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The Plasmidome of Firmicutes: Impact on the Emergence and the Spread of Resistance to Antimicrobials

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  • Authors: Val Fernández Lanza1, Ana P. Tedim4, José Luís Martínez7, Fernando Baquero9, Teresa M. Coque12
  • Editors: Marcelo Tolmasky15, Juan Carlos Alonso16
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Servicio de Microbiología, Hospital Universitario Ramón y Cajal, Instituto Ramón y Cajal de Investigación Sanitaria (IRYCIS), Madrid, Spain; 2: Unidad de Resistencia a Antibióticos y Virulencia Bacteriana (HRYC-CSIC), Madrid, Spain; 3: Centro de Investigación en Red en Epidemiología y Salud Pública (CIBER-ESP), Spain; 4: Servicio de Microbiología, Hospital Universitario Ramón y Cajal, Instituto Ramón y Cajal de Investigación Sanitaria (IRYCIS), Madrid, Spain; 5: Unidad de Resistencia a Antibióticos y Virulencia Bacteriana (HRYC-CSIC), Madrid, Spain; 6: Centro de Investigación en Red en Epidemiología y Salud Pública (CIBER-ESP), Spain; 7: Unidad de Resistencia a Antibióticos y Virulencia Bacteriana (HRYC-CSIC), Madrid, Spain; 8: Centro Nacional de Biotecnología (CNB-CSIC), Madrid, Spain; 9: Servicio de Microbiología, Hospital Universitario Ramón y Cajal, Instituto Ramón y Cajal de Investigación Sanitaria (IRYCIS), Madrid, Spain; 10: Unidad de Resistencia a Antibióticos y Virulencia Bacteriana (HRYC-CSIC), Madrid, Spain; 11: Centro de Investigación en Red en Epidemiología y Salud Pública (CIBER-ESP), Spain; 12: Servicio de Microbiología, Hospital Universitario Ramón y Cajal, Instituto Ramón y Cajal de Investigación Sanitaria (IRYCIS), Madrid, Spain; 13: Unidad de Resistencia a Antibióticos y Virulencia Bacteriana (HRYC-CSIC), Madrid, Spain; 14: Centro de Investigación en Red en Epidemiología y Salud Pública (CIBER-ESP), Spain; 15: California State University, Fullerton, CA; 16: Centro Nacional de Biotecnología, Cantoblanco, Madrid, Spain
  • Source: microbiolspec April 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.PLAS-0039-2014
  • Received 14 January 2015 Accepted 15 January 2015 Published 03 April 2015
  • Teresa M. Coque, mariateresa.coque@salud.madrid.org; teresacoque@gmail.com
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  • Abstract:

    The phylum is one of the most abundant groups of prokaryotes in the microbiota of humans and animals and includes genera of outstanding relevance in biomedicine, health care, and industry. Antimicrobial drug resistance is now considered a global health security challenge of the 21st century, and this heterogeneous group of microorganisms represents a significant part of this public health issue.

    The presence of the same resistant genes in unrelated bacterial genera indicates a complex history of genetic interactions. Plasmids have largely contributed to the spread of resistance genes among , , and species, also influencing the selection and ecological variation of specific populations. However, this information is fragmented and often omits species outside these genera. To date, the antimicrobial resistance problem has been analyzed under a “single centric” perspective (“gene tracking” or “vehicle centric” in “single host-single pathogen” systems) that has greatly delayed the understanding of gene and plasmid dynamics and their role in the evolution of bacterial communities.

    This work analyzes the dynamics of antimicrobial resistance genes using gene exchange networks; the role of plasmids in the emergence, dissemination, and maintenance of genes encoding resistance to antimicrobials (antibiotics, heavy metals, and biocides); and their influence on the genomic diversity of the main Gram-positive opportunistic pathogens under the light of evolutionary ecology. A revision of the approaches to categorize plasmids in this group of microorganisms is given using the 1,326 fully sequenced plasmids of Gram-positive bacteria available in the GenBank database at the time the article was written.

