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Article ; Online: Roles of long and short replication initiation proteins in the fate of IncP-1 plasmids.

Yano, Hirokazu / Deckert, Gail E / Rogers, Linda M / Top, Eva M

2012 Volume 194, Issue 6, Page(s) 1533–1543

Abstract: Broad-host-range IncP-1 plasmids generally encode two replication initiation proteins, TrfA1 and TrfA2. TrfA2 is produced from an internal translational start site within trfA1. While TrfA1 was previously shown to be essential for replication in ... ...

Abstract	Broad-host-range IncP-1 plasmids generally encode two replication initiation proteins, TrfA1 and TrfA2. TrfA2 is produced from an internal translational start site within trfA1. While TrfA1 was previously shown to be essential for replication in Pseudomonas aeruginosa, its role in other bacteria within its broad host range has not been established. To address the role of TrfA1 and TrfA2 in other hosts, efficiency of transformation, plasmid copy number (PCN), and plasmid stability were first compared between a mini-IncP-1β plasmid and its trfA1 frameshift variant in four phylogenetically distant hosts: Escherichia coli, Pseudomonas putida, Sphingobium japonicum, and Cupriavidus necator. TrfA2 was sufficient for replication in these hosts, but the presence of TrfA1 enhanced transformation efficiency and PCN. However, TrfA1 did not contribute to, and even negatively affected, long-term plasmid persistence. When trfA genes were cloned under a constitutive promoter in the chromosomes of the four hosts, strains expressing either both TrfA1 and TrfA2 or TrfA1 alone, again, generally elicited a higher PCN of an IncP1-β replicon than strains expressing TrfA2 alone. When a single species of TrfA was produced at different concentrations in E. coli cells, TrfA1 maintained a 3- to 4-fold higher PCN than TrfA2 at the same TrfA concentrations, indicating that replication mediated by TrfA1 is more efficient than that by TrfA2. These results suggest that the broad-host-range properties of IncP-1 plasmids are essentially conferred by TrfA2 and the intact replication origin alone but that TrfA1 is nonetheless important to efficiently establish plasmid replication upon transfer into a broad range of hosts.
MeSH term(s)	DNA Replication ; DNA, Bacterial/genetics ; DNA, Bacterial/metabolism ; Escherichia coli Proteins/genetics ; Escherichia coli Proteins/metabolism ; Genomic Instability ; Gram-Negative Bacteria/genetics ; Gram-Negative Bacteria/metabolism ; Plasmids ; Transformation, Bacterial
Chemical Substances	DNA, Bacterial ; Escherichia coli Proteins ; TrfA protein, E coli
Language	English
Publishing date	2012-01-06
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2968-3
ISSN	1098-5530 ; 0021-9193
ISSN (online)	1098-5530
ISSN	0021-9193
DOI	10.1128/JB.06395-11
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Article: Roles of Long and Short Replication Initiation Proteins in the Fate of IncP-1 Plasmids

