This article isprotected rights by All copyright. reserved. 10.1111/mec.14007doi: lead todifferences version between this andthe ofPleasec Version Record. been and throughtypesetting, proofreadingwhich may thecopyediting, process, pagination This article undergone has for and buthas accepted been not review publication fullpeer 7 6 5 4 3 2 1 Affiliations: M. D. versatilemobile genetic elements resistancethrough multiplehorizontal gene transfersof complexand Adaptationofgenetically monomorphic bacteria: mssThis is for"Microbial Local Adaptation" special issue Article typeIssue :Special Accepted Date :08 Revised Date :28 Received :05 Date MR. DAMIEN RICHARD (Orcid ID 0000:
Cirad, U Inra, CBGP, UMR F ANSES, Cirad, UMR PVBMT,F INTA, Inra, UMR PVBMT,F Universitéla de Réunion, UMR PVBMT,F
Richard Accepted Article Terville Estación Experimental Agropecuaria Bella Vista, Plant HealthPlant Laboratory, MR BGPI,MR F 1 1 ,2,3 , B. ,† , I.
V.
Canteros
Ravigné - - 34090 Montpellier,France - - - 34398 Nov Jun Dec - 97410 St Pierre,Réunion, France - 97410 StPierre, Réunion, - 6 - 2016 -
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ite this articleite this as Lefeuvre S.
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, This article isprotected rights by All copyright. reserved. pathogens human cases, require full genes housekeeping that polymorphism of level a display bacteria The environments community, versatility Tn3 to gendivisionThe system. in identification found were resistance copper in involved Genes technology. copper resistant copLAB from strains and genotyping strains resistant of resistance pathogen citrus P Copper Abstract Shorttitle: Copper resistance in monomorphicbacteria +262Fax: 97410 Saint Pierre,Réunion, Address † Stenotrophomonas Keywords: Corresponding author Accepted adapted have athogens Article dynamics of genomeevolution of dynamics - - genetically -
ie transposon like resistant : ae antimicrobial based amplicons. Pôlede ProtectionPlantes, des UMR PVBMT, Station Ligne Paradis, 7 chemin de l'Irat, X. . 262
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strains from Réunion were assigned to two frequent haplotypes frequent two to assigned were Réunion from strains = resistantand susceptible strains also 2 85 i.e
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; P ; ale defined by these markers, strains from the three the from strains markers, these by defined ale
11 . Cu copLAB 2, strain assignation probabilities to clusters were often low often were clusters to probabilities assignation strain 2,
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same haplotype. Most haplotype. same < i 0.001). 0.001).
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In contrast, strains from Argentina (i.e. Argentina from strains contrast, In of from strains collected in Martinique and Réunion and Martinique in collected strains from
copL
the same origin. Similarly, haplotype #51, the #51, haplotype Similarly, origin. same the = ;
20), strains from Argentina, Martinique and Martinique Argentina, from strains 20), Cu nomto o hpoye aalbe at available haplotypes on information , copA and e R
A strains
,
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and Cu , -
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This article isprotected rights by All copyright. reserved. ( unclassified or SXT/R391thefamily,belongedtothe ICEs 582 al. SXT/R391andplasmids IncA/Csome with organization pLH201.1 16 These Tra search a conducted we three least at in organized plasmid the of regions different two The < value which A HigB putative a of domain suggesting trfA encoded reference. the from plasmid the Consequently, X. Davenport of strain the from data WGS Cop Featuresof plasmids associated with copper resistancein xanthomonads xanthomonads S in detected was plasmid No 7 plasmids. remaining into the circularized of 34 and circularized successfully were sequences chromosome per After Sequencing locus variant) mandarin historical(1978 CC main the join not did double of consistedsingletons, and CC smaller to corresponding haplotypes variation They related. tenotrophomonas
222
Acceptedeuvesicatoria Article
2014; Fricke 2014;
protein
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amino acid amino ih sre s n nioi protein antitoxin an as serve might
10
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- in 1989) was the closest historical strain to the main group of group main the to strain historical closest the was 1989) in
8 , (see (see M et al. et ) that
from each of thethree pLH201 .
