Abstract
In a natural habitat, microbes respond to alterations in the amounts of nutrients or to stresses such as osmotic stress and stresses caused by low or high pH, salt, heat, and antibiotics by changing their mode for proliferation or survival. Similarly, Escherichia coli cells in a test tube change the growth mode according to environmental conditions when they enter a stationary phase. Until a sufficient supply of nutrients, the organism survives under such stressful and nutrient-limited conditions by altering gene expression to be more protective against such conditions. The definite trigger of the onset of stationary phase is still unclear, but several lines of evidence indicate that the regulation mechanism is very complicated and involves several transcriptional factors including alternative sigma factors, σE and σS. In addition, E. coli cells behave as a community of species and give rise to programmed cell death (PCD) for ensuring survival by controlling the cell number and supplying nutrients to sibling cells in long-term stationary phase (LTSP). The main PCD is probably performed by σE in E. coli. In this chapter, physiological functions of σE and PCD are introduced and reviewed and their possible involvement in survival mechanisms in stationary phase, especially LTSP, is shown.
Keywords
- survival mechanism
- envelop stress
- σE
- programmed cell death
- long-term stationary phase
1. Introduction
1.1. Brief introduction of σE
Living
1.2. Brief introduction of PCD
PCD is conserved for all genetically encoded processes that lead to cell suicide. This conceptual word was first proposed in 1964 [5]. PCD that is observed in development, aging, and pathology in eukaryotic multicellular organisms is classified into three categories based on morphological characteristics such as apoptosis, autophagy, and necrosis. Among these, apoptosis, first described in 1972 [6], is the most well-characterized PCD. The morphological manifestations associated with apoptosis include chromatin condensation, chromosomal DNA fragmentation, membrane blebbing, cell shrinkage, and disassembly of the cell into membrane-enclosed vesicles. Apoptosis is highly regulated, and proteases called caspases play key roles in the induction of DNA fragmentation in the activation cascade [7]. Autophagy is the process by which a vesicle called an autophagosome is constructed for atrophy of the nucleus but with no DNA fragmentation [7]. Necrosis is triggered by activation of various receptors for loss of cell membrane integrity and uncontrollable release of intracellular contents into the extracellular space [7]. The physiological importance of these PCDs in the development of an animal has been well defined. For example, during embryonic development, the earliest form of the human hand resembles a paddle due to the elimination of excess cells by apoptosis. PCD mechanisms are also responsible for the homeostasis of multicellular organisms by the elimination of damaged cells that may become a source of cancer cells in the body.
It was thought that PCD only exists in eukaryotic cells, but several scientists have considered the possibility of the existence of bacterial PCD resembling eukaryotic PCD mechanisms. Indeed, a growing body of evidence has shown that PCD is indispensable for bacterial development and is closely associated with bacterial survival mechanisms [8, 9]. Bacterial communities utilize PCD for survival of their population when suffering from oxidative stress, nutrient deprivation, phage infections, or other problems. The cell survival mechanism is a response to stresses outside cells and inside cells, but excessive damage turns on the PCD mechanism of some cells to help sibling cells. In the development processes of bacteria, PCD provides nutrients to sibling cells, releases components, and promotes special aspects. Indeed, biofilm formation, sporulation, and other multiple cell-like developments have been shown to bear PCD mechanisms in these processes. In biofilm development, cell death and lysis are required for the release of genomic DNA (known as extracellular DNA), which becomes incorporated into the biofilm matrix and serves as an adherence molecule [10]. For the development of sporulation, sporulating cells produce a killing factor for nonsporulating cells, from which released nutrients support sporulation. Moreover, the mother cell in the sporulating population undergoes PCD to release the mature spore via its autolysis [11]. As other mechanisms,
Many bacterial PCDs are induced through the toxin-antitoxin (TA) system. Five types of TA systems have been found and characterized [9, 12]. Type I has an antisense RNA that pairs with its corresponding toxin mRNA. The difference in transcription between toxin RNA and antitoxin RNA controls the toxin activity. Type II has a protein antitoxin that detoxifies its corresponding toxin protein by their protein-protein interaction. This type of TA system is most abundant. Type III has an antitoxin RNA that interacts directly with the target toxin protein to form an antitoxin RNA-toxin inactive complex. Type IV has a protein antitoxin that stabilizes the target of the toxin by direct binding. Type V has an endoribonuclease that cleaves the target toxin mRNA. These TA systems play important roles in several cellular processes such as plasmid stabilization, formation of persistent cells, peptidoglycan synthesis, resistance to bacteriophages and antibiotics, and inhibition of macromolecule and biofilm formation [9, 12]. PCD via a TA system is executed by the role of toxin proteins.