Yano, Hirokazu / Deckert, Gail E / Rogers, Linda M / Top, Eva M

Journal of bacteriology. 2012 Mar. 15, v. 194, no. 6

2012

Abstract	Broad-host-range IncP-1 plasmids generally encode two replication initiation proteins, TrfA1 and TrfA2. TrfA2 is produced from an internal translational start site within trfA1. While TrfA1 was previously shown to be essential for replication in Pseudomonas aeruginosa, its role in other bacteria within its broad host range has not been established. To address the role of TrfA1 and TrfA2 in other hosts, efficiency of transformation, plasmid copy number (PCN), and plasmid stability were first compared between a mini-IncP-1β plasmid and its trfA1 frameshift variant in four phylogenetically distant hosts: Escherichia coli, Pseudomonas putida, Sphingobium japonicum, and Cupriavidus necator. TrfA2 was sufficient for replication in these hosts, but the presence of TrfA1 enhanced transformation efficiency and PCN. However, TrfA1 did not contribute to, and even negatively affected, long-term plasmid persistence. When trfA genes were cloned under a constitutive promoter in the chromosomes of the four hosts, strains expressing either both TrfA1 and TrfA2 or TrfA1 alone, again, generally elicited a higher PCN of an IncP1-β replicon than strains expressing TrfA2 alone. When a single species of TrfA was produced at different concentrations in E. coli cells, TrfA1 maintained a 3- to 4-fold higher PCN than TrfA2 at the same TrfA concentrations, indicating that replication mediated by TrfA1 is more efficient than that by TrfA2. These results suggest that the broad-host-range properties of IncP-1 plasmids are essentially conferred by TrfA2 and the intact replication origin alone but that TrfA1 is nonetheless important to efficiently establish plasmid replication upon transfer into a broad range of hosts.
Keywords	Cupriavidus necator ; Escherichia coli ; Pseudomonas aeruginosa ; Pseudomonas putida ; Sphingomonas ; bacteria ; bacteriology ; chromosomes ; genes ; host range ; hosts ; phylogeny ; plasmids ; proteins ; replication origin
Language	English
Dates of publication	2012-0315
Size	p. 1533-1543.
Publishing place	American Society for Microbiology
Document type	Article
ZDB-ID	2968-3
ISSN	1098-5530 ; 0021-9193
ISSN (online)	1098-5530
ISSN	0021-9193
DOI	10.1128/JB.06395-11
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Evolved plasmid-host interactions reduce plasmid interference cost.

Yano, Hirokazu / Wegrzyn, Katarznya / Loftie-Eaton, Wesley / Johnson, Jenny / Deckert, Gail E / Rogers, Linda M / Konieczny, Igor / Top, Eva M

Molecular microbiology

2016 Volume 101, Issue 5, Page(s) 743–756

Abstract: Antibiotic selection drives adaptation of antibiotic resistance plasmids to new bacterial hosts, but the molecular mechanisms are still poorly understood. We previously showed that a broad-host-range plasmid was poorly maintained in Shewanella oneidensis, ...

Abstract	Antibiotic selection drives adaptation of antibiotic resistance plasmids to new bacterial hosts, but the molecular mechanisms are still poorly understood. We previously showed that a broad-host-range plasmid was poorly maintained in Shewanella oneidensis, but rapidly adapted through mutations in the replication initiation gene trfA1. Here we examined if these mutations reduced the fitness cost of TrfA1, and whether this was due to changes in interaction with the host's DNA helicase DnaB. The strains expressing evolved TrfA1 variants showed a higher growth rate than those expressing ancestral TrfA1. The evolved TrfA1 variants showed a lower affinity to the helicase than ancestral TrfA1 and were no longer able to activate the helicase at the oriV without host DnaA. Moreover, persistence of the ancestral plasmid was increased upon overexpression of DnaB. Finally, the evolved TrfA1 variants generated higher plasmid copy numbers than ancestral TrfA1. The findings suggest that ancestral plasmid instability can at least partly be explained by titration of DnaB by TrfA1. Thus under antibiotic selection resistance plasmids can adapt to a novel bacterial host through partial loss of function mutations that simultaneously increase plasmid copy number and decrease unfavorably high affinity to one of the hosts' essential proteins.
MeSH term(s)	DNA Helicases/metabolism ; DNA Replication/genetics ; DNA-Binding Proteins/metabolism ; DnaB Helicases/genetics ; DnaB Helicases/metabolism ; Drug Resistance, Microbial ; Escherichia coli/genetics ; Escherichia coli/metabolism ; Escherichia coli/virology ; Escherichia coli Proteins/genetics ; Escherichia coli Proteins/metabolism ; Plasmids/genetics ; Plasmids/metabolism ; Shewanella/genetics ; Shewanella/virology
Chemical Substances	DNA-Binding Proteins ; Escherichia coli Proteins ; TrfA protein, E coli ; DNA Helicases (EC 3.6.4.-) ; DnaB Helicases (EC 3.6.4.12)
Language	English
Publishing date	2016-06-15
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	619315-8
ISSN	1365-2958 ; 0950-382X
ISSN (online)	1365-2958
ISSN	0950-382X
DOI	10.1111/mmi.13407
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: The impact of spatial structure on viral genomic diversity generated during adaptation to thermal stress.

