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EcoSal Plus

Domain 7:

Genetics and Genetic Tools

Mechanisms of Theta Plasmid Replication in Enterobacteria and Implications for Adaptation to Its Host

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  • Authors: Jay W. Kim1, Vega Bugata2, Gerardo Cortés-Cortés3, Giselle Quevedo-Martínez4, and Manel Camps5
  • Editors: James M. Slauch6, Gregory Phillips7
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Microbiology and Environmental Toxicology, University of California at Santa Cruz, Santa Cruz, CA, 95064; 2: Department of Microbiology and Environmental Toxicology, University of California at Santa Cruz, Santa Cruz, CA, 95064; 3: Department of Microbiology and Environmental Toxicology, University of California at Santa Cruz, Santa Cruz, CA, 95064; 4: Department of Microbiology and Environmental Toxicology, University of California at Santa Cruz, Santa Cruz, CA, 95064; 5: Department of Microbiology and Environmental Toxicology, University of California at Santa Cruz, Santa Cruz, CA, 95064; 6: The School of Molecular and Cellular Biology, University of Illinois at Urbana-Champaign, Urbana, IL; 7: College of Veterinary Medicine, Iowa State University, Ames, IA
  • Received 26 March 2020 Accepted 07 October 2020 Published 18 November 2020
  • Address correspondence to Manel Camps, [email protected]
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  • Abstract:

    Plasmids are autonomously replicating sequences that help cells adapt to diverse stresses. Theta plasmids are the most frequent plasmid class in enterobacteria. They co-opt two host replication mechanisms: replication at , a DnaA-dependent pathway leading to replisome assembly (theta class A), and replication fork restart, a PriA-dependent pathway leading to primosome assembly through primer extension and D-loop formation (theta classes B, C, and D). To ensure autonomy from the host’s replication and to facilitate copy number regulation, theta plasmids have unique mechanisms of replication initiation at the plasmid origin of replication (). Tight plasmid copy number regulation is essential because of the major and direct impact plasmid gene dosage has on gene expression. The timing of plasmid replication and segregation are also critical for optimizing plasmid gene expression. Therefore, we propose that plasmid replication needs to be understood in its biological context, where complex origins of replication (redundant origins, mosaic and cointegrated replicons), plasmid segregation, and toxin-antitoxin systems are often present. Highlighting their tight functional integration with function, we show that both partition and toxin-antitoxin systems tend to be encoded in close physical proximity to the in a large collection of plasmids. We also propose that adaptation of plasmids to their host optimizes their contribution to the host’s fitness while restricting access to broad genetic diversity, and we argue that this trade-off between adaptation to host and access to genetic diversity is likely a determinant factor shaping the distribution of replicons in populations of enterobacteria.

  • Citation: Kim J, Bugata V, Cortés-Cortés G, Quevedo-Martínez G, Camps M. 2020. Mechanisms of Theta Plasmid Replication in Enterobacteria and Implications for Adaptation to Its Host, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0026-2019

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/content/journal/ecosalplus/10.1128/ecosalplus.ESP-0026-2019
2020-11-18
2020-11-28

Abstract:

Plasmids are autonomously replicating sequences that help cells adapt to diverse stresses. Theta plasmids are the most frequent plasmid class in enterobacteria. They co-opt two host replication mechanisms: replication at , a DnaA-dependent pathway leading to replisome assembly (theta class A), and replication fork restart, a PriA-dependent pathway leading to primosome assembly through primer extension and D-loop formation (theta classes B, C, and D). To ensure autonomy from the host’s replication and to facilitate copy number regulation, theta plasmids have unique mechanisms of replication initiation at the plasmid origin of replication (). Tight plasmid copy number regulation is essential because of the major and direct impact plasmid gene dosage has on gene expression. The timing of plasmid replication and segregation are also critical for optimizing plasmid gene expression. Therefore, we propose that plasmid replication needs to be understood in its biological context, where complex origins of replication (redundant origins, mosaic and cointegrated replicons), plasmid segregation, and toxin-antitoxin systems are often present. Highlighting their tight functional integration with function, we show that both partition and toxin-antitoxin systems tend to be encoded in close physical proximity to the in a large collection of plasmids. We also propose that adaptation of plasmids to their host optimizes their contribution to the host’s fitness while restricting access to broad genetic diversity, and we argue that this trade-off between adaptation to host and access to genetic diversity is likely a determinant factor shaping the distribution of replicons in populations of enterobacteria.

