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Novel Plasmids and Resistance Phenotypes in Yersinia pestis: Unique Plasmid Inventory of Strain Java 9 Mediates High Levels of Arsenic Resistance

Journal Article · · PLoS ONE
 [1];  [2];  [2];  [3];  [4];  [4];  [5];  [4]
  1. Univ. of Maryland Baltimore County (UMBC), Baltimore, MD (United States). School of Medicine, Dept. of Microbiology and Immunology and Inst. for Genome Sciences; DOE/OSTI
  2. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
  3. U.S. Army Medical Research Inst. of Infectious Diseases, Fort Detrick, MD (United States). Bacteriology Division
  4. U.S. Army Medical Research Inst. of Infectious Diseases, Fort Detrick, MD (United States). Bacteriology Division
  5. Univ. of Maryland Baltimore County (UMBC), Baltimore, MD (United States). School of Medicine, Dept. of Microbiology and Immunology and Inst. for Genome Sciences

Growing evidence suggests that the plasmid repertoire of Yersinia pestis is not restricted to the three classical virulence plasmids. The Java 9 strain of Y. pestis is a biovar Orientalis isolate obtained from a rat in Indonesia. Although it lacks the Y. pestis-specific plasmid pMT, which encodes the F1 capsule, it retains virulence in mouse and non-human primate animal models. While comparing diverse Y. pestis strains using subtractive hybridization, we identified sequences in Java 9 that were homologous to a Y. enterocolitica strain carrying the transposon Tn2502, which is known to encode arsenic resistance. Here we demonstrate that Java 9 exhibits high levels of arsenic and arsenite resistance mediated by a novel promiscuous class II transposon, named Tn2503. Arsenic resistance was self-transmissible from Java 9 to other Y. pestis strains via conjugation. Genomic analysis of the atypical plasmid inventory of Java 9 identified pCD and pPCP plasmids of atypical size and two previously uncharacterized cryptic plasmids. Unlike the Tn2502-mediated arsenic resistance encoded on the Y. enterocolitica virulence plasmid; the resistance loci in Java 9 are found on all four indigenous plasmids, including the two novel cryptic plasmids. This unique mobilome introduces more than 105 genes into the species gene pool. The majority of these are encoded by the two entirely novel self-transmissible plasmids, which show partial homology and synteny to other enterics. In contrast to the reductive evolution in Y. pestis, this study underlines the major impact of a dynamic mobilome and lateral acquisition in the genome evolution of the plague bacterium.

Research Organization:
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; Defense Threat Reduction Agency (DTRA); US Department of the Army; National Institute of Allergy and Infectious Diseases (NIAID); National Institutes of Health (NIH); US Department of Health and Human Services (HHS)
Grant/Contract Number:
AC52-07NA27344
OSTI ID:
1627503
Journal Information:
PLoS ONE, Journal Name: PLoS ONE Journal Issue: 3 Vol. 7; ISSN 1932-6203
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English

References (56)