Ally, Dilara / Wiss, Valorie R / Deckert, Gail E / Green, Danielle / Roychoudhury, Pavitra / Wichman, Holly A / Brown, Celeste J / Krone, Stephen M

PloS one

2014 Volume 9, Issue 2, Page(s) e88702

Abstract: Background: Most clinical and natural microbial communities live and evolve in spatially structured environments. When changes in environmental conditions trigger evolutionary responses, spatial structure can impact the types of adaptive response and ... ...

Abstract	Background: Most clinical and natural microbial communities live and evolve in spatially structured environments. When changes in environmental conditions trigger evolutionary responses, spatial structure can impact the types of adaptive response and the extent to which they spread. In particular, localized competition in a spatial landscape can lead to the emergence of a larger number of different adaptive trajectories than would be found in well-mixed populations. Our goal was to determine how two levels of spatial structure affect genomic diversity in a population and how this diversity is manifested spatially. Methodology/principal findings: We serially transferred bacteriophage populations growing at high temperatures (40°C) on agar plates for 550 generations at two levels of spatial structure. The level of spatial structure was determined by whether the physical locations of the phage subsamples were preserved or disrupted at each passage to fresh bacterial host populations. When spatial structure of the phage populations was preserved, there was significantly greater diversity on a global scale with restricted and patchy distribution. When spatial structure was disrupted with passaging to fresh hosts, beneficial mutants were spread across the entire plate. This resulted in reduced diversity, possibly due to clonal interference as the most fit mutants entered into competition on a global scale. Almost all substitutions present at the end of the adaptation in the populations with disrupted spatial structure were also present in the populations with structure preserved. Conclusions/significance: Our results are consistent with the patchy nature of the spread of adaptive mutants in a spatial landscape. Spatial structure enhances diversity and slows fixation of beneficial mutants. This added diversity could be beneficial in fluctuating environments. We also connect observed substitutions and their effects on fitness to aspects of phage biology, and we provide evidence that some substitutions exclude each other.
MeSH term(s)	Acclimatization/genetics ; Bacteriophages/genetics ; Bacteriophages/physiology ; Cluster Analysis ; Environment ; Escherichia coli/virology ; Genetic Variation ; Genome, Viral ; Genotype ; Hot Temperature ; Mutation ; Oligonucleotides/chemistry ; Phenotype ; Sequence Analysis, DNA
Chemical Substances	Oligonucleotides
Language	English
Publishing date	2014-02-12
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0088702
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: The role of clonal interference in the evolutionary dynamics of plasmid-host adaptation.

Hughes, Julie M / Lohman, Brian K / Deckert, Gail E / Nichols, Eric P / Settles, Matt / Abdo, Zaid / Top, Eva M

mBio

2012 Volume 3, Issue 4, Page(s) e00077–12

Abstract: Unlabelled: Promiscuous plasmids replicate in a wide range of bacteria and therefore play a key role in the dissemination of various host-beneficial traits, including antibiotic resistance. Despite the medical relevance, little is known about the ... ...