It has been suggested that the bacterial strategy for survival against DNA damage resembles the PCD mechanisms in eukaryotes [13]. The PCD mechanisms characterized in both prokaryotic and eukaryotic cells indicate that DNA damage leads to cell death when the damage is irreparable. Bayles reported that the death pathway also leads to apoptosis-like processes or autolysis [13]. The similarity of cell death systems in eukaryotes and bacteria suggests that the common origin of this system is derived from endosymbiotic bacteria [9]. Therefore, PCD is a basic mechanism for organisms in all kingdoms for the maintenance of communities, and this system has been acquired at a very early stage of appearance of life on earth. In Section 3, we summarize PCDs in
1.3. Brief introduction of LTSP
In nutrient-sufficient media in the laboratory,
What factors can lead
2. Functions of σE
2.1. Mechanisms of membrane stress responses for σE activation
Bacteria have mechanisms for rapid responses to environmental stresses, especially on the envelope because cell structure is maintained by integrity of the membrane. There have been many studies on membrane stress responses. In Gram-negative bacteria, such responses are known as envelope stress responses (ESRs). There are five known ESRs, Cpx, σE, Bae, Rcs, and Psp ESRs, that are induced by a variety of envelope stresses and alter the expression of adaptive functions to modify the envelope, rid cells of a toxic entity, and/or repair substantial damage [3]. Of these ESRs, σE ESR, a subset first found in
These dual molecular signals (unfolded OMPs and LPS) are key factors for the σE ESR to sense outer membrane stresses [29]. For cell formation, OMPs and LPS are transported from the cytoplasm to the outer membrane in
This kind of proteolytic signal transduction and regulator-activating mechanism provides distinctive features for σE regulon as a transient expression. In the σE ESR, the initial signal-sensing cleavage of RseA is a rate-limiting step but the degradation of cytoplasmically fragmented RseA by AAA+ proteinase is relatively fast. Whereas, RseA is in excess over σE under normal conditions and the expression level of
2.2. σE regulon genes
Activated σE forms a holo-RNA polymerase with the core RNA polymerase complex to initiate transcription by recognizing consensus sequences located upstream from coding genes called promoters. Several experiments have been carried out in
3. σE-dependent PCD
3.1. PCD in E. coli
PCD in
An SOS response-mediated PCD pathway was recently identified in
In addition to DNA damage, envelope damage has been shown to be a trigger of PCD in
3.2. Mechanism of σE-dependent PCD
At the early stationary phase,
The level of PpiD is greatly reduced in σE-activated cells, though its regulation mechanism is unknown [68]. PpiD is a peptidyl-prolyl
As shown in the model in Figure 4, when cells are exposed to some stresses as signals, mainly oxidative stress [19, 70], unfolded proteins accumulate in the outer membrane or periplasmic space, in turn causing the elevation of active σE in the cytoplasm. Active σE induces the expression of sRNAs, leading to the reduction of OMPs including Lpp. Furthermore, the reduction of PpiD via active σE enhances the disintegration of OMPs, resulting in collapse of the integrity of the outer membrane and finally lysis of cells.
3.3. Function of σE-dependent PCD
Cell lysis in
The trigger for σE-dependent cell lysis seems to be not only oxidative stress but also other stresses. The proposed signal transduction cascade for active σE [28] indicates the possibility that extracellular stress evokes σE-dependent cell lysis. Indeed, a disrupted mutation of
As shown in Figure 4, active σE determines the direction to either the repair or cell lysis pathway, presumably reflecting the level of damage of OMPs. If only a few OMPs are damaged, the number of active σE molecules may be not enough to express sRNAs such as
σE-dependent cell lysis seems to eliminate some of the VBNC cells that have been damaged by some kinds of stress. The amount of cell lysis increases in parallel with increase in VBNC cells in the stationary phase, and most of the lysis was suppressed by enhanced expression of
Taken together, the findings have shown that
4. Contribution of PCD for LTSP
4.1. Survival mechanisms in LTSP
In the LTSP,
Using the
The mechanism of GASP acquisition has been investigated and two interesting aspects have been shown. One is the reproducibility of GASP mutants and the other is a relatively high mutation rate in the LTSP. Since the speed of cell proliferation is very low in the LTSP, beneficial mutations for the GASP phenotype can appear only under high mutation conditions. It is thus assumed that there are some molecular mechanisms to generate genetic diversity in the LTSP.
