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Harshey, R. M.

Publications and source records attributed to Harshey, R. M..

14 recordsLinked to original sources

Mu-seq reveals previously undetected long-range contact patterns in the Escherichia coli nucleoid

The spatial organization of the Escherichia coli chromosome is a key determinant of its functional and regulatory landscape, but widely used chromatin conformation capture methods, such as Hi-C, provide an incomplete view of the underlying three-dimensional genome connectivity. Here, we introduce Mu-seq, a massively multiplexed Mu transposition-based approach that maps genome-wide DNA-DNA proximity in live cells without crosslinking. By distributing engineered, barcoded Mu prophages throughout the chromosome and tracking their replicative transposition events, Mu-seq generates dense, uniform sampling of physical contacts across the genome, enabling a direct, in vivo snapshot of chromosome architecture. Applying this method in E. coli, we constructed a contact dataset spanning over 200,000 unique loci, revealing interaction patterns not accessible to current crosslinking-based techniques. Mu-seq findings can be broken down into three layers. First, it recapitulates polymer-like enrichment of short-range contacts. Second, contacts identified by Mu-seq are strongly shaped by chromatin state: transcriptionally active and accessible regions disproportionately contribute to long-range connectivity, whereas protein-occupied domains, including H-NS-enriched regions, are depleted of insertions and contacts. Third, beyond distance-dependent polymer behavior and chromatin accessibility, Mu-seq reveals specific long-range associations among functionally related loci, such as ribosomal operons. These findings suggest that bacterial chromosome organization can bring functionally related regions into shared three-dimensional neighborhoods even when they are widely separated along the linear genome. Together, these findings support a layered model of nucleoid organization, in which transcriptionally active loops extend outward from a dense, protein-rich axial core. Mu-seq thus provides a powerful, complementary in vivo framework for probing bacterial chromosome architecture, uncovering regulatory and structural features of genome organization that are largely invisible to crosslinking-based approaches.

microbiology↗

Aer is a bidirectional redox sensor mediating negative chemotaxis to antibiotic-induced ROS in E. coli

The Aer chemoreceptor in E. coli is known to perform oxygen- or aero-taxis by sensing metabolic flux through ETC via an FAD cofactor bound to its PAS domain. We show in this study that Aer also senses oxidative stress and performs FAD-dependent negative chemotaxis in response to the known ROS H2O2. The ability of Aer to detect both oxidizing and reducing intracellular environments redefines its functional range and establishes Aer as a bidirectional redox sensor. We show in addition that the ability of bacterial swarms to move away from bactericidal antibiotics is Aer-dependent and is abolished by expression of the catalase-peroxidase enzyme KatG, which scavenges intracellular ROS. Our study thus provides independent behavioral evidence that certain antibiotics generate intracellular ROS, while also offering a sensitive assay for detecting these reactive species. ImportanceMotile bacteria rely on aerotaxis to seek environments that maximize energy production. We show that in E. coli, Aer mediates not only positive chemotaxis toward favorable redox conditions but also negative chemotaxis in response to oxidative stress. The ability of Aer to detect both oxidizing and reducing cellular environments reveals an unexpected sensory versatility, shared to varying degrees by other E. coli chemoreceptors. We show that E. coli uses Aer to actively move away from ROS-generating antibiotics, revealing a previously unrecognized behavioral mechanism for bacterial survival under oxidative stress.

microbiology↗

Texas 2-Step: A new Model for YcgR::c-di-GMP Action at the Flagellar Motor

YcgR is a c-di-GMP effector that inhibits chemotaxis and swimming speed in Escherichia coli and Salmonella. Genetic, biochemical, and structural studies suggest that YcgR interacts with both the bidirectional flagellar rotor and the stator to bias rotation toward counterclockwise (CCW) and reduce motor speed, but the underlying mechanism remains unresolved. Recent cryo-EM structures revealing conformational changes in the rotor-stator complex during directional switching suggested to us a mechanism by which YcgR acts. We call this the Texas 2-Step model, after the country dance in which partners move smoothly in a CCW arc with quick steps followed by slow ones. In this model, YcgR first binds a MotA subunit when the rotor adopts the CCW conformation, in which stators are largely displaced from the C-ring. In the next step, the rotating MotA pentamer delivers YcgR to the rotor protein FliG, thereby slowing motor speed. We provide evidence for the first step of this model, offering testable predictions for future work. ImportanceThe mechanism of YcgR action has been investigated by multiple laboratories using diverse approaches, yet no consensus has emerged. Some studies implicate the rotor, others the stator. A key complication is the involvement of four interacting proteins--MotA, FliG, FliM, and YcgR--with multiple contact sites in several of them. Recent rotor-stator cryo-EM structures revealing conformational changes during directional switching suggested a mechanism that we set out to test. Our experiments show that rotor conformation is crucial for YcgR function.