Abstract	Unlabelled: Promiscuous plasmids replicate in a wide range of bacteria and therefore play a key role in the dissemination of various host-beneficial traits, including antibiotic resistance. Despite the medical relevance, little is known about the evolutionary dynamics through which drug resistance plasmids adapt to new hosts and thereby persist in the absence of antibiotics. We previously showed that the incompatibility group P-1 (IncP-1) minireplicon pMS0506 drastically improved its stability in novel host Shewanella oneidensis MR-1 after 1,000 generations under antibiotic selection for the plasmid. The only mutations found were those affecting the N terminus of the plasmid replication initiation protein TrfA1. Our aim in this study was to gain insight into the dynamics of plasmid evolution. Changes in stability and genotype frequencies of pMS0506 were monitored in evolving populations of MR-1 (pMS0506). Genotypes were determined by sequencing trfA1 amplicons from individual clones and by 454 pyrosequencing of whole plasmids from entire populations. Stability of pMS0506 drastically improved by generation 200. Many evolved plasmid genotypes with point mutations as well as in-frame and frameshift deletions and duplications in trfA1 were observed in all lineages with both sequencing methods. Strikingly, multiple genotypes were simultaneously present at high frequencies (>10%) in each population. Their relative abundances changed over time, but after 1,000 generations only one or two genotypes dominated the populations. This suggests that hosts with different plasmid genotypes were competing with each other, thus affecting the evolutionary trajectory. Plasmids can thus rapidly improve their stability, and clonal interference plays a significant role in plasmid-host adaptation dynamics. Importance: Promiscuous plasmids play an important role in the spread of antibiotic resistance and many other traits between closely and distantly related bacteria. However, little is known about the dynamics by which these broad-host-range antibiotic resistance plasmids adapt to novel bacteria and thereby become more persistent, even in the absence of antibiotics. In this study, we show that after no more than 200 generations of growth in the presence of antibiotics, a plasmid that was initially poorly maintained in a novel bacterial host evolved to become drastically more persistent in the absence of antibiotics. In each of the evolving populations, an unexpectedly large number of bacterial variants arose with distinct mutations in the plasmid's replication initiation protein. Our results suggest that clonal interference, characterized by competition between variant clones in a population, plays a major role in the evolution of the persistence of drug resistance.
MeSH term(s)	Adaptation, Physiological ; Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Clonal Evolution ; DNA Helicases/genetics ; DNA Helicases/metabolism ; Evolution, Molecular ; Mutation ; Plasmids/genetics ; Plasmids/metabolism ; Shewanella/genetics ; Shewanella/physiology ; Trans-Activators/genetics ; Trans-Activators/metabolism
Chemical Substances	Bacterial Proteins ; Trans-Activators ; replication initiator protein ; DNA Helicases (EC 3.6.4.-)
Language	English
Publishing date	2012-07-03
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2557172-2
ISSN	2150-7511 ; 2161-2129
ISSN (online)	2150-7511
ISSN	2161-2129
DOI	10.1128/mBio.00077-12
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: The Role of Clonal Interference in the Evolutionary Dynamics of Plasmid-Host Adaptation

Hughes, Julie M / Lohman, Brian K / Deckert, Gail E / Nichols, Eric P / Settles, Matt / Abdo, Zaid / Top, Eva M

mBio. 2012 Aug. 31, v. 3, no. 4

2012

Abstract: Promiscuous plasmids replicate in a wide range of bacteria and therefore play a key role in the dissemination of various host-beneficial traits, including antibiotic resistance. Despite the medical relevance, little is known about the evolutionary ... ...