Involvement of the methyl-directed mismatch repair (MMR) system and SOS-induced DNA polymerases has been considered for GASP mutations (Figure 1). It is known that when
4.2. Importance of σE-dependent PCD for survival in the LTSP
σE-dependent PCD lyses damaged cells but not undamaged cells or cells with little damage and thus has no influence on viable and culturable (VAC) cells [19]. This PCD is responsible for major cell lysis under general cultivation conditions and is enhanced in the stationary phase due to accumulation of stresses including oxidative stress as described above, and forms ghost cells that discharge cytosolic contents to the outside [59]. This lysis thus appears to be different from explosive cell lysis for the biogenesis of membrane vesicles [84]. As in the stationary phase, it is assumed that cells in the LTSP are exposed to metabolically accumulated stresses including oxidative stress, which trigger σE-dependent PCD. Therefore, σE-dependent PCD may provide nutrients that are indispensable for the formation and maintenance of new populations in the LTSP.
As mentioned in the previous section, disrupted mutations of
Although we still have no evidence that dynamic cell population changes continuously occur in the LTSP, results of studies [14, 16, 17] and results of preliminary experiments in its early phase suggest that cells acquiring mutations for GASP become dominant to form a new population and that new GASP mutations constantly appear and displace the preexisting population. σE-dependent PCD may contribute to the alteration of populations by the lysis of preexisting populations and the provision of nutrients during the LTSP. For the emergence of GASP mutations, a large number of mutations should be present in addition to them under such nutrient-limited conditions. A hypermutable state might exist in the LTSP as mentioned above [14]. In order for hypermutation and σE-dependent PCD to take place, active metabolisms should be maintained in fractions of the cell population. These active metabolisms are thought to lead to the selection of a dominant mutant and generate genetic diversity.
Further analysis of the LTSP
Acknowledgments
This work was supported by the Japan Society for the Promotion of Science, MEXT/JSPS Kakenhi (25250028) and the Advanced Low Carbon Technology Research and Development Program, Japan Science and Technology Agency (JST). This work was partially performed as collaborative research in the Asian Core Program and in the Core to Core Program, which was supported by the Scientific Cooperation Program agreed by the Japan Society for the Promotion of Science (JSPS), the National Research Council of Thailand (NRCT) and universities involved in the program.
Abbreviations
ALD | apoptosis-like death |
CFU | colony-forming unit |
ESR | envelope stress response |
EDF | extracellular death factor |
GASP | growth advantage in stationary phase |
LPS | lipopolysaccharide |
LTSP | long-term stationary phase |
MMR | mismatch repair |
OMPs | outer membrane proteins |
PCD | programmed cell death |
ROS | reactive oxygen species |
sRNAs | small RNAs |
TA | toxin-antitoxin |
VAC | viable and culturable |
VBNC | viable but nonculturable |
References
- 1.
Ishihama A. Modulation of the nucleoid, the transcription apparatus, and the translation machinery in bacteria for stationary phase survival. Genes Cells. 1999; 4 :135-143. - 2.
Raina S, Missiakas D, Georgopoulos C. The rpoE gene encoding the σE (σ24) heat shock sigma factor ofEscherichia coli . EMBO J. 1995;14 :1043-1055. - 3.
Guest RL, Raivio TL. Role of the Gram-negative envelope stress response in the presence of antimicrobial agents. Trends Microbiol. 2016; 24 :377-390. DOI: 10.1016/j.tim.2016.03.001. - 4.