  • Citation: Lanza V, Tedim A, Martínez J, Baquero F, Coque T. 2015. The Plasmidome of Firmicutes: Impact on the Emergence and the Spread of Resistance to Antimicrobials. Microbiol Spectrum 3(2):PLAS-0039-2014. doi:10.1128/microbiolspec.PLAS-0039-2014.

Key Concept Ranking

Mobile Genetic Elements
0.4647078
Type IV Secretion Systems
0.42010155
0.4647078

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/content/journal/microbiolspec/10.1128/microbiolspec.PLAS-0039-2014
2015-04-03
2017-11-18

Abstract:

The phylum is one of the most abundant groups of prokaryotes in the microbiota of humans and animals and includes genera of outstanding relevance in biomedicine, health care, and industry. Antimicrobial drug resistance is now considered a global health security challenge of the 21st century, and this heterogeneous group of microorganisms represents a significant part of this public health issue.

The presence of the same resistant genes in unrelated bacterial genera indicates a complex history of genetic interactions. Plasmids have largely contributed to the spread of resistance genes among , , and species, also influencing the selection and ecological variation of specific populations. However, this information is fragmented and often omits species outside these genera. To date, the antimicrobial resistance problem has been analyzed under a “single centric” perspective (“gene tracking” or “vehicle centric” in “single host-single pathogen” systems) that has greatly delayed the understanding of gene and plasmid dynamics and their role in the evolution of bacterial communities.

This work analyzes the dynamics of antimicrobial resistance genes using gene exchange networks; the role of plasmids in the emergence, dissemination, and maintenance of genes encoding resistance to antimicrobials (antibiotics, heavy metals, and biocides); and their influence on the genomic diversity of the main Gram-positive opportunistic pathogens under the light of evolutionary ecology. A revision of the approaches to categorize plasmids in this group of microorganisms is given using the 1,326 fully sequenced plasmids of Gram-positive bacteria available in the GenBank database at the time the article was written.

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FIGURE 1

Protein content network (PCN) of AbR proteins found in plasmids and chromosomes of and . To determine the AbR protein catalog of Gram-positive strains (chromosomes and plasmids), a Blastp search was performed of all their proteomes against the ARG-ANNOT database (http://en.mediterranee-infection.com/article.php?laref=283&titre=arg-annot) using a cut-off of 1e-30 and 85% of identity. The presence of the Gram-positive AbR proteins identified above in all bacterial species (only complete sequences, not partial) was determined using a similar Blast search (blastp, 1e-30 E-value and 85% identity) against the NCBI GenBank database. The nodes correspond to bacterial species (circular nodes; each color indicates one genus) and AbR proteins (square nodes). Nodes were connected by an edge when a positive hit between AbR proteins and one or more strains of a given species were identified. Edges further indicate the location of the AbR genes associated with each AbR protein of the Gram-positive catalog. Solid lines represent chromosomal location, and dotted lines represent plasmid location. When an AbR gene was located in both chromosomes and plasmids, both lines were plotted. doi:10.1128/microbiolspec.PLAS-0039-2014.f1

Source: microbiolspec April 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.PLAS-0039-2014
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FIGURE 2

PCN of metal-biocide (Met/Bc) proteins found in plasmids and chromosomes of and . To determine the Met/Bc protein catalog of Gram-positive strains (chromosomes and plasmids), a Blastp search was performed of all their proteomes against the BacMet database (http://bacmet.biomedicine.gu.se/) using a cut-off of 1e-30 and 85% of identity. The presence of the Gram-positive Met/Bc proteins identified above in all bacterial species (only complete sequences, not partial) was determined using a similar Blastp search (blastp, 1e-30 evalue and 85% identity) against the NCBI GenBank database. The nodes correspond to bacterial species (circular nodes) and Met/Bc proteins (triangular nodes). Nodes were connected by an edge when a positive hit between Met/Bc proteins on one or more strains of a given species was identified. Edges further indicate the location of the Met/Bc genes associated with each Met/Bc protein of the Gram-positive catalog. Solid lines represent chromosomal location, and dotted lines represent plasmid location. When a Met/Bc gene was located in both chromosomes and plasmids, both lines were plotted. doi:10.1128/microbiolspec.PLAS-0039-2014.f2