Abstract	Promiscuous plasmids replicate in a wide range of bacteria and therefore play a key role in the dissemination of various host-beneficial traits, including antibiotic resistance. Despite the medical relevance, little is known about the evolutionary dynamics through which drug resistance plasmids adapt to new hosts and thereby persist in the absence of antibiotics. We previously showed that the incompatibility group P-1 (IncP-1) minireplicon pMS0506 drastically improved its stability in novel host Shewanella oneidensis MR-1 after 1,000 generations under antibiotic selection for the plasmid. The only mutations found were those affecting the N terminus of the plasmid replication initiation protein TrfA1. Our aim in this study was to gain insight into the dynamics of plasmid evolution. Changes in stability and genotype frequencies of pMS0506 were monitored in evolving populations of MR-1 (pMS0506). Genotypes were determined by sequencing trfA1 amplicons from individual clones and by 454 pyrosequencing of whole plasmids from entire populations. Stability of pMS0506 drastically improved by generation 200. Many evolved plasmid genotypes with point mutations as well as in-frame and frameshift deletions and duplications in trfA1 were observed in all lineages with both sequencing methods. Strikingly, multiple genotypes were simultaneously present at high frequencies (>10%) in each population. Their relative abundances changed over time, but after 1,000 generations only one or two genotypes dominated the populations. This suggests that hosts with different plasmid genotypes were competing with each other, thus affecting the evolutionary trajectory. Plasmids can thus rapidly improve their stability, and clonal interference plays a significant role in plasmid-host adaptation dynamics. IMPORTANCE Promiscuous plasmids play an important role in the spread of antibiotic resistance and many other traits between closely and distantly related bacteria. However, little is known about the dynamics by which these broad-host-range antibiotic resistance plasmids adapt to novel bacteria and thereby become more persistent, even in the absence of antibiotics. In this study, we show that after no more than 200 generations of growth in the presence of antibiotics, a plasmid that was initially poorly maintained in a novel bacterial host evolved to become drastically more persistent in the absence of antibiotics. In each of the evolving populations, an unexpectedly large number of bacterial variants arose with distinct mutations in the plasmid’s replication initiation protein. Our results suggest that clonal interference, characterized by competition between variant clones in a population, plays a major role in the evolution of the persistence of drug resistance.
Keywords	Shewanella oneidensis ; antibiotic resistance ; antibiotics ; bacteria ; clones ; evolution ; genotype ; hosts ; plasmids ; point mutation ; sequence analysis
Language	English
Dates of publication	2012-0831
Size	p. e00077-12.
Publishing place	American Society for Microbiology
Document type	Article
ZDB-ID	2557172-2
ISSN	2150-7511 ; 2161-2129
ISSN (online)	2150-7511
ISSN	2161-2129
DOI	10.1128/mBio.00077-12
Database	NAL-Catalogue (AGRICOLA)

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Article: His(20) provides the sole functionally significant side chain in the essential TonB transmembrane domain.

Larsen, Ray A / Deckert, Gail E / Kastead, Kyle A / Devanathan, Surendranathan / Keller, Kimberly L / Postle, Kathleen

Journal of bacteriology

2007 Volume 189, Issue 7, Page(s) 2825–2833

Abstract: The cytoplasmic membrane protein TonB couples the protonmotive force of the cytoplasmic membrane to active transport across the outer membrane of Escherichia coli. The uncleaved amino-terminal signal anchor transmembrane domain (TMD; residues 12 to 32) ... ...