Kabir MS, Yamashita D, Koyama S, Oshima T, Kurokawa K, Maeda M, Tsunedomi R, Murata M, Wada C, Mori H, Yamada M. Cell lysis directed by σE in early stationary phase and effect of induction of the rpoE gene on global gene expression inEscherichia coli . Microbiology. 2005;151 :2721-2735. DOI: 10.1099/mic.0.28004-0. - 5.
Lockshin RA. Programmed cell death: history and future of a concept. J Soc Biol. 2005; 199 :169-173. - 6.
Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 1972; 26 :239-257. - 7.
Danial NN, Korsmeyer SJ. Cell death: critical control points. Cell. 2004; 116 :205-219. - 8.
Kabir MS, Yamada M. σE-dependent programmed cell death in Escherichia coli . In: Yamada M, editor. Survival and death in bacteria. Kerala, India: Research Signpost; 2005. pp. 1-13. - 9.
Allocati N, Masulli M, Di Ilio C, De Laurenzi V. Die for the community: an overview of programmed cell death in bacteria. Cell Death Dis. 2015; 6 :e1609. DOI: 10.1038/cddis.2014.570. - 10.
Bayles KW. The biological role of death and lysis in biofilm development. Nat Rev Microbiol. 2007; 5 :721-726. DOI: 10.1038/nrmicro1743. - 11.
González-Pastor JE, Hobbs EC, Losick R. Cannibalism by sporulating bacteria. Science. 2003; 301 :510-513. DOI: 10.1126/science.1086462. - 12.
Yamaguchi Y, Inouye M. Regulation of growth and death in Escherichia coli by toxin-antitoxin systems. Nat Rev Microbiol. 2011;9 :779-790. DOI: 10.1038/nrmicro2651. - 13.
Bayles KW. Bacterial programmed cell death: making sense of a paradox. Nat Rev Microbiol. 2014; 12 :63-69. DOI: 10.1038/nrmicro3136. - 14.
Finkel SE. Long-term survival during stationary phase: evolution and the GASP phenotype. Nat Rev Microbiol. 2006; 4 :113-120. DOI: 10.1038/nrmicro1340. - 15.
Navarro Llorens JM, Tormo A, Martínez-García E. Stationary phase in gram-negative bacteria. FEMS Microbiol Rev. 2010; 34 :476-495. DOI: 10.1111/j.1574-6976.2010.00213.x. - 16.
Zambrano MM, Siegele DA, Almirón M, Tormo A, Kolter R. Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science. 1993;259 :1757-1760. - 17.
Finkel SE, Kolter R. Evolution of microbial diversity during prolonged starvation. Proc Natl Acad Sci U S A. 1999; 96 :4023-4027. - 18.
Pletnev P, Osterman I, Sergiev P, Bogdanov A, Dontsova O. Survival guide: Escherichia coli in the stationary phase. Acta Naturae. 2015;7 :22-33. - 19.
Nitta T, Nagamitsu H, Murata M, Izu H, Yamada M. Function of the σE regulon in dead-cell lysis in stationary-phase. J Bacteriol. 2000; 182 :5231-5237. - 20.
Costanzo A, Ades SE. Growth phase-dependent regulation of the extracytoplasmic stress factor, σE, by guanosine 3′,5′-bispyrophosphate (ppGpp). J Bacteriol. 2006; 188 :4627-4634. DOI: 10.1128/JB.01981-05. - 21.
Yuste L, Hervás AB, Canosa I, Tobes R, Jiménez JI, Nogales J, Pérez-Pérez MM, Santero E, Díaz E, Ramos JL, de Lorenzo V, Rojo F. Growth phase-dependent expression of the Pseudomonas putida KT2440 transcriptional machinery analysed with a genome-wide DNA microarray. Environ Microbiol. 2006;8 :165-177. DOI: 10.1111/j.1462-2920.2005.00890.x. - 22.
Gefen O, Fridman O, Ronin I, Balaban NQ. Direct observation of single stationary-phase bacteria reveals a surprisingly long period of constant protein production activity. Proc Natl Acad Sci U S A. 2014; 111 :556-561. DOI: 10.1073/pnas.1314114111. - 23.
Zambrano MM, Kolter R. Escherichia coli mutants lacking NADH dehydrogenase I have a competitive disadvantage in stationary phase. J Bacteriol. 1993;175 :5642-5647. - 24.