ersnig 5 sris (69 strains 152 representing A .
were - G other
, skew switchskew S -
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et al. et the M90 al te pamd bearing plasmids other all LMG930, Stenotrophomonas three
2014; Pak 2014;
noaino ti pamd revealed plasmid this of annotation long putative tra putative long
sp s five as structured
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, Supportinginformation ,
( of the 13 fully sequenced strains sequenced fully 13 the of Table temporarystrains(≥
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commonly indicates the origin of replication( oforigin commonlyindicatesthe
2015)
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acid level, keeping only sequences only keeping level, acid CCs , Supporting information Supporting , X. . A . sltd rm irs phyllosphere citrus from isolated homolog (region d best ed . (Fig.
3 citri
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Using t Using a fud ontem and downstream found was conjugative operons. AUVE
3
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u to due 1: tee ee wr peet n h crmsm of chromosome the on present were genes these , ue
amino
69 citri .
comparison suggested that, with the exception of exception the with that, suggested comparison
for 2009). T 2009). d e eeld an revealed We he
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tan H0 was LH201 strain - (e toxin nopee apig B sampling. incomplete NCBI plasmid and the ICEberg ICE ICEberg the and plasmid NCBI details). Among these, a major CC (CC1) comprised 64comprised(CC1) CC major a these,Among two cop related ICE conjugative apparatusconjugative ICE related -
and cd dniy (AAI) identity acid
strains sequenced. Consistent with previous withConsistent sequenced. strains – h copper the
74
heC
RA n 5 CS 16o wih (68%) which of 176 CDS, 258 and tRNA ee wr gntcly related genetically were genes on
5; region 152; i.e - , we obtained we , value AAI e ). u I . - i iprat o oe that note to important is t
S
locus variants of CC of variants locus to
On the 52 plasmid hits ( hits plasmid 52 the On haplotypes D07
= superior to 60%.
four 3 wr anttd s IncA/C as annotated were 23) < the - 7 mn ai ln conserved long acid amino 87 eitn cmesl tan of strain commensal resistant
10 strain SPI - plasmids were detected in detected were plasmids arbitrarily 10 that matched that 2 antisens Cu )
: - (Crossman
fo 2 t 58 to 20 (from 182 (Schuessler 7 family 7 ( (sampledfromsatsuma R Tra proteinsTra from sharing no no sharing
oriV strains t cutr included clusters oth
783 ) e one (Grigoriev1998)
Twelve eetd s our as selected
o h toxin the to 1 0 –
one
. These strains These . (
205 i.e. otg were contigs to 18 contigs 18 to
t al. et
at least one least at al. et single , located atlocated, (Carraro
database sequence)
a double a 120 8) and 787) matched
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family l the all Fig. 2013)
- 2008; kb locus
(e 2 to et s, ) - - . , , .
This article isprotected rights by All copyright. reserved. 1998) Tn3 a on reported been also has transposons, TnpLH201.1 of repeat, bp 34 the of copy transposonsfamily respectively. Tn their with 90% helicaseDNA a andproteinrecombination tra plasmid bp 34 of repeats inverted two by ( region this plasmid the that suggestevidence of lines These variations. higher lower 59.2%, of content GC a had pLH201.1 tra adaptive transposons with associated genes plasmids, IncA/C In Copgenes arepart of a Tn3 new plasmidsICE IncA/CSXT/R391 and that of with shared clearly apparatus conjugative pLH201.1 of organization and content the Globally, 2.35 Alarcon elements genetic SXT the to homologous was types ICE R391 and SXT the of (e relaxases ICE of family PFL_4751 the of domain conserved MOB the to related al. 2010) MOB typ its with literature the the As and ( bacterialfamilies five p plasmids, lasmid incompatibility groups. incompatibility lasmid
Acceptedprotein cointegrate related nsposon Article 2009)
AAI
Vibrionaceae
system e H
.
