Dynamics of the Escherichia coli proteome in response to nitrogen starvation and entry into the stationary phase

Sanchuki, Heloisa Bruna Soligo; Gravina, Fernanda Sbaraini; Rodrigues, Thiago E.; Gerhardt, Edileusa C. M.; Pedrosa, F. O.; Souza, Emanuel Maltempi de; Raittz, Roberto Tadeu; Valdameri, Gláucio; Souza, Gustavo; Huergo, Luciano F.

doi:10.1016/j.bbapap.2016.12.002

Cited by 19 publications

(9 citation statements)

References 62 publications

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“…The small (6.5 kDa) ribosome modulation factor (RMF) is only expressed in gammaproteobacteria but not found in other bacteria (Ueta et al, 2008) (Table 1). RMF is typically produced under nutrient starvation and stress conditions, and more recently it was observed that RMF expression is induced under nitrogen limitation in E. coli (Sanchuki et al, 2017) and under anoxic conditions in Pseudomonas aeruginosa (P. aeruginosa) (Williamson et al, 2012). Upon replenishment with fresh medium, the rmf transcript is rapidly degraded (Aiso et al, 2005).…”

Section: Hibernation Of Translation In Gammaproteobacteriamentioning

confidence: 99%

“…Chloroplast PSRP1 is translated as a precursor with an N-terminal chloroplast transit peptide (light green, cpTP) which is cleaved off upon successful import into the organelle. Yoshida et al, 2002Yoshida et al, , 2004Aiso et al, 2005;Ueta et al, 2008;Williamson et al, 2012;Sanchuki et al, 2017;Beckert et al, 2018 100S during starvation HPFshort No 100S ribosome formation Maki et al, 2000;Ueta et al, 2005Ueta et al, , 2008Ueta et al, , 2013Beckert et al, 2018 70S stabilization pY/YfiA Ribosome degradation Agafonov et al, 1999Agafonov et al, , 2001Agafonov and Spirin 2004;Maki et al, 2000;Vila-Sanjurjo et al, 2004;Sato et al, 2009;Di Pietro et al, Coe et al, 1988;Byrne and Taylor, 1996;Jiang et al, 2007;Häuser et al, 2012;Rorbach et al, 2012;Wanschers et al, 2012;Fung et al, 2013;Li et al, 2015SRA Non-essential Izutsu et al, 2001a Johnson et al, 1990;Sharma et al, 2007;Sharma et al, 2010;Ahmed et al, 2017;Bieri et al, 2017;Graf et al, 2017a,b;Boerema et al, also observed that their hibernating 100S ribosomes of E. coli frequently contained deacylated tRNAs. This matches well with previous reports that uncharged tRNAs accumulate at high levels in starving cells (Hauryliuk et al, 2015) and it suggests that the binding of deacylated tRNAs may la...…”

Section: Hibernation Of Translation In Gammaproteobacteriamentioning

confidence: 99%

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The conserved theme of ribosome hibernation: from bacteria to chloroplasts of plants

Trösch

Willmund

2019

Biological Chemistry

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Cells are highly adaptive systems that respond and adapt to changing environmental conditions such as temperature fluctuations or altered nutrient availability. Such acclimation processes involve reprogramming of the cellular gene expression profile, tuning of protein synthesis, remodeling of metabolic pathways and morphological changes of the cell shape. Nutrient starvation can lead to limited energy supply and consequently, remodeling of protein synthesis is one of the key steps of regulation since the translation of the genetic code into functional polypeptides may consume up to 40% of a cell’s energy during proliferation. In eukaryotic cells, downregulation of protein synthesis during stress is mainly mediated by modification of the translation initiation factors. Prokaryotic cells suppress protein synthesis by the active formation of dimeric so-called ‘hibernating’ 100S ribosome complexes. Such a transition involves a number of proteins which are found in various forms in prokaryotes but also in chloroplasts of plants. Here, we review the current understanding of these hibernation factors and elaborate conserved principles which are shared between species.