Kram KE, Finkel SE. Culture volume and vessel affect long-term survival, mutation frequency, and oxidative stress of Escherichia coli . Appl Environ Microbiol. 2014;80 :1732-1738. DOI: 10.1128/AEM.03150-13. - 25.
Nagamitsu H, Murata M, Kosaka T, Kawaguchi J, Mori H, Yamada M. Crucial roles of MicA and RybB as vital factors for σE-dependent cell lysis in Escherichia coli long-term stationary phase. J Mol Microbiol Biotechnol. 2013;23 :227-232. DOI: 10.1159/000350370. - 26.
Walsh NP, Alba BM, Bose B, Gross CA, Sauer RT. OMP peptide signals initiate the envelope-stress response by activating DegS protease via relief of inhibition mediated by its PDZ domain. Cell. 2003; 113 :61-71. - 27.
Cezairliyan BO, Sauer RT. Inhibition of regulated proteolysis by RseB. Proc Natl Acad Sci U S A. 2007; 104 :3771-3776. DOI: 10.1073/pnas.0611567104. - 28.
Kim DY. Two stress sensor proteins for the expression of sigmaE regulon: DegS and RseB. J Microbiol. 2015; 53 :306-310. DOI: 10.1007/s12275-015-5112-6. - 29.
Lima S, Guo MS, Chaba R, Gross CA, Sauer RT. Dual molecular signals mediate the bacterial response to outer-membrane stress. Science. 2013; 340 :837-841. DOI: 10.1126/science.1235358. - 30.
Hizukuri Y, Oda T, Tabata S, Tamura-Kawakami K, Oi R, Sato M, Takagi J, Akiyama Y, Nogi T. A structure-based model of substrate discrimination by a noncanonical PDZ tandem in the intramembrane-cleaving protease RseP. Structure. 2014; 22 :326-336. DOI: 10.1016/j.str.2013.12.003. - 31.
Akiyama Y, Kanehara K, Ito K. RseP (YaeL), an Escherichia coli RIP protease, cleaves transmembrane sequences. EMBO J. 2004;23 :4434-4442. DOI: 10.1038/sj.emboj.7600449. - 32.
Flynn JM, Levchenko I, Sauer RT, Baker TA. Modulating substrate choice: the SspB adaptor delivers a regulator of the extracytoplasmic-stress response to the AAA+ protease ClpXP for degradation. Genes Dev. 2004; 18 :2292-2301. DOI: 10.1101/gad.1240104. - 33.
Chaba R, Grigorova IL, Flynn JM, Baker TA, Gross CA. Design principles of the proteolytic cascade governing the σE-mediated envelope stress response in Escherichia coli : keys to graded, buffered, and rapid signal transduction. Genes Dev. 2007;21 :124-136. DOI: 10.1101/gad.1496707. - 34.
Hizukuri Y, Akiyama Y. PDZ domains of RseP are not essential for sequential cleavage of RseA or stress-induced σE activation in vivo . Mol Microbiol. 2012;86 :1232-1245. DOI: 10.1111/mmi.12053. - 35.
Goemans C, Denoncin K, Collet JF. Folding mechanisms of periplasmic proteins. Biochim Biophys Acta. 2014; 1843 :1517-1528. DOI: 10.1016/j.bbamcr.2013.10.014. - 36.
Chng SS, Gronenberg LS, Kahne D. Proteins required for lipopolysaccharide assembly in Escherichia coli form a transenvelope complex. Biochemistry. 2010;49 :4565-4567. DOI: 10.1021/bi100493e. - 37.
Chaba R, Alba BM, Guo MS, Sohn J, Ahuja N, Sauer RT, Gross CA. Signal integration by DegS and RseB governs the σE-mediated envelope stress response in Escherichia coli . Proc Natl Acad Sci U S A. 2011;108 :2106-2111. DOI: 10.1073/pnas.1019277108. - 38.
Ades SE, Grigorova IL, Gross CA. Regulation of the alternative sigma factor σE during initiation, adaptation, and shutoff of the extracytoplasmic heat shock response in Escherichia coli . J Bacteriol. 2003;185 :2512-2519. DOI: 10.1128/JB.185.8.2512-2519.2003. - 39.