-
and found in the incompatibility groups IncH, IncJ, IncT, IncP7 and IncA/C and IncP7 IncT, IncJ, IncH, groups incompatibility the in found and 19 re protein local
- ) from) IncWconjugative plasmids of the pLH201.1 relaxase (TraI relaxase pLH201.1 the of encoded t al. et laxases are scarce are laxases O al nw MOB known all Of .
(Garcillan while ical amino ical
hereafter that has
C otn (33) n h ~ 108 ~ the in (63.3%) content GC Hre & al 2014) Hall & (Harmer tnpT
2011) sequences of conjugative relaxases are useful for plasmid classification, we assessed we classification, plasmid for useful are relaxases conjugative of sequences
n oe netd oy t h ohr xrmt. hs atr, yia o composite of typical pattern, This extremity. other the at copy inverted one and the ) with) contrasted ecological nichesand geographical origins. , Xo19 (Beaber Xanthomonas tnpS (Tsuda & Iino 1988; Yano1988;Iino (Tsuda& - Barcia TraD . H121 not yet eane were remainder
referred to as TnpLH201.1, located at 108 at located TnpLH201.1, as to referred acid signature acid Pseudomonadaceae,Enterobacteriaceae,Aeromonadaceae,B
homologs, on 94 on homologs,
and sub
which formed which et al. et
pLH201
t al. et and have and
- been TraD domain (e domain TraD - tnpA ld o MOB of clade H
(Daccord .1
lds n sblds te TraI the subclades, and clades - All the All 2002) . It .
liketransposon Tn
also also 2009) described. were all were
Xo19
and display a higher GC content content GC higher a display and contained genes that are syntenic and similar to genes from the from genes to similar and syntenicare thatgenes contained
(
(HQ) only
ped n rus , , , , , utrpio and multireplicon F, J, T, P, H, groups in spread share pLH201.1 and various groups of plasmids including IncA/C including plasmids of groups various and plasmids TraI . tnpT
%
a Tn a , et al. et two direct copies direct two (Gomis , 70 , , that all display nucleotideidentity display all that , -
x2 been shown to be to shown H12 , a cointegrate protein cointegrate a , d
- ) et al. et pLH201.1 value = 0) found in conjugative in found 0) = value -
% -
PASE than to that to . However.
good like transposon from transposon like 2010) 3 - , 26 , (Alvarado
-
5 kb 152 - ie transposon like conferred multi conferred reported in large in reported Ruth
2013)
- % h 6.% of 64.8% the x solely . Similarly, the conjugative coupling factor TraD factor coupling conjugative the Similarly, . AAI - , 100 , HHH of each of the six MOB groups defined in the in defined groups MOB six the of each of
et al.et
region . Inside TnpLH201.1, we found an foundTnpLH201.1, weInside . , involved with
the % - t ae fe fud s at f complex of part as found often are its t al. et ace te MOB the matched x3 separated by 43 by separated
shows 2002) and 100% of TnPLH201.1’s gene length, gene TnPLH201.1’s of 100% and -
-
value = 2.20 = value low GG the GC . pLH201.1
- 034 2012) - drug resistance drug (Niu h hoooe bt ipae a displayed but chromosome, the
AAI x3 . in the transposition of some Tn3 some of transposition the in
rB opig atr (e factor coupling TrwB a mosaic structure. On pLH201.1,On structure. mosaic a - plasmids (> 60 kb) 60 (> plasmids tnpS kw rfls rsne several presented profiles skew Pseudomonas putida Pseudomonas - H
–
level appeared (Zhang -
TraI . t al. et x 151 , a transposase a , - L and (LV) and L
e s
- 931 bp) was surrounded was bp) 931 897 indicate that itthat indicate 21
pLH201.1 -
transposon 2 ), required for transfer for required ), H (NI) t al. et
015) ye (e type
bp
o be to (Garcillan and
between 70between - Ti icue a includes This . lo ipae a displayed also