microbiology↗

c-di-GMP is required for swarming motility in E. coli

Many bacteria use flagella to swim individually through bulk liquid, or swarm collectively over a semi-solid surface. In E. coli, c-di-GMP inhibits swimming via the effector protein YcgR. We show in this study that contrary to its effect on swimming, a certain threshold level of c-di-GMP is required for swarming. Gene expression profiles first indicated that several c-di-GMP synthases - dgcJ, dgcM, dgcO - were upregulated during swarming. Of these, we found DgcO to play a critical role. DgcO is reported to affect PGA (poly-{beta}-1,6-N-acetylglucosamine) synthesis in E. coli. We show that DgcO also promotes production of colanic acid - one of the three major exopolysaccharides in E. coli, and that colanic acid has hitherto-unknown surfactant properties that are expected to aid swarming. ImportanceIt is well-established that in bacteria, c-di-GMP inhibits flagella-driven motility at various points in the pathway. Concomitantly, elevated c-di-GMP levels induce the expression and synthesis of a variety of exopolysaccharides that enmesh the bacteria in a biofilm, thereby also interfering with flagella function. This study reports the surprising finding that in E. coli, the exopolysaccharide colanic acid is required to enable surface navigation and that the diguanylate cyclase DgcO is employed for this purpose. For surface navigation, there appears to be a sweet spot where c-di-GMP levels are just right to produce polysaccharides that can serve as surfactants and wetting agents rather than promote formation of biofilms.

microbiology↗

Phage Mu Utilizes the Sliding Clamp for Late Gene Transcription

MuC, along with core RNAP and {sigma}70, is required for transcription of late genes of phage Mu. We observed that overexpression of MuC is lethal in E. coli and that host replication was over-initiating under these conditions. Suppressors of MuC lethality occurred in dnaA, diaA, and dnaX, genes involved in initiation of DNA replication. We hypothesized that lethality was likely due to increase in ATP-DnaA levels, which are normally kept in check by Hda-DnaN ({beta} clamp). We noticed that MuC harbors a well-defined motif for interaction with the {beta} clamp. We provide experimental support for this interaction and show that disrupting it through mutations in the clamp-binding motif on MuC, expressed from both plasmid and the phage genome, abrogated transcription from a MuC-dependent promoter as well as production of viable phage, respectively. Furthermore, we show that inactivation of {beta}-clamp specifically inactivates C-dependent transcription but not {sigma}70-dependent transcription. We conclude that MuC requires the b sliding clamp for transcribing late phage genes. To the best of our knowledge, this is the first demonstration of the involvement of the clamp, a processivity factor essential for DNA replication, for transcription by E. coli RNAP.

microbiology↗

Clustering of rRNA operons in E. coli is disrupted by σH

Chromosomal organization in E. coli as examined by Hi-C methodology indicates that long-range interactions are sparse. Yet, spatial co-localization or clustering of 6/7 ribosomal RNA (rrn) operons distributed over half the 4.6 Mbp genome has been captured by two other methodologies - fluorescence microscopy and Mu transposition. Our current understanding of the mechanism of clustering is limited to mapping essential cis elements. To identify trans elements, we resorted to perturbing the system by chemical and physical means and observed that heat shock disrupts clustering. Levels of {sigma}H are known to rise as a cellular response to the shock. We show that elevated expression of {sigma}H alone is sufficient to disrupt clustering, independent of heat stress. The anti-clustering activity of {sigma}H does not depend on its transcriptional activity but requires core-RNAP interaction and DNA-binding activities. This activity of {sigma}H is suppressed by ectopic expression of {sigma}D suggesting a competition for core-RNAP. A query of the other five known {sigma} factors of E. coli found that elevated expression of FecI, the ECF {sigma} factor that controls iron citrate transport, also perturbs clustering and is also suppressed by {sigma}D. We discuss a possible scenario for how these membrane-associated {sigma} factors participate in clustering of distant rrn loci.

microbiology↗

Flagellar Motility is Mutagenic

Flagella are highly complex rotary molecular machines that enable bacteria to not only migrate to optimal environments but to also promote range expansion, competitiveness, virulence, and antibiotic survival. Flagellar motility is an energy-demanding process, where the sum of its production (biosynthesis) and operation (rotation) costs has been estimated to total [~]10% of the entire energy budget of an E. coli cell. The acquisition of such a costly adaptation process is expected to secure short-term benefits by increasing competitiveness and survival, as well as long-term evolutionary fitness gains. While the role of flagellar motility in bacterial survival has been widely reported, its direct influence on the rate of evolution remains unclear. We show here that both production and operation costs contribute to elevated mutation frequencies. Our findings suggest that flagellar movement may be an important player in tuning the rate of bacterial evolution.