Dartigalongue C, Missiakas D, Raina S. Characterization of the Escherichia coli σE regulon. J Biol Chem. 2001;276 :20866-20875. DOI: 10.1074/jbc.M100464200. - 40.
Rezuchova B, Miticka H, Homerova D, Roberts M, Kormanec J. New members of the Escherichia coli σE regulon identified by a two-plasmid system. FEMS Microbiol Lett. 2003;225 :1-7. DOI: 10.1016/S0378-1097(03)00480-4. - 41.
Rhodius VA, Suh WC, Nonaka G, West J, Gross CA. Conserved and variable functions of the σE stress response in related genomes. PLoS Biol. 2006; 4 :e2. DOI: 10.1371/journal.pbio.0040002. - 42.
Klein G, Raina S. Regulated control of the assembly and diversity of LPS by noncoding sRNAs. Biomed Res Int. 2015; 2015 :153561. DOI: 10.1155/2015/153561. - 43.
Koo MS, Lee JH, Rah SY, Yeo WS, Lee JW, Lee KL, Koh YS, Kang SO, Roe JH. A reducing system of the superoxide sensor SoxR in Escherichia coli . EMBO J. 2003;22 :2614-2622. DOI: 10.1093/emboj/cdg252. - 44.
Gogol EB, Rhodius VA, Papenfort K, Vogel J, Gross CA. Small RNAs endow a transcriptional activator with essential repressor functions for single-tier control of a global stress regulon. Proc Natl Acad Sci U S A. 2011; 108 :12875-12880. DOI: 10.1073/pnas.1109379108. - 45.
Guo MS, Updegrove TB, Gogol EB, Shabalina SA, Gross CA, Storz G. MicL, a new σE-dependent sRNA, combats envelope stress by repressing synthesis of Lpp, the major outer membrane lipoprotein. Genes Dev. 2014; 28 :1620-1634. DOI: 10.1101/gad.243485.114. - 46.
Aizenman E, Engelberg-Kulka H, Glaser G. An Escherichia coli chromosomal “addiction module” regulated by 3′,5′-bispyrophosphate: a model for programmed bacterial cell death. Proc Natl Acad Sci U S A. 1996;93 :6059-6063. - 47.
Engelberg-Kulka H, Amitai S, Kolodkin-Gal I, Hazan R. Bacterial programmed cell death and multicellular behavior in bacteria. PLoS Genet. 2006; 2 :e135. DOI: 10.1371/journal.pgen.0020135. - 48.
Erental A, Sharon I, Engelberg-Kulka H. Two programmed cell death systems in Escherichia coli : an apoptotic-like death is inhibited by themazEF -mediated death pathway. Kerala, India: PLoS Biol. 2012;10 :e1001281. DOI: 10.1371/journal.pbio.1001281. - 49.
Zhang Y, Zhang J, Hoeflich KP, Ikura M, Qing G, Inouye M. MazF cleaves cellular mRNAs specifically at ACA to block protein synthesis in Escherichia coli . Mol Cell. 2003;12 :913-923. - 50.
Amitai S, Kolodkin-Gal I, Hananya-Meltabashi M, Sacher A, Engelberg-Kulka H. Escherichia coli MazF leads to the simultaneous selective synthesis of both “death proteins” and “survival proteins”. PLoS Genet. 2009;5 :e1000390. DOI: 10.1371/journal.pgen.1000390. - 51.
Kolodkin-Gal I, Hazan R, Gaathon A, Carmeli S, Engelberg-Kulka H. A linear pentapeptide is a quorum-sensing factor required for mazEF -mediated cell death inEscherichia coli . Science. 2007;318 :652-655. DOI: 10.1126/science.1147248. - 52.
Belitsky M, Avshalom H, Erental A, Yelin I, Kumar S, London N, Sperber M, Schueler-Furman O, Engelberg-Kulka H. The Escherichia coli extracellular death factor EDF induces the endoribonucleolytic activities of the toxins MazF and ChpBK. Mol Cell. 2011;41 :625-635. DOI: 10.1016/j.molcel.2011.02.023. - 53.
Erental A, Kalderon Z, Saada A, Smith Y, Engelberg-Kulka H. Apoptosis-like death, an extreme SOS response in Escherichia coli . MBio. 2014;5 :e01426-14. DOI: 10.1128/mBio.01426-14. - 54.