at one extremity one at x urkholderiaceae 2014) -
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(Smillie - ot closely most au < value tnpA (Fernandez - - like mobile like (AVLI) similarities (Lauf
. additional - unknown - may Barcia Globally au of value , a DNA a ,
%
et al. et
et al. et - 10
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et - 4 - - ) ,
This article isprotected rights by All copyright. reserved. theof Ile of use the in bias revealedusagea Codon LH201. is which anticodon), (UAU tRNA Ile an comprised bp LM Cu other on 907 perfect almost two by surrounded was cluster pv. pumps efflux copper/silver known of that (HME division g TnpLH201.1, In Stoyanov metals heavy including stimuli, the to close and in as pLM199, in found system were that (Table designed Fig. (see length) gene’s amino 63% whereas ambiguous: quite is nomenclature X. a showed respectively its at repeats length gene’s each of 80% than more on 90% above disp however Tn (Fig. region transposon copper distinct ba plasmid a displayed sequence genome to specific pairs primer using amplicons PCR produce information Supporting study) 10 the sequenced six) of (out five the between in present Argentinian in resistance copper encompassed S3 rearrangements showing sometimes however content, gene syntenic and conserved TnpLH201.1. The G
ene content Spotn information Supporting , arboricola L19 eeld the revealed pLM199
Accepted0 Article citri 91) P. L211 otie to lses f ev mtl eitne ee ta wr icue in included were that genes resistance metal heavy of clusters two contained pLH201.1 NI
-
acid sequences only display low display only sequences acid syringae 328 n kon o e functionally be to known and , one , (both on 74% of the gene length) with their with length) gene the of 74% on (both for -
encoding codons) and plasmid et al. copLAB
. maltophilia S. bp region bp all
copABCD R X. pv. layed a transposa layed pr fo L19 al h str the all LM199, from Apart -
- ern DA oeue (lsis o al strains all for (plasmids molecules DNA bearing the RND) (> RND)
several extremities.
2001) . gardneri
ofthe Tn3 S juglandis However, 3 ns oooos to homologous enes
other strainsother and Spotn information) Supporting , negative by PCR all produced amplicons of the expected size for for size expected the of amplicons produced all PCR by negative . , which was which ,
cluster. This regulator family has family regulator This cluster.
95% genes, NI ).
and one and
4 Spotn information). Supporting S4, rsne f h atrae copper alternate the of presence
Interestingly,
(Crossman of 97, 98, 98 and 98% with those of of those with 98% and 98 98, 97, of Xaj417 isolated from walnut from isolated Xaj417
tasrpinl euao ta blns o h Mr fml ws found was family MerR the to belongs that regulator transcriptional a h ncetd sqecs of sequences nucleotide The AAI - ) . like transposons
ition apparatus ( apparatusition including h frt lse ws eietd y w 34 two by delineated was cluster first The . ) of of )
It X.
S X.
described in described
also controls the expression of of expression the controls also tenotrophomonas arboricola S. maltophilia S.
none citri
t al. et
the
novd n Cu in involved -
c AAI reported previously the bornegenes (6.5%)(data not shown). 2 pv.
X. usAB inInterestingly,LH3. TnpLH201.1,ontwocopies the of 907 ) . On all strains from Réunion and Martinique (five Martinique and Réunion from strains all On .
ckbone hratr ald TnpLM199 called hereafter ,
Cu citri
copA 2008) citri is display ains . their with levels
pv. R tnpA /smmD h seven The
X. X.
pv.