Plasmid R6K Contains Two FunctionaloriTswhich can Assemble Simultaneously in Relaxosomesin vivo journal August 1996
The Yersiniae — a model genus to study the rapid evolution of bacterial pathogens journal October 2003
Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis journal September 2004
Experimental evidence for negative selection in the evolution of a Yersinia pestis pseudogene journal June 2008
Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis journal November 1999
DNA sequence of the transposase gene of the new category of class II transposon, Tn2501 journal January 1987
The divergent chromosomal ars operon of Acidithiobacillus ferrooxidans is regulated by an atypical ArsR protein journal December 2002
An unusual Tn21-like transposon containing an ars operon is present in highly arsenic-resistant strains of the biomining bacterium Acidithiobacillus caldus journal September 2005
Microbial arsenic: from geocycles to genes and enzymes journal August 2002
Draft Genome Sequences of Yersinia pestis Isolates from Natural Foci of Endemic Plague in China journal October 2009
The Virulence Plasmid of Yersinia, an Antihost Genome journal December 1998
The Complete Genome Sequence of Yersinia pseudotuberculosis IP31758, the Causative Agent of Far East Scarlet-Like Fever journal August 2007
Complete DNA Sequence and Analysis of an Emerging Cryptic Plasmid Isolated from Yersinia pestis journal March 2000
Site-specific recombinations between direct and inverted res sites of Tn2501 journal November 1989
Arsenical resistance in the IncHI2 plasmids journal May 2002
An experimental field study to evaluate a trap-barrier system and fumigation for controlling the rice field rat, Rattus argentiventer, in rice crops in West Java journal February 1998
Identification of encapsulated and non-encapsulated Yersinia pestis by immunofluorescence tests using polyclonal and monoclonal antibodies journal August 1988
Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18 journal October 2001
Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity journal October 2010
Genes involved in conjugative DNA processing of plasmid R6K journal June 1997
Multidrug Resistance in Yersinia pestis Mediated by a Transferable Plasmid journal September 1997
Genomic anatomy of Escherichia coli O157:H7 outbreaks journal November 2011
Design of a compartmentalized shotgun assembler for the human genome journal June 2001
Relationship Between Virulence and Immunity as Revealed in Recent Studies of the Fl Capsule of Yersinia pestis journal October 1995
Complete Genome Sequence of Yersinia pestis Strain 91001, an Isolate Avirulent to Humans journal January 2004
Temperature sensitivity of transposition of class II transposons journal January 1990
Genome plasticity in Yersinia pestis journal June 2002
A Caenorhabditis elegans model of Yersinia infection: biofilm formation on a biotic surface journal November 2003
Plasmid content in Yersinia pestis strains of different origin journal January 1990
Role of Yersinia Murine Toxin in Survival of Yersinia pestis in the Midgut of the Flea Vector journal April 2002
The Chromosomal Arsenic Resistance Genes of Thiobacillus ferrooxidans Have an Unusual Arrangement and Confer Increased Arsenic and Antimony Resistance to Escherichia coli journal May 2000
Resistance Determinants of a Highly Arsenic-Resistant Strain of Leptospirillum ferriphilum Isolated from a Commercial Biooxidation Tank journal March 2006
Yersinia pestis YopJ Suppresses Tumor Necrosis Factor Alpha Induction and Contributes to Apoptosis of Immune Cells in the Lymph Node but Is Not Required for Virulence in a Rat Model of Bubonic Plague journal September 2006
Structural Organization of the pFra Virulence-Associated Plasmid of Rhamnose-Positive Yersinia pestis journal October 2004
Complete Genome Sequence of Yersinia pestis Strains Antiqua and Nepal516: Evidence of Gene Reduction in an Emerging Pathogen journal June 2006
Draft Genome Sequences of Yersinia pestis Isolates from Natural Foci of Endemic Plague in China journal October 2009
Genome Sequence of the Deep-Rooted Yersinia pestis Strain Angola Reveals New Insights into the Evolution and Pangenome of the Plague Bacterium journal January 2010
Detection and characterization of Tn2501, a transposon included within the lactose transposon Tn951. journal January 1984
Genome Sequence of Yersinia pestis KIM journal August 2002
Diversity in a Variable-Number Tandem Repeat fromYersinia pestis journal January 2000
The Virulence Plasmid of Yersinia, an Antihost Genome journal December 1998
Tn2501, a component of the lactose transposon Tn951, is an example of a new category of class II transposable elements. journal January 1987
The ars operon of Escherichia coli confers arsenical and antimonial resistance. journal February 1995
Virulence and arsenic resistance in Yersiniae. journal January 1997
Arsenic and cadmium resistance in environmental isolates of Yersinia enterocolitica and Yersinia intermedia journal May 2000
YopH inhibits early pro-inflammatory cytokine responses during plague pneumonia journal January 2010
Versatile and open software for comparing large genomes journal January 2004
Arsenate reductases in prokaryotes and eukaryotes. journal October 2002
Detection of Conjugation Related Type Four Secretion Machinery in Aeromonas culicicola journal December 2006
Multiple Antimicrobial Resistance in Plague: An Emerging Public Health Risk journal March 2007
Klebsiella pneumoniae Multiresistance Plasmid pMET1: Similarity with the Yersinia pestis Plasmid pCRY and Integrative Conjugative Elements journal March 2008
Differential Control of Yersinia pestis Biofilm Formation In Vitro and in the Flea Vector by Two c-di-GMP Diguanylate Cyclases journal April 2011
Genomic Evidence for the Evolution of Streptococcus equi: Host Restriction, Increased Virulence, and Genetic Exchange with Human Pathogens journal March 2009
Atypical plague bacilli isolated from rodents, fleas, and man. journal March 1978
An Electrophoretic and Bacteriologic Study of Yersinia Pestis Isolates from Central Java, Asia, and the Western Hemisphere journal September 1973
A cryptic 19-kilobase plasmid associated with U.S. isolates of Yersinia pestis: a dimer of the 9.5-kilobase plasmid. journal November 1998

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Overcoming Fish Defences: The Virulence Factors of Yersinia ruckeri journal September 2019

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