Jacob AI, Köhrer C, Davies BW, RajBhandary UL, Walker GC. Conserved bacterial RNase YbeY plays key roles in 70S ribosome quality control and 16S rRNA maturation. Mol Cell. 2013; 49 :427-438. DOI: 10.1016/j.molcel.2012.11.025. - 55.
Hayden JD, Ades SE. The extracytoplasmic stress factor, σE, is required to maintain cell envelope integrity in Escherichia coli . PLoS One. 2008;3 :e1573. DOI: 10.1371/journal.pone.0001573. - 56.
Button JE, Silhavy TJ, Ruiz N. A suppressor of cell death caused by the loss of σE downregulates extracytoplasmic stress responses and outer membrane vesicle production in Escherichia coli . J Bacteriol. 2007;189 :1523-1530. DOI: 10.1128/JB.01534-06. - 57.
Daimon Y, Narita S, Akiyama Y. Activation of toxin-antitoxin system toxins suppresses lethality caused by the loss of σE in Escherichia coli . J Bacteriol. 2015;197 :2316-2324. DOI: 10.1128/JB.00079-15. - 58.
Desnues B, Cuny C, Grégori G, Dukan S, Aguilaniu H, Nyström T. Differential oxidative damage and expression of stress defence regulons in culturable and non-culturable Escherichia coli cells. EMBO Rep. 2003;4 :400-404. DOI: 10.1038/sj.embor.embor799. - 59.
Murata M, Noor R, Nagamitsu H, Tanaka S, Yamada M. Novel pathway directed by σE to cause cell lysis in Escherichia coli . Genes Cells. 2012;17 :234-247. DOI: 10.1111/j.1365-2443.2012.01585.x. - 60.
Murata M, Kosaka T, Yamada M. Small non-coding RNAs and their involvement in regulation of various biological processes in and other bacteria. In: Yoshito S, Matsumoto K, editors. Escherichia coli andBacillus subtilis ; the frontiers of molecular microbiology revisited. Research Signpost; 2012. pp. 197-217. - 61.
Udekwu KI, Wagner EG. Sigma E controls biogenesis of the antisense RNA MicA. Nucleic Acids Res. 2007; 35 :1279-1288. DOI: 10.1093/nar/gkl1154. - 62.
Thompson KM, Rhodius VA, Gottesman S. σE regulates and is regulated by a small RNA in Escherichia coli . J Bacteriol. 2007;189 :4243-4256. DOI: 10.1128/JB.00020-07. - 63.
Valentin-Hansen P, Johansen J, Rasmussen AA. Small RNAs controlling outer membrane porins. Curr Opin Microbiol. 2007; 10 :152-155. DOI: 10.1016/j.mib.2007.03.001. - 64.
Nikaido H. Molecular basis of bacterial outer membrane permeability revisited. Microbiology and Molecular Biology Reviews. 2003; 67 :593-656. DOI: 10.1128/MMBR.67.4.593-656.2003. - 65.
Saint N, El Hamel C, Dé E, Molle G. Ion channel formation by N-terminal domain: a common feature of OprFs of Pseudomonas and OmpA ofEscherichia coli . FEMS Microbiol Lett. 2000;190 :261-265. - 66.
Apirakaramwong A, Fukuchi J, Kashiwagi K, Kakinuma Y, Ito E, Ishihama A, Igarashi K. Enhancement of cell death due to decrease in Mg2+ uptake by OmpC (cation-selective porin) deficiency in ribosome modulation factor-deficient mutant. Biochem Biophys Res Commun. 1998; 251 :482-487. - 67.
Pilsl H, Smajs D, Braun V. Characterization of colicin S4 and its receptor, OmpW, a minor protein of the Escherichia coli outer membrane. J Bacteriol. 1999;181 :3578-3581. - 68.
Noor R, Murata M, Nagamitsu H, Klein G, Raina S, Yamada M. Dissection of σE-dependent cell lysis in Escherichia coli : roles of RpoE regulators RseA, RseB and periplasmic folding catalyst PpiD. Genes Cells. 2009;14 :885-899. DOI: 10.1111/j.1365-2443.2009.01318.x. - 69.