populations
juglandis the ATA codon the ATA were identified. These sequences corresponded to correspondedsequences These identified. were and citri citri The . extremely ,
bp citri tnpT ) and comprised almost identical 34 bp invertedbp 34 identical almost comprised and )
sp a ev mtl flx resistance efflux metal heavy a ,
copLAB copL copB pv. absent on the chromosome of chromosome the on absent - pv. R long direct repeats. direct long C pies agtn te or ee were genes four the targeting primers PCR . (Pereira
) and in one Argentinian strain (LM180), this (LM180), strainArgentinian one in and ) been reported to respond to environmental to respond to reported been copLABMGCDF strains that possessed this system and with and system this possessed that strains ed (Behlau and
Cu citri citri copA , ,
- from copA did not encode for CopRS for encode not did TpH0. hmlg ih globally a with homolog TnpLH201.1 a R eitne system resistance
similar to that of pLH201.1 but with a with but pLH201.1 of that to similar TnpS
(Behlau homologs, CopC homologs,
X. copLAB strain from Argentina LM199 failed to failed LM199 Argentina from strain strain A44 strain ,
et al. et
the
citri
between chromosomalgenes(1.4%between copB copABCD and pr from apart t al. et copLABMGCDF copA ) similar to that of TnpLH201.1 of thatto similar )
known chromosomal system of system chromosomal known
pv.
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copC ein a i was region in Ide, h antto of annotation the Indeed, .
2011) citri (i.e
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We .
2011)
Copper . coli and p iet eet and repeats direct bp strain
S
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( copABCD only only i. S3 Fig.
(Brown
copD
copLAB ee ivle in involved genes and s
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(Fig. 2 (Fig. X. , copABCD
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n Fg S4 Fig. and -
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system. Its system.
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citri citri The Fig. ( sp NI - . ,
This article isprotected rights by All copyright. reserved. three in located betaproteobacterium vietnamensis Burkholderia LMG930 homolog X. X. homolog found species: solaneous LL74 and pLH201.1 that of blocks the between divergence nucleotide other Homolog TnpLH201.1is found invarious genomic environments strain ( single a for except plasmids, sequenced the in conserved were resistance metal heavy in involved 2015) rearrangements, and deletions insertions, of on data previous hotspot with consistent a be to appeared TnpLH201.1 Therefore, the PilT. the proteinof deletion motility twitching the and resolvase addition a transposase, a encoded which pXAC33, ends. both a6 displayed va Slight exoribonuclease binding metal a and copper) to ( affinity higher a with copper to and promoter prote efflux metal heavy ( protein chelator metal 66 by surrounded was clusters two the between region The hmrR antimonite the of downstream located 67%) to (30 moderately arse ( reductase arsenate an resistance, arsenic czcD al genes contained cluster second The which
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Acceptedperforans Article
czcABCD nite/antimonitetransporter(
TnpLH201.1 in involved putatively genes three and system), efflux cobalt/zinc/cadmium a encode (which .
from the MerR family
that eune strains sequenced X. mighthelp degrade the transcriptional repressor in thepresence of copper). w dfeet Tn3 different Two pM90 ipae a isre gn (99% gene inserted an displayed pLMG930 , , ue ue
itos ee bevd ewe te TnpLH201.1 the between observed were riations ue - euvesicatoria . These conserved plasmids conserved These . USA). The conjugative apparatus of of apparatusconjugative The USA). 4
highly homologoushighly transposoncopiesthewereintegratedalso of inpLH201.1 rearranged s s (Wang ( e on an found We
' ht a itgae i a in integrated was that from clusters
of the transposon the of
rsn i sris f other of strains in present 945 LH3 ( LH3 M91 Nw Zealand) (New LMG911 ars
separate bp insertionbpposition at 154
was the et al. et
synonym cluster and several gene re gene several and cluster X.
(Fig.