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Figures

Image of Figure 1
Figure 1

Class A theta replicons typically include a replication initiator gene: (rectangle), DnaA boxes upstream or downstream of the Rep (square), iterons (arrow heads), and an AT-rich DNA unwinding element (DUE, oval). Sites for binding of nucleoid associated-proteins (such as IHF) or for methylation by Dam methylase are also frequently present as well but not shown. of the RK2 plasmid (which belongs to the IncP compatibility group) is shown as an example. RK2’s replication initiator is TrfA. The gene is under the control of a strong promoter. Transcription produces two products (a longer and a shorter one) that in this figure are considered largely redundant. During plasmid origin recognition (phase 1), replication initiation proteins (in their monomeric forms) cooperatively bind iterons until those iterons are saturated. The formation of an open complex (phase 2) involves unwinding of the DUE and continued binding of the replication initiator into the bottom strand of ssDNA; the rest of the bottom strand of ssDNA and the top strand are bound by SSB, which is a tetramer. In the case of RK2, the plasmid encodes its own SSB, which is under the control of the same promoter as the replication initiator gene (). DnaA enhances/stabilizes the formation of the TrfA-mediated open complex and assists with the recruitment of DnaBC. Finally, the longer form of TrfA also assists in strand-specific replisome assembly in a DnaA-independent manner via direct interaction with the β clamp and through a sequence-specific interaction with one strand of the plasmid origin DUE ( 8 , 136 ).

Citation: Kim J, Bugata V, Cortés-Cortés G, Quevedo-Martínez G, Camps M. 2020. Mechanisms of Theta Plasmid Replication in Enterobacteria and Implications for Adaptation to Its Host, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0026-2019
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Figure 2

Processing of the R-loop terminus by RNaseH generates a free 3′-OH terminus. RNAII needs to be in the right conformation and orientation for processing by RNaseH. The 3′-OH terminus generated by RNaseH processing is extended by DNA polymerase I (Pol I), further opening the duplex and revealing a hairpin structure in the lagging strand that can serve as a primosome assembly signal (). PriA-mediated replisome assembly starts the coordinated replication of both strands by Pol III, although there is some evidence that Pol I can functionally replace Pol III ( 69 ). For antisense RNA regulation, as it is being transcribed from promoter P2 in the sense direction, the preprimer (RNAII) forms three symmetrical stem-loop structures (stem-loops 1, 2, and 3 [SL1, SL2, and SL3]). A small and short-lived antisense transcript (RNAI) that is transcribed from a promoter going in the opposite direction also forms these three stem-loops. The RNAII nascent transcript and the antisense RNAI contact each other through the 6- to 7-nt loop portion of their respective stem-loops. This pairing makes the preprimer incompetent for R-loop formation, thus blocking replication initiation (reviewed in references 66 , 92 , and 93 ). The half-life of RNAI is short because it contains RNase E recognition sites. Preprimer transcripts larger than 200 nt long are refractory of RNAI-induced inhibition because they form an alternate stem-loop (SL4) by pairing two sequence areas of the transcript (α and β), further reducing the effective half-life of RNAI. This short half-life ensures that RNAI-mediated suppression of replication initiation is reflective of plasmid copy number.