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FIGURE 3

Plasmid homology network. The genomic homology network was performed using “All-versus-All” genomic Megablast ( 238 ) of 1,326 fully sequenced plasmids from low G+C bacterial species ( and phyla) available at public gene databases. The nodes correspond to bacterial plasmids (circular nodes; different colors representing different genera). Two nodes are connected by an edge if they share homologous DNA. doi:10.1128/microbiolspec.PLAS-0039-2014.f3

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PCN of AbR and Met/Bc proteins located on plasmids of and . PCN of AbR and Met proteins found in Gram-positive plasmids. We formed the PCN by representing plasmids as circular nodes, AbR as square nodes, and Met/Bc as triangular nodes, connecting two nodes (plasmid and AbR or Met/Bc) if one plasmid has this AbR or Met/Bc. The presence of the Met/Bc gene was determined by blasp of all plasmid proteins against the BacMet database. The presence of the AbR gene was determined by blasp of all plasmid proteins against the ARG-ANNOT database. The colors for the genus are the same as those in Fig. 3 . doi:10.1128/microbiolspec.PLAS-0039-2014.f4

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FIGURE 5

Plasmids from spp. The presence of an orange border in the RIP family indicates that the corresponding RIP is truncated. PriCT_1; *One of these plasmids (GenBank accession number NC_013381) has a truncated rep_pKH21 (rep_1) gene, and no other known RIPs were identified. **Two of these plasmids (GenBank accession number NC_016054 and NC_019144) appear to have two copies of the MOB gene. One of these plasmids (GenBank accession number NC_008354) has two copies of the gene. One plasmid (GenBank accession number NC_001393) has a truncated copy of the gene. One plasmid (GenBank accession number NC_010419) has a truncated copy of the gene. The plasmid (GenBank accession number NC_005076) appears to have two copies of the MOB gene. One plasmid (GenBank accession number NC_018959) has a truncated copy of the gene. Two plasmids (GenBank accession numbers NC_007931 and NC_016942) have two copies of the and genes. This plasmid (GenBank accession number NC_013320) appears to have two copies of the MOB gene. This plasmid (GenBank accession number NC_005004) has a truncated copy of the gene. Three plasmids (GenBank accession numbers NC_013321, NC_019007, and NC_018976) have a truncated copy of the gene. Eleven of these plasmids have a truncated copy of the gene (GenBank accession numbers NC_020531, NC_020538, NC_013337, NC_020534, NC_020565, NC_020567, NC_020530, NC_020539, NC_017352, NC_013323, and NC_022610). One plasmid (GenBank accession number NC_013334) has a truncated copy of the gene. This plasmid (GenBank accession number NC_020237) appears to have two copies of the MOB gene. This plasmid (GenBank accession number NC_022598) appears to have two copies of the MOB gene. Abbreviations: MRIP, Multi-RIP; S, spp; Sar, ; Sa, ; Sc, ; Se, ; Sha, ; Shy, ; Sle, ; Slu, ; Sp, ; Ssa, ; Ssc, ; Ssi, ; Sw, . doi:10.1128/microbiolspec.PLAS-0039-2014.f5

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Hierarchical clustering dendrogram of plasmids from enterococci. The matrix distance used for building the UPGMA dendrogram is based on the Raup-Crick distance of the orthologous protein profile of each plasmid. For each plasmid, a presence/absence protein profile was made using cut-off values of 80% identity and 80% coverage. Protein clustering was made by using CD-HIT ( 239 ). Different background colors are used to emphasize branches of related plasmids and are the same as those defined in Fig. 5 . Names to the left of the dendrogram indicate the RIP family. Background colors were used to point out plasmid groups frequently involved in mobility of AbR genes and pheromone-responsive plasmids. Circles indicate RIPs identified in each plasmid according to data shown in Fig. 7 . doi:10.1128/microbiolspec.PLAS-0039-2014.f6