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2004) also
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, Supporting information) regions X. 4 a eooial vraie ie root rice versatile ecologically an G4, ecie i Tn in described copper encodedalsoa This cluster .
arsR
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ht were that , Tn3
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This article isprotected rights by All copyright. reserved. Cu including with associated plasmids of analysis genomic comparative plasmids of understanding X. c of Determinants copper pathogens, to response In Discussion homolog sufficient was them multiple (accession of iontransport or ( perfect c are they that clusters entire ( clustersfoundwith was patternsecond The pLH201.1. pattern first The emerged. homology length) gene of 70% After of the of 30% further apart in the taxonomy than plasmid backbone Pelomonas Pseudoxanthomonas, from detected cons homolog sharing gene of Networks WGS. and NR databases NCBI public the in As Networksof gene sharing citrus ( the of chromosome the in integrated 93 sharing Réunion opLABMGCDF
citri which a Accepted Articlecluesthe set ih aa produced data with istent X. clustering
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citri shared only that we that
NI . strain from Réunion from strain ' by , contig accession JZUY01000051, that can be circularized with a 21bp a with circularized be can that JZUY01000051, accession contig , ' However, t However,
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NI and
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ig matching the whole backbone region of pLH201.1 of region backbone whole the matching only determinants This
R . circularize.
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. Globally, ). 7 6 homolog
repeatedly
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792 whose backbone regionbackbonewhose share Spotn information Supporting , data ofre ta hgl smlr TnpLH201.1 similar highly that confirmed
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compounds . d (
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one or two genes with pLH201.1, with genes two or one
ue Finally, the third pattern third the Finally, respectively. and the evolution of the associated the of evolution the and Xanthomonas R Cu searchedp for s
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This article isprotected rights by All copyright. reserved. Accepted Th Bui evolution of mechanisms the into insights Developing (2012) SD Bentley C, Chewapreecha J, Bryant Brun J(1971)Le chancre bactérien Citrus. des regulators. transcriptional of family MerR The (2003) JL Hobman SP, Kidd JV, Stoyanov NL, Brown transport and genetics Molecular (1995) DA Rouch BT, Lee J, Camakaris SR, Barrett NL, Brown J Jones JC, Hong F, Behlau BI, Canteros F, Behlau different from genes resistance Copper (2012) JH Graham JB, Jones BI, Canteros F, Behlau func and Genomic (2002) MK Waldor B, Hochhut JW, Beaber Garcillan A, Alvarado bacterial monomorphic Article genetically of comparisons genomic from Insights (2012) M Achtman (2008)AchtmanMEvolution, population structure,and phylogeography ge of References support Agro Départemental dela F Development for Roumagnac discussions P. and Doublet B. Barrès, B. thank to like would We Acknowledgements – No L Vrir C Vtl K Vital C, Verniere L, Ngoc i
. citrus cankerbacterium, bacterialof pathogens from whole FEMS Microbiol Rev Mol Microbiol analy from differentsources incitrus subsp from Genes Resistance Copper citri to resistance confer bacteria epiphytic citrus and xanthomonads from derived element Bacteriology transfer gene resistance antibiotic OnePlos gamma classify to method pathogens. bacterial pathogens.
otele, E Montpellier, ,
. as well as all those who provided help during field during help provided who those all as well as European Journal of PlantPathology sis of the copper the of sis citrumelonis und
7 , e40438.
Philos TransR Soc LondBiol B Sci (ERDF) and European Agricultural Fund for Rural Development (EAFRD), Development Rural for Fund Agricultural European and (ERDF)
184 Réunion, -
17 aca P d l Cu F 21) dgnrt pie MB yig (DPMT) typing MOB primer degenerate A (2012) F Cruz la de MP, Barcia
- isvg G, oe J, rhm H 21) oeua Caatrzto of Characterization Molecular (2011) JH Graham JB, Jones GV, Minsavage PC poet ubr 1504 number project SPACE , 4259 , 1153 . B, Graham JH (2013) Evidence for acquisition of copper resistance genes resistance copper of acquisition for Evidence (2013) JH Graham B,
Applied and Environmental Microbiology 27 Annu. Rev. Microbiol.
Région - , 145 - - resistance determinant (pco) from (pco) determinant resistance 4269. 1166. Xanthomonascitri - e al. et , - proteobacterial plasmids in clinical and environmental settings. environmental and clinical in plasmids proteobacterial 163.
