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Coping with Reactive Oxygen Species to Ensure Genome Stability in Escherichia Coli

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Coping with Reactive Oxygen Species to Ensure Genome Stability in Escherichia Coli G C A T T A C G G C A T genes Review Coping with Reactive Oxygen Species to Ensure Genome Stability in Escherichia coli Belén Mendoza-Chamizo, Anders Løbner-Olesen and Godefroid Charbon * Department of Biology, University of Copenhagen, Ole Maaløes vej 5, 2200 Copenhagen N, Denmark; [email protected] (B.M.-C.); [email protected] (A.L.-O.) * Correspondence: [email protected]; Tel.: +45-35-32-20-98 Received: 26 October 2018; Accepted: 16 November 2018; Published: 21 November 2018 Abstract: The facultative aerobic bacterium Escherichia coli adjusts its cell cycle to environmental conditions. Because of its lifestyle, the bacterium has to balance the use of oxygen with the potential lethal effects of its poisonous derivatives. Oxidative damages perpetrated by molecules such as hydrogen peroxide and superoxide anions directly incapacitate metabolic activities relying on enzymes co-factored with iron and flavins. Consequently, growth is inhibited when the bacterium faces substantial reactive oxygen insults coming from environmental or cellular sources. Although hydrogen peroxide and superoxide anions do not oxidize DNA directly, these molecules feed directly or indirectly the generation of the highly reactive hydroxyl radical that damages the bacterial chromosome. Oxidized bases are normally excised and the single strand gap repaired by the base excision repair pathway (BER). This process is especially problematic in E. coli because replication forks do not sense the presence of damages or a stalled fork ahead of them. As consequence, single-strand breaks are turned into double-strand breaks (DSB) through replication. Since E. coli tolerates the presence of DSBs poorly, BER can become toxic during oxidative stress. Here we review the repair strategies that E. coli adopts to preserve genome integrity during oxidative stress and their relation to cell cycle control of DNA replication. Keywords: Escherichia coli; DNA replication; genome stability; oxidative damage; ROS 1. Introduction Depending on nutrient conditions, Escherichia coli can grow with a generation time of several hours or less than 20 min. Classically, the cell cycle of slow-growing cells (more than one hour doubling time) is represented in three phases: after birth the pre-replication period (B) starts during which cells increase their size without duplicating their DNA, then comes the replication period (C) during which the chromosome is duplicated and finally the division period (D) corresponding to the time between the termination of DNA synthesis and cell division [1]. In slow growing cells, C and D periods vary with growth rate between ~40 to ~100 min and ~20 to ~60 min, respectively. When bacteria are growing fast, C and D periods are almost constant and last about 40 min and 20 min, respectively [2]. During fast growth, there is no B period and because the cellular doubling time is shorter than the time required to duplicate the chromosome and divide (C plus D), cells are born with chromosome in the process of being replicated. In this case, DNA replication is initiated in the mother, grandmother or great-grandmother cell, depending on the growth rate. DNA replication commences at a unique origin of replication (oriC) and proceeds bidirectionally on the circular chromosome until replication forks meet at the terminus region situated opposite of oriC on the chromosome. Regardless of how fast cells grow, DNA replication is initiated at a constant mass per origin (cell mass/oriC) called the initiation mass [3]. This phenomenon is primarily explained by the necessity to accumulate a fixed amount of active ATP-bound DnaA initiator protein in order to start replication [4]. At initiation, Genes 2018, 9, 565; doi:10.3390/genes9110565 www.mdpi.com/journal/genes Genes 2018, 9, 565 2 of 12 DnaA–ATP forms one or two filaments on oriC [5], which in turn results in assembly of two replication machineriesGenes to 2018 start, 9, x FOR DNA PEER replication. REVIEW The mechanisms controlling DnaA activity and/or2 of 12 its access to oriC directlyinitiation, or DnaA–ATP indirectly forms are quiteone or complex,two filaments but on our oriC understanding[5], which in turn results is that in the assembly accumulation of of the initiatortwo in replication its active machineries form (bound to start to DNA ATP) replication. plays an The essential mechanisms role controlling while the DnaA inactive activity form of the initiator (boundand/or its to access ADP) to wouldoriC directly have or anindirectly inhibitory are quite role, complex, although but our this understanding is debated is (for that review the [6–8]). Interestingly,accumulation because of of the