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Section: Hibernation Of Translation In Gammaproteobacteriamentioning

confidence: 99%

Section: Hibernation Of Translation In Gammaproteobacteriamentioning

confidence: 99%

The conserved theme of ribosome hibernation: from bacteria to chloroplasts of plants

Trösch

Willmund

2019

Biological Chemistry

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“…Overall, the Krebs-Henseleit/AST pathways release ammonia and fumarate very similar to the aspartase reaction. The latter pathway for ammonia assimilation appears to be of significance in particular in late exponential growth (Sanchuki et al, 2017). The bacteria excreted C 4 -dicarboxylates in nearly equimolar levels to the consumed L-aspartate in a DcuA-dependent manner.…”

Section: Dcua Serves As a N-shuttle (L-aspartate/fumarate Antiport) Dmentioning

confidence: 99%

DcuA of aerobically grown Escherichia coli serves as a nitrogen shuttle (L‐aspartate/fumarate) for nitrogen uptake

Strecker

Schubert

Zedler

et al. 2018

Molecular Microbiology

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DcuA of Escherichia coli is known as an alternative C -dicarboxylate transporter for the main anaerobic C -dicarboxylate transporter DcuB. Since dcuA is expressed constitutively under aerobic and anaerobic conditions, DcuA was suggested to serve aerobically as a backup for the aerobic (DctA) transporter, or for the anabolic uptake of C -dicarboxylates. In this work, it is shown that DcuA is required for aerobic growth with L-aspartate as a nitrogen source, whereas for growth with L-aspartate as a carbon source, DctA was needed. Strains with DcuA catalyzed L-aspartate and C -dicarboxylate uptake (like DctA), or an L-aspartate/C -dicarboxylate antiport (unlike DctA). DcuA preferred L-aspartate to succinate in transport (K = 43 and 844 µM, respectively), whereas DctA has higher affinity for C -dicarboxylates like succinate compared to L-aspartate. When L-aspartate was supplied as the sole nitrogen source together with glycerol as the carbon source, L-aspartate was taken up by the bacteria and fumarate (or L-malate) was excreted in equimolar amounts. Both reactions depended on DcuA. L-Aspartate was taken up in amounts required for nitrogen metabolism but not for carbon metabolism. Therefore, DcuA catalyzes an L-aspartate/C -dicarboxylate antiport serving as a nitrogen shuttle for nitrogen supply without net carbon supply.

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“…Consistent with this observation, the levels of HPF long or RMF are substantially elevated in a murine pneumonia model (Michalik et al 2017), in starved cells (Aiso et al 2005; Sanchuki et al 2017), in biofilms (Williamson et al 2012), and in non-replicating persisters (Tkachenko et al 2017). Moreover, HPF long reduces translational efficiency of a subset of genes in vivo (Basu and Yap 2016; Hood et al 2016) and in cell-free translation assays (Basu and Yap 2016; Ueta et al 2008, 2013), presumably because 70S dimerization titrates functional ribosomes away from translational initiation.…”

Section: Functional Consequences Of the Loss Of 100s Ribosomesmentioning

confidence: 82%

“…In general, the phenotypes described above are manifested during slow growth, such as in aging and dormant cells, and intracellular growth inside the host cells, which are normally characterized by metabolic arrest and translational dormancy that restrict energy consumption (Dai et al 2016 ). Consistent with this observation, the levels of HPF long or RMF are substantially elevated in a murine pneumonia model (Michalik et al 2017 ), in starved cells (Aiso et al 2005 ; Sanchuki et al 2017 ), in biofilms (Williamson et al 2012 ), and in non-replicating persisters (Tkachenko et al 2017 ). Moreover, HPF long reduces translational efficiency of a subset of genes in vivo (Basu and Yap 2016 ; Hood et al 2016 ) and in cell-free translation assays (Basu and Yap 2016 ; Ueta et al 2008 , 2013 ), presumably because 70S dimerization titrates functional ribosomes away from translational initiation.…”

Section: Functional Consequences Of the Loss Of 100s Ribosomesmentioning

confidence: 82%

Survival of the drowsiest: the hibernating 100S ribosome in bacterial stress management

Gohara

Yap

2017

Curr Genet

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In response to nutrient deprivation and environmental insults, bacteria conjoin two copies of non-translating 70S ribosomes that form the translationally inactive 100S dimer. This widespread phenomenon is believed to prevent ribosome turnover and serves as a reservoir that, when conditions become favorable, allows the hibernating ribosomes to be disassembled and recycled for translation. New structural studies have revealed two distinct mechanisms for dimerizing 70S ribosomes, but the molecular basis of the disassembly process is still in its infancy. Many details regarding the sequence of dimerization-dissociation events with respect to the binding and departure of the hibernation factor and its antagonizing disassembly factor remain unclear.

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Dynamics of the Escherichia coli proteome in response to nitrogen starvation and entry into the stationary phase

Cited by 19 publications

References 62 publications

The conserved theme of ribosome hibernation: from bacteria to chloroplasts of plants

The conserved theme of ribosome hibernation: from bacteria to chloroplasts of plants

DcuA of aerobically grown Escherichia coli serves as a nitrogen shuttle (L‐aspartate/fumarate) for nitrogen uptake

Survival of the drowsiest: the hibernating 100S ribosome in bacterial stress management

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