Réunion - associated xanthomonads.
atooa citri Xanthomonas
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This article isprotected rights by All copyright. reserved. and pBS228 plasmid of Sequence (2007) CM Thomas IA, Kosheleva SM, Batt K, Accepted Jones AS, Haines R. in visualizationgenome and genecomparativegenoPlotR: (2010) SG Andersson JR, Kultima L, Guy diagrams. skew cumulative with genomes Analyzing (1998) A Grigoriev (2 DS Achor J, Cubero TR, Gottwald JH, Graham F hierarchical test and compute to R for package a Hierfstat, (2005) J Goudet Bergamin L, Amorim RB, Bassanezi TR, Gottwald A Escalon P, Lefeuvre JL, Gordon Gomis S Gironde S, Bonneau D, Giovanardi Garcillan ArticleGarcia Galimand M, Guiyoule A,Gerbaud G JL Gordon S, Bolot L, Gagnevin PF McDermott TJ, Welch WF, Fricke PT Monteiro C, Vaz AP, Francisco Olivei de RM, Ferreira Fernandez - - uh X Mnain , e a rz , ol (02 Cnuaie lsi poen rB an TrwB, protein plasmid Conjugative (2002) M Coll F, Cruz la de G, Moncalian FX, Ruth Vallve S, Romeu A, Palau J (2000) Horizontal gene transfer in bacterial and archaeal completearchaeal andbacterial in transfergene Horizontal (2000) J Palau A, Romeu S, Vallve reconstruction ofIncCP the Bioinformatics 2286 affecting successful eradication citrusof canker. Ecology Notes asian leafminer. canker ranges. citri and mapping of the active cleft.site membrane integral Italy. arboricola Xanthomonas application inplasmid classification. genomes. a transferable plasmid. pv. resistanceplasmid family. visualization for sequence based typing methods. of determinants pathogenicity other xanthomonads. of spread the in role major a play animal sources. pathogenic and commensal from plasmids IncA/C encoding - Barcia MP, Francia MV, de la Cruz F (2009) The diversity of conjugative relaxases and its and relaxases conjugative of diversity The (2009) F Cruz la de MV, Francia MP, Barcia - Alarcon C, Singer RS, Johnson TJ (2011) Comparative genomics of multidrug resistance multidrug of genomics Comparative (2011) TJ Johnson RS, Singer C, Alarcon allii pv. - European Journal of PlantPathology 2290. - infected plantings in sao paulo, Brazil, and au and Brazil, paulo, sao in plantings infected Strain CFBP 6369. Bmc Genomics citri Genome Res
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This article isprotected rights by All copyright. reserved. AcceptedMolecular (1994) MN Schroth NJ, Panopoulos M, Hendson YA, Lee K Boyer YN, Traore A, Leduc of plasmids the on resident elements transposable The (1998) H Herrmann C, Muller U, Lauf I Birol J, Schein M, Krzywinski StandleyK,(2013)Katoh DM MAFFT multiple sequence alignment softwareimprovementsversion 7: (2005) R Samson A, Darrasse K, Josi MA, Jacques Post (2006) G Carlton TD, Riley JH, Graham TR, Gottwald M, Irey PF Locascio GL, Chen D, Hyatt Article W Fan L, Lindler W, Hurtle resistance. ion metal antimicrobial Bacterial (2015) LC Crossman JL, Hobman plasmids conjugative Bacterial (1989) GF Sprague JA, Heinemann Zhan LY, He Plasmid (2012) MA Brockhurst E, Harrison p (2014) RM Hall CJ, Harmer JW,Cheaib(2010)LopezBaptesteNetworkS, Leigh P, E Halary B, analysesstructure genetic diversity Bacteriology from genes resistance copper juglandis of analysis sequence and Faso. bacterium: Mol Pseudomonasputida genomics. in performance and usability. field of phyllosphere Appl. Environ. the in sizes population biofilm stable in aggregated is 0822 events. weather catastrophic disease to estimate due to model spread predictive a of development the towards progress and spread initiation site identification. 3273 pestis Yersinia 471 bacteria and yeast. 44 copper of soils rhizosphere in communities bacterial of process. genes. 127 worlds. genetic independent in , 49 - -
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homology with small blue copper proteins and multicopper oxidase. multicopper and proteins copper blue small with homology RS. Xanthomonas citri citri Xanthomonas