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FIGURE 7

Plasmids from spp. The presence of an orange border in the RIP family indicates that the corresponding RIP is truncated. Rep_2; *One of these plasmids (GenBank accession number NC_015849) has a truncated rep_AUS0004_p2 (Rep_1) gene, and no other known replication initiator proteins were found. **This plasmid (GenBank accession number NC_017962) has two copies of Tn; in one of them the gene is not truncated; this plasmid also appears to have two copies of the MOB gene. These two plasmids (GenBank accession numbers NC_008768 and NC_008821) have a truncated copy of the gene. Abbreviations: MRIP, multi-RIP; Efm, ; Efc, ; Emu, ; Edu, ; Ehi, . doi:10.1128/microbiolspec.PLAS-0039-2014.f7

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FIGURE 8

Plasmids from spp. Rep_trans; This plasmid (GenBank accession number NC_015219) has two similar replication genes belonging to the Rep_3 family. This plasmid (GenBank accession number NC_006979) has two similar replication genes belonging to the PriCT_1 family. Abbreviations: MRIP, Multi-RIP; Sag, ; Sdy, ; Sga, ; Siu, ; Sin, ; Sma, ; Smu, ; Spa, ; Spn, ; Sps, ; Spy, ; Ssu, ; Sth, doi:10.1128/microbiolspec.PLAS-0039-2014.f8

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FIGURE 9

Plasmids from spp. rep_3. One plasmid (GenBank NC_013767) has two copies of the gene, one of which is truncated. One plasmid (GenBank NC_018888) has a truncated copy of the gene. This plasmid (GenBank NC_022045) has two copies of the operon. Abbreviations: MRIP, multi-RIP; Lm, ; Lg, ; Li, doi:10.1128/microbiolspec.PLAS-0039-2014.f9

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FIGURE 10

Plasmids from LAB. Rep_1. Rep_trans. PriCT_1. *This plasmid (GenBank accession number NC_010540) has two copies of the gene. **One of these plasmids (GenBank accession number NC_010603) has a truncated copy of the gene. One of these plasmids (GenBank accession number NC_014133) appears to have three copies of the MOB gene. One of these plasmids (GenBank accession number NC_022123) appears to have two copies of the MOB gene. Abbreviations: MRip, multi-RIP; Lb, spp; Lca, ; Lam, ; Lbr, ; Lbu, ; Lca, ; Lfe ; Lpa, ; Lpl, ; Lre, ; Lsa, Lga, ; Lla, ; Lcm, ; Lci, ; Lki, ; Lme, doi:10.1128/microbiolspec.PLAS-0039-2014.f10

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FIGURE 11

Similarity of -like sequences encoding RIPs of the Rep_1 family. A neighbor-joining tree of gene sequences coding for RIPs of the Rep_1 family was built using MEGA 6.06. A cut-off equal to or higher than 80% and a bootstrap analysis based on 1,000 permutations were applied to the analysis. Alignment of nucleotide sequences was performed using ClustalW2 (http://www.ebi.ac.uk/Tools/phylogeny/clustalw2_phylogeny/), and sequences showing an identity equal to or higher than 80% were clustered in groups that were highlighted by different backgrounds colors. Black dots indicate the RIP of the plasmid used for further comparison in Figs. 5 to 10 . doi:10.1128/microbiolspec.PLAS-0039-2014.f11

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FIGURE 12

Similarity of -like sequences encoding RIPs of the Rep_trans family. A neighbor-joining tree of gene sequences coding for RIPs of the Rep_trans family was built using MEGA 6.06. A cut-off equal to or higher than 80% and a bootstrap analysis based on 1,000 permutations were applied to the analysis. Alignment of nucleotide sequences was performed using ClustalW2 (http://www.ebi.ac.uk/Tools/phylogeny/clustalw2_phylogeny/), and sequences showing an identity equal to or higher than 80% were clustered in groups that were highlighted by different backgrounds colors. Black dots indicate the RIP of the plasmid used for further comparison in Figs. 5 to 10 . *Truncated gene. **Similar to and . Abbreviations: ND, not determined. doi:10.1128/microbiolspec.PLAS-0039-2014.f12