Citation: Kim J, Bugata V, Cortés-Cortés G, Quevedo-Martínez G, Camps M. 2020. Mechanisms of Theta Plasmid Replication in Enterobacteria and Implications for Adaptation to Its Host, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0026-2019
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Figure 3

The rate of replication is determined by the concentration of free (non-Rep-bound) iterons, which is determined by both plasmid copy number and cell volume. Given the cooperative interactions involved in saturating iterons, this regulatory mechanism is ultrasensitive to plasmid copy number and switch-like. Generic class A theta replicon structure: gene (rectangle), DnaA boxes, which can be found upstream or downstream of the Rep (squares), iterons (arrowheads), and an AT-rich DNA unwinding element (DUE, oval). (A) Replication initiator proteins (Reps) when the plasmid copy number is low. Reps (blue circles) are expressed from strong promoters and tend to be in their monomeric (active) form; in some cases, the activation of these monomers needs to be facilitated by chaperones (purple stars). Reps are also sensitive to protease activity (green ovals). Active monomers bind iterons until saturation; in some cases, additional clusters of iterons are present to decrease the level of Rep available, further tightening plasmid copy number control ( 86 ). (B) Replication initiator proteins when plasmid copy number is high. High Rep protein expression resulting from a high plasmid copy number favors the dimeric form of Rep. The symmetrical conformation of the dimeric form matches inverted iterons found in the promoter of genes. This results in a binding affinity for the promoter that is higher than that of the RNA polymerase, blocking transcription ( 137 ). Transcriptional autorepression by Reps is seen in IncFIA, IncN, and IncP plasmids and is also consistent with the structure of replicons from other groups, such as IncHI1 and IncY, although in the case of IncN and IncY, the iterons that overlap with the Rep promoter are not inverted ( 43 , 138 ). Rep dimers can also bridge Rep-bound iteron arrays, one of the proposed mechanisms of handcuffing (see panel C3). (C) Different handcuffing mechanisms. Once iteron-bound Rep arrays form, they can couple two different plasmids, a reaction in known as plasmid handcuffing that blocks melting by steric hindrance ( 139 ). Three mechanisms that pair different plasmids through iteron-bound replication initiation proteins have been proposed ( 43 ). From left to right: direct dimerization of the iteron-bound initiators (proposed for the plasmid RK6 [ 140 ]), direct interaction between arrays of iteron-bound monomers, associated with a Rep conformational change induced by iteron binding (proposed for the plasmid pPS10 [ 141 ]), and bridging via dimer formation (proposed for RK2 [ 139 ]). Chaperones counteract handcuffing by facilitating the dissociation of dimers to monomers or by increasing monomer-to-dimer ratios ( 139 , 142 ).

Citation: Kim J, Bugata V, Cortés-Cortés G, Quevedo-Martínez G, Camps M. 2020. Mechanisms of Theta Plasmid Replication in Enterobacteria and Implications for Adaptation to Its Host, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0026-2019
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Figure 4

Only 233 of the reported sequences were included in this analysis because of strict quality control standards. (A) Pie chart representation of the replicons identified. The replicons are ordered clockwise from most to least abundant: IncF ( = 180), IncI complex ( = 44), ColE ( = 14), IncY ( = 13), IncN ( = 8), IncP ( = 8), IncAC ( = 2), IncR ( = 2), and incL/M ( = 1). IncF denotes the presence of at least one of the following replicons: IncFIA, IncFIB, IncFII, or IncFrepB. The Inc-I complex includes IncI1 ( = 17), IncK ( = 17), and IncBO ( = 10). Note that the number of replicons ( = 272) is greater than the number of samples included ( = 233) because, often, multiple replicons can be found in the same sample. (B) Representation of IncF replicons, which are largely mosaic combinations of IncFIA, IncFIB, IncFII, or IncFrepB. Again, these replicons are ordered clockwise from most to least abundant: IB II repB (49.4%), IA IB II repB (22.8%), IA II repB (8.3%), II repB (6.7%), IA IB (5.6%), IA IB repB (2.2%), IA (1.7%), IB repB (1.1%), repB (1.1%), IA repB (0.6%), and IB (0.6%). Note that these combinations may be found in different plasmids; we are only showing combinations present in the same cell. Note also that we are observing a rapid sequence divergence for IncFII replicons (not shown). Therefore, frequently, IncFII may not have been an exact match for our diagnostic sequence, producing false negatives.