the initiator way the in its cell active cycle form is built,(bound DnaA to ATP) and/or plays an replisome essential role activities while the determine inactive form of the initiator (bound to ADP) would have an inhibitory role, although this is debated when cells(for divide: reviewif [6–8]). initiation Interestingly, of DNA because replication of the wa isy the delayed cell cycle or is the built, C periodDnaA and/or is prolonged, replisome the cells divide lateractivities (the cells determine become when longer). cells divide: Another if initiation corollary of DNA of E.replication coli cell is cycle delayed architecture or the C period is that is because initiation happensprolonged, once the cells per divide cell cycle later and(the atcells all become origins longer). present Another in the corollary cell, each of initiationE. coli cell cycle events will be separated byarchitecture one generation is that because time. initiation This is happens especially once pertinent per cell cycle when and at considering all origins present fast growingin the cell, cells with each initiation events will be separated by one generation time. This is especially pertinent when doubling timesconsidering shorter fast growing than the cells C with period doubling that cantimes contain shorter than up the to sixC period forks that replicating can contain aup chromosome to (Figure1A).six Each forks ofreplicating these is a initiated chromosome at oriC(Figureone 1A). doubling Each of these time isbefore initiated the at oriC following one doubling one. Cellstime are born with evenbefore more the replication following one. forks Cells when are theborn Cwith period even ismore prolonged, replication suchforks aswhen when the C DNA period replication is is challengedprolonged, by lowering such as deoxynucleotide when DNA replication triphosphate is challenged (dNTP) by lowering abundance. deoxynucleotide triphosphate (dNTP) abundance. Figure 1. Distribution of replication forks during normal replication and hyper-replication. Schematic Figure 1. Distribution of replication forks during normal replication and hyper-replication. Schematic representation of a chromosome in the process of replication in cells growing with a doubling time of representation~30 min; of a(A chromosome) normal replication in the and process (B) hyper-replication. of replication Origin in cellsof replication growing (oriC with) regions a doubling are time of ~30 min;marked (A) normal in blue and replication the terminus and region (B) hyper-replication.in green. Ongoing replication Origin forks of replicationare indicated (inoriC red) (V regions are marked inmarks). blue andNumbers the indicate terminus the number region of in replicatio green.n rounds. Ongoing The replicationdistance between forks replication are indicated forks, in red (V marks).represented Numbers by indicate arrows, theis shorte numberr in hyper-replicating of replication cells. rounds. The distance between replication forks, representedThe by bacterium’s arrows, is ability shorter to ingrow hyper-replicating fast comes at the cells. price of sensitizing the chromosome to DNA damage. When DNA damage is sensed, cell division is delayed by the SOS response [9]. However, The bacterium’sunlike the situation ability in eukaryotic to grow fastcells, comes there is atno theknown price check of point sensitizing blocking theinitiation. chromosome In other to DNA damage. Whenwords, DnaA DNA keeps damage initiating is sensed, new rounds cell of division DNA replication, is delayed despite by the the fact SOS that the response chromosome [9]. However, unlike theis situation plagued by in strand eukaryotic breaks [10–15]. cells, there This leaves is no E. known coli with check the daunting point blocking task of repairing initiation. the In other chromosome in a relative short time, else replication forks collide and generate strand breaks and/or words, DnaAsingle-strand keeps initiating breaks that neware turned rounds intoof double DNA-strand replication, breaks (DSB) despite during the DNA fact synthesis. that the These chromosome is plaguedDSBs by are strand poorly breaks tolerated [ 10by –E.15 coli]. that This is effectively leaves E. killed coli bywith the accumulation the daunting of only task few ofDSBs repairing in the chromosomethe chromosome in a relative [16,17]. short time, else replication forks collide and generate strand breaks and/or single-strandEscherichia breaks coli faces that many are conditions turned intoin which double-strand DNA can be damaged breaks (DSB)and, like during all aerobically DNA synthesis. living organisms, the bacterium is subject to the potentially lethal oxidation of its DNA (see review These DSBs[18]). are Molecular poorly toleratedoxygen does by notE. readily coli that react is wi effectivelyth the cell components, killed by the but accumulation its derivatives
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