Dartigalongue C, Raina S. A new heat-shock gene, ppiD , encodes a peptidyl-prolyl isomerase required for folding of outer membrane proteins inEscherichia coli . EMBO J. 1998;17 :3968-3980. DOI: 10.1093/emboj/17.14.3968. - 70.
Noor R, Murata M, Yamada M. Oxidative stress as a trigger for growth phase-specific σE-dependent cell lysis in Escherichia coli . J Mol Microbiol Biotechnol. 2009;17 :177-187. DOI: 10.1159/000236029. - 71.
Nyström T. Role of oxidative carbonylation in protein quality control and senescence. EMBO J. 2005; 24 :1311-1317. DOI: 10.1038/sj.emboj.7600599. - 72.
Kabir MS, Yamashita D, Noor R, Yamada M. Effect of σS on σE-directed cell lysis in Escherichia coli early stationary phase. J Mol Microbiol Biotechnol. 2004;8 :189-194. DOI: 10.1159/000085791. - 73.
Battesti A, Majdalani N, Gottesman S. The RpoS-mediated general stress response in Escherichia coli . Annu Rev Microbiol. 2011;65 :189-213. DOI: 10.1146/annurev-micro-090110-102946. - 74.
Hengge-Aronis R, Klein W, Lange R, Rimmele M, Boos W. Trehalose synthesis genes are controlled by the putative sigma factor encoded by rpoS and are involved in stationary-phase thermotolerance inEscherichia coli . J Bacteriol. 1991;173 :7918-7924. - 75.
Zambrano MM, Kolter R. GASPing for life in stationary phase. Cell. 1996; 86 :181-184. - 76.
Farrell MJ, Finkel SE. The growth advantage in stationary-phase phenotype conferred by rpoS mutations is dependent on the pH and nutrient environment. J Bacteriol. 2003;185 :7044-7052. DOI: 10.1128/JB.185.24.7044-7052.2003. - 77.
Zinser ER, Kolter R. Prolonged stationary-phase incubation selects for lrp mutations inEscherichia coli K-12. J Bacteriol. 2000;182 :4361-4365. DOI: 10.1128/JB.182.15.4361-4365.2000. - 78.
Zinser ER, Kolter R. Mutations enhancing amino acid catabolism confer a growth advantage in stationary phase. J Bacteriol. 1999; 181 :5800-5807. - 79.
Rozen DE, Philippe N, Arjan de Visser J, Lenski RE, Schneider D. Death and cannibalism in a seasonal environment facilitate bacterial coexistence. Ecol Lett. 2009; 12 :34-44. DOI: 10.1111/j.1461-0248.2008.01257.x. - 80.
Saint-Ruf C, Pesut J, Sopta M, Matic I. Causes and consequences of DNA repair activity modulation during stationary phase in Escherichia coli . Crit Rev Biochem Mol Biol. 2007;42 :259-270. DOI: 10.1080/10409230701495599. - 81.
Goodman MF. The discovery of error-prone DNA polymerase V and its unique regulation by RecA and ATP. J Biol Chem. 2014; 289 :26772-26782. DOI: 10.1074/jbc.X114.607374. - 82.
Yeiser B, Pepper ED, Goodman MF, Finkel SE. SOS-induced DNA polymerases enhance long-term survival and evolutionary fitness. Proc Natl Acad Sci U S A. 2002; 99 :8737-8741. DOI: 10.1073/pnas.092269199. - 83.
Corzett CH, Goodman MF, Finkel SE. Competitive fitness during feast and famine: how SOS DNA polymerases influence physiology and evolution in Escherichia coli . Genetics. 2013;194 :409-420. DOI: 10.1534/genetics.113.151837. - 84.
Turnbull L, Toyofuku M, Hynen AL, Kurosawa M, Pessi G, Petty NK, Osvath SR, Cárcamo-Oyarce G, Gloag ES, Shimoni R, Omasits U, Ito S, Yap X, Monahan LG, Cavaliere R, Ahrens CH, Charles IG, Nomura N, Eberl L, Whitchurch CB. Explosive cell lysis as a mechanism for the biogenesis of bacterial membrane vesicles and biofilms. Nat Commun. 2016; 7 :11220. DOI: 10.1038/ncomms11220.