microbiology↗

Flagellar motor remodeling during swarming requires FliL

FliL is an essential component of the flagellar machinery in some bacteria, but a conditional one in others. The conditional role is for optimal swarming in some bacteria. During swarming, physical forces associated with movement on a surface are expected to exert a higher load on the flagellum, requiring more motor torque to move. Bacterial physiology and morphology are also altered during swarming to cope with the challenges of surface navigation. FliL was reported to enhance motor output in several bacteria and observed to assemble as a ring around ion-conducting stators that power the motor. In this study we identify a common new function for FliL in diverse bacteria - Escherichia coli, Bacillus subtilis and Proteus mirabilis. During swarming, all these bacteria show increased cell speed and a skewed motor bias that suppresses cell tumbling. We demonstrate that these altered motor parameters, or motor remodeling, require FliL. Both swarming and motor remodeling can be restored in an E. coli fliL mutant by complementation with fliL genes from P. mirabilis and B. subtilis, showing conservation of swarming-associated FliL function across phyla. In addition, we demonstrate that the strong interaction we reported earlier between FliL and the flagellar MS-ring protein FliF is confined to the RBM-3 domain of FliF that links the periplasmic rod to the cytoplasmic C-ring. This interaction may explain several phenotypes associated with the absence of FliL.

microbiology↗

Iron Memory in E. coli

The importance of memory in bacterial decision-making is relatively unexplored. We show here that a prior experience of swarming is remembered when E. coli encounters a new surface, improving its future swarming efficiency. We conducted >10,000 single-cell swarm assays to discover that cells store memory in the form of cellular iron levels. This memory pre-exists in planktonic cells, but the act of swarming reinforces it. A cell with low iron initiates swarming early and is a better swarmer, while the opposite is true for a cell with high iron. The swarming potential of a mother cell, whether low or high, is passed down to its fourth-generation daughter cells. This memory is naturally lost by the seventh generation, but artificially manipulating iron levels allows it to persist much longer. A mathematical model with a time-delay component faithfully recreates the observed dynamic interconversions between different swarming potentials. We also demonstrate that iron memory can integrate multiple stimuli, impacting other bacterial behaviors such as biofilm formation and antibiotic tolerance.

microbiology↗

A Second Role for the Second Messenger Cyclic-di-GMP in E. coli: Arresting Cell Growth by Altering Metabolic Flow

C-di-GMP primarily controls motile to sessile transitions in bacteria. Diguanylate cyclases (DGCs) catalyze the synthesis of c-di-GMP from two GTP molecules. Typically, bacteria encode multiple DGCs that are activated by specific environmental signals. Their catalytic activity is modulated by c-di-GMP binding to autoinhibitory sites (I-sites). YfiN is a conserved inner membrane DGC that lacks these sites. Instead, YfiN activity is directly repressed by periplasmic YfiR, which is inactivated by redox stress. In E. coli, an additional envelope stress causes YfiN to relocate to the mid-cell to inhibit cell division by interacting with the division machinery. Here, we report a third activity for YfiN in E. coli, where cell growth is inhibited without YfiN relocating to the division site. This action of YfiN is only observed when the bacteria are cultured on gluconeogenic carbon sources, and is dependent on absence of the autoinhibitory sites. Restoration of I-site function relieves the growth-arrest phenotype, and disabling this function in a heterologous DGC causes acquisition of this phenotype. Arrested cells are tolerant to a wide range of antibiotics. We show that the likely cause of growth arrest is depletion of cellular GTP from run-away synthesis of c-di-GMP, explaining the dependence of growth arrest on gluconeogenic carbon sources that exhaust more GTP during production of glucose. This is the first report of c-di-GMP-mediated growth arrest by altering metabolic flow. SignificanceThe c-di-GMP signaling network in bacteria not only controls a variety of cellular processes such as motility, biofilms, cell development and virulence, but does so by a dizzying array of mechanisms. The DGC YfiN singularly represents the versatility of this network in that it not only inhibits motility and promotes biofilms, but also arrests growth in E. coli by relocating to the mid-cell and blocking cell division. The work described here reveals that YfiN arrests growth by yet another mechanism in E. coli - changing metabolic flow. This function of YfiN, or of DGCs without autoinhibitory I-sites, may contribute to antibiotic tolerant persisters in relevant niches such as the gut where gluconeogenic sugars are found.

microbiology↗

Efflux-linked Accelerated Evolution of Antibiotic Resistance at a Population Edge

