Environmentally co-occurring mercury resistance plasmids are genetically and phenotypically diverse and confer variable context-dependent fitness effects

James P. J. Hall, Ellie Harrison, Andrew K. Lilley, Steve Paterson, Andrew J. Spiers, Michael A. Brockhurst

Research output: Contribution to journalArticle

17 Citations (Scopus)
15 Downloads (Pure)

Abstract

Plasmids are important mobile elements that can facilitate genetic exchange and local adaptation within microbial communities. We compared the sequences of four co-occurring pQBR-family environmental mercury resistance plasmids and measured their effects on competitive fitness of a Pseudomonas fluorescens SBW25 host, which was isolated at the same field site. Fitness effects of carriage differed between plasmids and were strongly context dependent, varying with medium, plasmid status of competitor and levels of environmental mercury. The plasmids also varied widely in their rates of conjugation and segregational loss. We found that few of the plasmid-borne accessory genes could be ascribed functions, although we identified a putative chemotaxis operon, a type IV pilus-encoding cluster, and a region encoding putative arylsulfatase enzymes, which were conserved across geographically distant isolates. One plasmid, pQBR55, conferred the ability to catabolise sucrose. Transposons, including the mercury resistance Tn5042, appeared to have been acquired by the different pQBR plasmids by recombination, indicating an important role for horizontal gene transfer in the recent evolution of pQBR plasmids. Our findings demonstrate extensive genetic and phenotypic diversity amongst co-occurring members of a plasmid community and suggest a role for environmental heterogeneity in the maintenance of plasmid diversity.
Original languageEnglish
Pages (from-to)5008-5022
Number of pages15
JournalEnvironmental Microbiology
Volume17
Issue number12
Early online date25 Jun 2015
DOIs
Publication statusPublished - Dec 2015

Fingerprint

Mercury
plasmid
mercury
plasmids
Plasmids
fitness
effect
Arylsulfatases
chemotaxis
Horizontal Gene Transfer
Pseudomonas fluorescens
arylsulfatase
Aptitude
gene transfer
local adaptation
fimbriae
Chemotaxis
operon
Operon
sucrose

Cite this

Hall, James P. J. ; Harrison, Ellie ; Lilley, Andrew K. ; Paterson, Steve ; Spiers, Andrew J. ; Brockhurst, Michael A. / Environmentally co-occurring mercury resistance plasmids are genetically and phenotypically diverse and confer variable context-dependent fitness effects. In: Environmental Microbiology. 2015 ; Vol. 17, No. 12. pp. 5008-5022.
@article{ba9defed78ae4e6eb010983f9daf9a98,
title = "Environmentally co-occurring mercury resistance plasmids are genetically and phenotypically diverse and confer variable context-dependent fitness effects",
abstract = "Plasmids are important mobile elements that can facilitate genetic exchange and local adaptation within microbial communities. We compared the sequences of four co-occurring pQBR-family environmental mercury resistance plasmids and measured their effects on competitive fitness of a Pseudomonas fluorescens SBW25 host, which was isolated at the same field site. Fitness effects of carriage differed between plasmids and were strongly context dependent, varying with medium, plasmid status of competitor and levels of environmental mercury. The plasmids also varied widely in their rates of conjugation and segregational loss. We found that few of the plasmid-borne accessory genes could be ascribed functions, although we identified a putative chemotaxis operon, a type IV pilus-encoding cluster, and a region encoding putative arylsulfatase enzymes, which were conserved across geographically distant isolates. One plasmid, pQBR55, conferred the ability to catabolise sucrose. Transposons, including the mercury resistance Tn5042, appeared to have been acquired by the different pQBR plasmids by recombination, indicating an important role for horizontal gene transfer in the recent evolution of pQBR plasmids. Our findings demonstrate extensive genetic and phenotypic diversity amongst co-occurring members of a plasmid community and suggest a role for environmental heterogeneity in the maintenance of plasmid diversity.",
author = "Hall, {James P. J.} and Ellie Harrison and Lilley, {Andrew K.} and Steve Paterson and Spiers, {Andrew J.} and Brockhurst, {Michael A.}",
year = "2015",
month = "12",
doi = "10.1111/1462-2920.12901",
language = "English",
volume = "17",
pages = "5008--5022",
journal = "Environmental Microbiology",
issn = "1462-2912",
publisher = "Wiley-Blackwell",
number = "12",

