populations. Moreover, auxotrophs also evolved in environments lacking amino acids–yet to a much lesser extent. Loss of these biosynthetic functions was due to mutations in both structural and regulatory genes. In competition experiments performed in the presence of amino acids, auxotrophic mutants gained a significant fitness advantage over the evolutionary ancestor, suggesting their emergence was selectively favored. Interestingly, auxotrophic mutants derived amino acids not only via an environmental uptake, but also by cross-feeding from coexisting strains. Our results show that adaptive fitness benefits can favor biosynthetic loss-of-function mutants and drive the establishment of intricate metabolic interactions within microbial communities.

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Nutritional stress induces exchange of cell material and energetic coupling between bacterial species

Cited by 143 publications

References 57 publications

Metabolic cross-feeding via intercellular nanotubes among bacteria

Metabolic cross-feeding via intercellular nanotubes among bacteria

Regulation of Gene Expression in Shewanella oneidensis MR-1 during Electron Acceptor Limitation and Bacterial Nanowire Formation

Experimental Evolution of Metabolic Dependency in Bacteria

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