Citation: Kim J, Bugata V, Cortés-Cortés G, Quevedo-Martínez G, Camps M. 2020. Mechanisms of Theta Plasmid Replication in Enterobacteria and Implications for Adaptation to Its Host, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0026-2019
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Figure 5

The average number of replicons for samples that have at least one plasmid is 3.26. If all IncF replicons are considered as a single category, the average number goes down to 1.2.

Citation: Kim J, Bugata V, Cortés-Cortés G, Quevedo-Martínez G, Camps M. 2020. Mechanisms of Theta Plasmid Replication in Enterobacteria and Implications for Adaptation to Its Host, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0026-2019
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Figure 6

Completely assembled plasmid sequences obtained from NCBI as of April 2019 were grouped by Inc type based on the diagnostic PCR amplicons for the PBRT system ( 82 ). Within each incompatibility group, we looked for PFAM matches within a 10-kb window centered around the diagnostic PCR amplicons. PFAM protein families present in at least 75% of the samples in at least one Inc group were identified and mapped to individual open reading frames. These PFAMs were also identified in other Inc groups. These PFAM representation data were compiled into a matrix and plotted using color-coding, with darker colors representing a higher prevalence of protein families within each Inc group. Inc groups are arranged by similarity using a hierarchical clustering algorithm for PFAMs. Note that the percentage can be higher than 100% in the case of duplications or if two domains are found in the same ORF. PFAMs are listed in the axis, grouped in the following color-coded functional categories. Replication initiation-related PFAMs (orange): m5C methylase (PF00145), initiator replication protein (PF01051), and IncFII RepA protein family (PF02387). Plasmid maintenance PFAMs (light blue): PemK endoribonuclease toxin (PF01845) ParB-like nuclease domain (PF02195), StnA protein (PF06406), post-segregation TA CcdA (PF07362), ParB family (PF08775), ParA AAA+ and HT domains (PF13614 PF18607), centromere-binding protein HTH domain (PF18090). Environmental stress protection PFAMs (light gray): MerR family regulatory protein (PF00376), heavy metal-associated domain (PF00403), EamA-like transporter family (PF00892), mercuric transport protein (PF02411), tetracycline repressor family (PF02909 PF00440), MerC mercury resistance protein (PF03203), major facilitator superfamily (PF07690), MerR (PF09278), impB/mucB/samB Y family polymerase (PF13438, PF11799). Conjugation/mobilization PFAMs (green): phage integrase family (PF00589), ProQ/FINO family (PF04352), replication regulatory protein repB (PF10723), TraC_F_IV F pilus assembly (PF11130), DDE domain found in transposases (PF13610). Other PFAMs (white): EAL domain (PF00563), phosphoadenosine phosphosulfate reductase family (PF01507), DUF1281 (PF06924), bacterial IgE domain (PF12245), bacterial IgE-like domain (group3) (PF13750), DUF4165 (PF13752), ferredoxin-like domain in Api92-like protein (PF18406).

Citation: Kim J, Bugata V, Cortés-Cortés G, Quevedo-Martínez G, Camps M. 2020. Mechanisms of Theta Plasmid Replication in Enterobacteria and Implications for Adaptation to Its Host, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0026-2019
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Tables

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Table 1

Comparison of the different modes of plasmid replication

Citation: Kim J, Bugata V, Cortés-Cortés G, Quevedo-Martínez G, Camps M. 2020. Mechanisms of Theta Plasmid Replication in Enterobacteria and Implications for Adaptation to Its Host, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0026-2019
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Table 2

Comparison between DnaA and theta A Rep-mediated replication initiation

Citation: Kim J, Bugata V, Cortés-Cortés G, Quevedo-Martínez G, Camps M. 2020. Mechanisms of Theta Plasmid Replication in Enterobacteria and Implications for Adaptation to Its Host, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0026-2019
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Table 3

Inc plasmid classification and associated biological traits

Citation: Kim J, Bugata V, Cortés-Cortés G, Quevedo-Martínez G, Camps M. 2020. Mechanisms of Theta Plasmid Replication in Enterobacteria and Implications for Adaptation to Its Host, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0026-2019

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