Abstract	The cytoplasmic membrane protein TonB couples the protonmotive force of the cytoplasmic membrane to active transport across the outer membrane of Escherichia coli. The uncleaved amino-terminal signal anchor transmembrane domain (TMD; residues 12 to 32) of TonB and the integral cytoplasmic membrane proteins ExbB and ExbD are essential to this process, with important interactions occurring among the several TMDs of all three proteins. Here, we show that, of all the residues in the TonB TMD, only His(20) is essential for TonB activity. When alanyl residues replaced all TMD residues except Ser(16) and His(20), the resultant "all-Ala Ser(16) His(20)" TMD TonB retained 90% of wild-type iron transport activity. Ser(16)Ala in the context of a wild-type TonB TMD was fully active. In contrast, His(20)Ala in the wild-type TMD was entirely inactive. In more mechanistically informative assays, the all-Ala Ser(16) His(20) TMD TonB unexpectedly failed to support formation of disulfide-linked dimers by TonB derivatives bearing Cys substitutions for the aromatic residues in the carboxy terminus. We hypothesize that, because ExbB/D apparently cannot efficiently down-regulate conformational changes at the TonB carboxy terminus through the all-Ala Ser(16) His(20) TMD, the TonB carboxy terminus might fold so rapidly that disulfide-linked dimers cannot be efficiently trapped. In formaldehyde cross-linking experiments, the all-Ala Ser(16) His(20) TMD also supported large numbers of apparently nonspecific contacts with unknown proteins. The all-Ala Ser(16) His(20) TMD TonB retained its dependence on ExbB/D. Together, these results suggest that a role for ExbB/D might be to control rapid and nonspecific folding that the unregulated TonB carboxy terminus otherwise undergoes. Such a model helps to reconcile the crystal/nuclear magnetic resonance structures of the TonB carboxy terminus with conformational changes and mutant phenotypes observed at the TonB carboxy terminus in vivo.
MeSH term(s)	Amino Acid Sequence ; Amino Acid Substitution ; Cell Membrane/metabolism ; Escherichia coli/genetics ; Escherichia coli/metabolism ; Escherichia coli Proteins/chemistry ; Escherichia coli Proteins/genetics ; Escherichia coli Proteins/metabolism ; Genotype ; Histidine ; Kinetics ; Membrane Proteins/chemistry ; Membrane Proteins/genetics ; Membrane Proteins/metabolism ; Molecular Sequence Data ; Phenotype ; Plasmids ; Recombinant Proteins/chemistry ; Recombinant Proteins/metabolism
Chemical Substances	Escherichia coli Proteins ; Membrane Proteins ; Recombinant Proteins ; tonB protein, E coli ; Histidine (4QD397987E)
Language	English
Publishing date	2007-04
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2968-3
ISSN	1098-5530 ; 0021-9193
ISSN (online)	1098-5530
ISSN	0021-9193
DOI	10.1128/JB.01925-06
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Roles of Long and Short Replication Initiation Proteins in the Fate of IncP-1 Plasmids

Yano, Hirokazu / Deckert, Gail E. / Rogers, Linda M. / Top, Eva M.

Journal of bacteriology

Volume v. 194,, Issue no. 6

Abstract	Broad-host-range IncP-1 plasmids generally encode two replication initiation proteins, TrfA1 and TrfA2. TrfA2 is produced from an internal translational start site within trfA1. While TrfA1 was previously shown to be essential for replication in Pseudomonas aeruginosa, its role in other bacteria within its broad host range has not been established. To address the role of TrfA1 and TrfA2 in other hosts, efficiency of transformation, plasmid copy number (PCN), and plasmid stability were first compared between a mini-IncP-1β plasmid and its trfA1 frameshift variant in four phylogenetically distant hosts: Escherichia coli, Pseudomonas putida, Sphingobium japonicum, and Cupriavidus necator. TrfA2 was sufficient for replication in these hosts, but the presence of TrfA1 enhanced transformation efficiency and PCN. However, TrfA1 did not contribute to, and even negatively affected, long-term plasmid persistence. When trfA genes were cloned under a constitutive promoter in the chromosomes of the four hosts, strains expressing either both TrfA1 and TrfA2 or TrfA1 alone, again, generally elicited a higher PCN of an IncP1-β replicon than strains expressing TrfA2 alone. When a single species of TrfA was produced at different concentrations in E. coli cells, TrfA1 maintained a 3- to 4-fold higher PCN than TrfA2 at the same TrfA concentrations, indicating that replication mediated by TrfA1 is more efficient than that by TrfA2. These results suggest that the broad-host-range properties of IncP-1 plasmids are essentially conferred by TrfA2 and the intact replication origin alone but that TrfA1 is nonetheless important to efficiently establish plasmid replication upon transfer into a broad range of hosts.
Keywords	genes ; phylogeny ; host range ; replication origin ; Cupriavidus necator ; Sphingomonas ; chromosomes ; bacteria ; Escherichia coli ; hosts ; plasmids ; Pseudomonas putida ; Pseudomonas aeruginosa ; proteins ; bacteriology
Language	English
Document type	Article
ISSN	0021-9193
Database	AGRIS - International Information System for the Agricultural Sciences and Technology

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