}

Environmentally co-occurring mercury resistance plasmids are genetically and phenotypically diverse and confer variable context-dependent fitness effects. / Hall, James P. J.; Harrison, Ellie; Lilley, Andrew K.; Paterson, Steve; Spiers, Andrew J.; Brockhurst, Michael A.

In: Environmental Microbiology, Vol. 17, No. 12, 12.2015, p. 5008-5022.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Environmentally co-occurring mercury resistance plasmids are genetically and phenotypically diverse and confer variable context-dependent fitness effects

AU - Hall, James P. J.

AU - Harrison, Ellie

AU - Lilley, Andrew K.

AU - Paterson, Steve

AU - Spiers, Andrew J.

AU - Brockhurst, Michael A.

PY - 2015/12

Y1 - 2015/12

N2 - Plasmids are important mobile elements that can facilitate genetic exchange and local adaptation within microbial communities. We compared the sequences of four co-occurring pQBR-family environmental mercury resistance plasmids and measured their effects on competitive fitness of a Pseudomonas fluorescens SBW25 host, which was isolated at the same field site. Fitness effects of carriage differed between plasmids and were strongly context dependent, varying with medium, plasmid status of competitor and levels of environmental mercury. The plasmids also varied widely in their rates of conjugation and segregational loss. We found that few of the plasmid-borne accessory genes could be ascribed functions, although we identified a putative chemotaxis operon, a type IV pilus-encoding cluster, and a region encoding putative arylsulfatase enzymes, which were conserved across geographically distant isolates. One plasmid, pQBR55, conferred the ability to catabolise sucrose. Transposons, including the mercury resistance Tn5042, appeared to have been acquired by the different pQBR plasmids by recombination, indicating an important role for horizontal gene transfer in the recent evolution of pQBR plasmids. Our findings demonstrate extensive genetic and phenotypic diversity amongst co-occurring members of a plasmid community and suggest a role for environmental heterogeneity in the maintenance of plasmid diversity.

AB - Plasmids are important mobile elements that can facilitate genetic exchange and local adaptation within microbial communities. We compared the sequences of four co-occurring pQBR-family environmental mercury resistance plasmids and measured their effects on competitive fitness of a Pseudomonas fluorescens SBW25 host, which was isolated at the same field site. Fitness effects of carriage differed between plasmids and were strongly context dependent, varying with medium, plasmid status of competitor and levels of environmental mercury. The plasmids also varied widely in their rates of conjugation and segregational loss. We found that few of the plasmid-borne accessory genes could be ascribed functions, although we identified a putative chemotaxis operon, a type IV pilus-encoding cluster, and a region encoding putative arylsulfatase enzymes, which were conserved across geographically distant isolates. One plasmid, pQBR55, conferred the ability to catabolise sucrose. Transposons, including the mercury resistance Tn5042, appeared to have been acquired by the different pQBR plasmids by recombination, indicating an important role for horizontal gene transfer in the recent evolution of pQBR plasmids. Our findings demonstrate extensive genetic and phenotypic diversity amongst co-occurring members of a plasmid community and suggest a role for environmental heterogeneity in the maintenance of plasmid diversity.

U2 - 10.1111/1462-2920.12901

DO - 10.1111/1462-2920.12901

M3 - Article

VL - 17

SP - 5008

EP - 5022

JO - Environmental Microbiology

JF - Environmental Microbiology

SN - 1462-2912

IS - 12

ER -