Efflux is a common mechanism of resistance to antibiotics. We show that efflux itself promotes accumulation of antibiotic-resistance mutations (ARM). This phenomenon was initially discovered in a bacterial swarm where the linked phenotypes of high efflux and high mutation frequencies spatially segregated to the swarm edge, driven there by motility. We uncovered and validated a global regulatory network that connects high efflux to downregulation of specific DNA repair pathways even in non-swarming states. The efflux-DNA repair link was corroborated in a clinical resistome database: genomes with mutations that increase efflux exhibit a significant increase in ARMs. Accordingly, efflux inhibitors decreased evolvability to antibiotic resistance. Swarms also revealed how bacterial populations serve as reservoir of ARMs even in absence of antibiotic selection pressure. High efflux at the edge births mutants that, despite compromised fitness, survive there because of reduced competition. This finding is relevant to biofilms where efflux activity is high.

microbiology↗

Remodeling of Chemotaxis is a Cornerstone of Bacterial Swarming

Many bacteria use flagella-driven motility to swarm or move collectively over a surface terrain. Bacterial adaptations for swarming can include cell elongation, hyper-flagellation, recruitment of special stator proteins and surfactant secretion, among others. We recently demonstrated another swarming adaptation in Escherichia coli, wherein the chemotaxis pathway is remodeled to increase run durations (decrease tumble bias), with running speeds increased as well. We show here that the modification of motility parameters during swarming is not unique to E. coli, but shared by a diverse group of bacteria we examined - Proteus mirabilis, Serratia marcescens, Salmonella enterica, Bacillus subtilis, and Pseudomonas aeruginosa - suggesting that altering the chemosensory physiology is a cornerstone of swarming. ImportanceBacteria within a swarm move characteristically in packs, displaying an intricate swirling motion where hundreds of dynamic packs continuously form and dissociate as the swarm colonizes increasing expanse of territory. The demonstrated property of E. coli to reduce its tumble bias and hence increase its run duration during swarming is expected to maintain/promote side-by-side alignment and cohesion within the bacterial packs. Here we observe a similar low tumble bias in five different bacterial species, both Gram positive and Gram negative, each inhabiting a unique habitat and posing unique problems to our health. The unanimous display of an altered run-tumble bias in swarms of all species examined here suggests that this behavioral adaptation is crucial for swarming.

microbiology↗

Mu Transposition in the Absence of the Target-capture Protein MuB Reveals New Roles of MuB in Target Immunity and Target Selection, and Redraws the Boundaries of the Insular Ter Region of E. coli

The target capture protein MuB is responsible for the high efficiency of phage Mu transposition within the E. coli genome. However, some targets are off-limits, such as regions immediately outside the Mu ends (cis-immunity) as well as the entire [~]37 kb genome of Mu (Mu genome immunity). Paradoxically, MuB is responsible for cis-immunity and is also implicated in Mu genome immunity, but via different mechanisms. In this study, we tracked Mu transposition from six different starting locations on the E. coli genome, in the presence and absence of MuB. The data reveal that Mus ability to sample the entire genome during a single hop in a clonal population is independent of MuB, and that MuB is responsible for cis-immunity, plays a lesser role in Mu genome immunity, and facilitates insertions into transcriptionally active regions. Unexpectedly, transposition patterns in the absence of MuB have helped extend the boundaries of the insular Ter segment of the E. coli genome.

microbiology↗

Necrosignaling: Cell death triggers antibiotic survival pathways in bacterial swarms

Swarming is form of collective bacterial motion enabled by flagella on the surface of semi-solid media1. Many bacterial species exhibit non-genetic adaptive resistance to a broad range of antibiotics only when swarming (SR)2-4. While the swarming population as a whole survives antibiotic challenge, it nonetheless sustains considerable cell death5. In this study focused mainly on E. coli, an initial analysis of antibiotic-induced killing patterns of swarm vs planktonic cells indicated that death of a sub-population is beneficial to the swarm in promoting SR. Introduction of pre-killed cells into a swarm indeed enhanced SR, allowing us to purify the SR factor from killed cells, and to establish that cell death is directly involved in SR. The SR-enhancing factor was identified to be AcrA, a periplasmic component of a tripartite RND efflux pump6, of which the outer membrane component TolC is shared by multiple drug efflux pumps7. We show that AcrA stimulates drug efflux in live cells by interacting with TolC from the outside. This stimulus acts as a signal to activate efflux in the short term, and to induce the expression of other classes of efflux pumps in the long term, amplifying the response and establishing SR. We call this phenomenon necrosignaling, and show the existence of species-specific necrosignaling in both Gram-positive and Gram-negative bacteria. Our results have implications for the adaptive resistance of other surface-associated bacterial collectives such as biofilms. Given that such resistance is known to be an incubator for evolving genetic resistance8, our findings may also be relevant to chemotherapy-resistant cancers.

microbiology↗