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FIGURE 13

Similarity of -like sequences encoding RIPs of the Rep_2 family. A neighbor-joining tree of gene sequences coding for RIPs of the Rep_2 family was built using MEGA 6.06. A cut-off equal to or higher than 80% and a bootstrap analysis based on 1,000 permutations were applied to the analysis. Alignment of nucleotide sequences was performed using ClustalW2 (http://www.ebi.ac.uk/Tools/phylogeny/clustalw2_phylogeny/), and sequences showing an identity equal to or higher than 80% were clustered in groups that were highlighted by different background colors. Black dots indicate the RIP of the plasmid used for further comparison in Figs. 5 to 10 . doi:10.1128/microbiolspec.PLAS-0039-2014.f13

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FIGURE 14

Similarity of -like sequences encoding RIPs of the Rep_L family. A neighbor-joining tree of gene sequences coding for RIPs of the Rep_L family was built using MEGA 6.06. A cut-off equal to or higher than 80% and a bootstrap analysis based on 1,000 permutations were applied to the analysis. Alignment of nucleotide sequences was performed using ClustalW2 (http://www.ebi.ac.uk/Tools/phylogeny/clustalw2_phylogeny/), and sequences showing an identity equal to or higher than 80% were clustered in groups that were highlighted by different background colors. Black dots indicate the RIP of the plasmid used for further comparison in Figs. 5 to 10 . doi:10.1128/microbiolspec.PLAS-0039-2014.f14

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FIGURE 15

Similarity of -like sequences encoding RIPs of the Rep_3 family. A neighbor-joining tree of gene sequences coding for RIPs of the Rep_3 family was built using MEGA 6.06. A cut-off equal to or higher than 80% and a bootstrap analysis based on 1,000 permutations were applied to the analysis. Alignment of nucleotide sequences was performed using ClustalW2 (http://www.ebi.ac.uk/Tools/phylogeny/clustalw2_phylogeny/), and sequences showing an identity equal to or higher than 80% were clustered in groups that were highlighted by different background colors. Black dots indicate the RIP of the plasmid used for further comparison in Figs. 5 to 10 . Abbreviations: ND, not determined. doi:10.1128/microbiolspec.PLAS-0039-2014.f15

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FIGURE 16

Similarity of -like sequences encoding RIPs with the PriCT_1 domain. A neighbor-joining tree of gene sequences coding for RIPs with PriCT_1 domains was built using MEGA 6.06. A cut-off equal to or higher than 80% and a bootstrap analysis based on 1,000 permutations were applied to the analysis. Alignment of nucleotide sequences was performed using ClustalW2 (http://www.ebi.ac.uk/Tools/phylogeny/clustalw2_phylogeny/), and sequences showing an identity equal to or higher than 80% were clustered in groups that were highlighted by different background colors. Black dots indicate the RIP of the plasmid used for further comparison in Figs. 5 to 10 . Abbreviations: ND, not determined. doi:10.1128/microbiolspec.PLAS-0039-2014.f16

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FIGURE 17

Similarity of -like sequences encoding RIPs of the RepA_N family. A neighbor-joining tree of gene sequences coding for replication initiator proteins of the RepA_N family was built using MEGA 6.06. A cut-off equal to or higher than 80% and a bootstrap analysis based on 1,000 permutations were applied to the analysis. Alignment of nucleotide sequences was performed using ClustalW2 (http://www.ebi.ac.uk/Tools/phylogeny/clustalw2_phylogeny/), and sequences showing an identity equal to or higher than 80% were clustered in groups that were highlighted by different background colors. Black dots indicate the RIP of the plasmid used for further comparison in Figs. 5 to 10 . *Truncated gene. Similar to and . Abbreviations: ND, not determined. doi:10.1128/microbiolspec.PLAS-0039-2014.f17

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Tables

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TABLE 1

Fully characterized plasmids from low G+C bacteria available in GenBank database (updated September 2014)

Source: microbiolspec April 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.PLAS-0039-2014

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