176 Microbiol.
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This article isprotected rights by All copyright. reserved. AcceptedAM Molina R, Iglesia la De N, Trefault IncP bp 68,869the Sequenceof (2005)A Schluter A, PuhlerI, Krahn SzczepanowskiR, T, Tennstedt F Marchesi P, Imboden A, Telenti to plasmids bacterial phytopathogenic of contribution the into insights Genomic (2007) GW Sundin Hobma JV, Stoyanov assembler. genome lightweight fast, a Minimus: (2007) M Pop SL, Salzberg AL, Delcher DD, Sommer (1985) IM Smith Garcillan C, Smillie for centre reference the ISfinder: (2006) M Chandler J, Mahillon L, Lestrade J, Perochon P, Siguier D HarrisonBi EM, Y, Shao Article Barloy EW, Sevin IncP of history evolutionary the Inferring (2013) J Sullivan EM, Top CJ, Brown DY, Sen metal Heavy (2012) TU Berendonk C, Seiler Fivian T, Cortes DL, Schuessler MD, Routh of pathovars of spread and Multiplication (1986) JA Callow JN, Robinson hoormtc oltns n eouin f pcaie clraoai degradation chloroaromatic specialized of evolution pathways. and pollutants chloroaromatic from pJP4 waste a ba from pTB11 plasmid alpha Mycobacterium tuberculosis the evolutionary history of their hosts. controlling expression of thecopper exporter CopA. Bmc Bioinformatics Mixture Centenary Meeting Bordeaux, : France, 5th Microbiology and Molecular Biology Reviews bacterial insertion sequences. bacteria and archaea. inloci prokaryotes. 166. incongruenceam despite water bodies impacted by agricultureand aquaculture. mRNAs and cleavage tmRNA.of tuberculosis Mycobacterium gram in regulation and Enzymol RelatAreas Mol Biol function, structure, their of perspective and host non 1009 pathotypeA causing Asiatic ckbone,Tn402 a Zalucki Y, Su CC Su Y, Zalucki
- 1016 Fungicides for crop protection : 100 years of progress : progress of years 100 : protection crop for Fungicides - Hubler F (2007) RASTA (2007) F Hubler - Environmental Microbiology - 1387 aca P Faca V Rca P, e a rz (00 Mblt o plasmids. of Mobility (2010) F Cruz la de EPC, Rocha MV, Francia MP, Barcia n JL, Brown NL (2001) CueR (YbbI) of (YbbI) CueR (2001) NL Brown JL, n asoi eutropha Ralstonia - host plants. - PDN. , et al. et , - , et al. et ,
like integron and other transposable elements. Genome Biol 8 , 64. Nucleic AcidsResearch
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results in growth inhibition, reduced abundance of a subset of subset a of abundance reduced inhibition, growth in results Lancet 77 Nucleic A , et al. et , , 109 Mol Microbiol 8 - , R155. , et al. et , Bacteria: a web a Bacteria: M14 pP) eel mcaim o adaptat of mechanisms reveals (pJP4) JMP134
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1 - - This article isprotected rights by All copyright. reserved. Accepted Sequencesproduced in this study ( database genotyping MLVA The AccessibilityData WJ, Zhang Y Ohtsubo H, Genka H, Yano genetic mobile mosaic elements: conjugative and Integrative (2010) MK Waldor RA, Wozniak M Panijel I, Barash DM, Weinthal DasS C, Rensing S, Fasiludeen SP, Kennedy Article G, Wang mobile bacteria: phytopathogenic in plasmids of roles The (2001) RW Jackson J, Murillo A, Vivian Metageno (2009) M Ferrer PN, Golyshin A, Beloqui ME, Guazzaroni JM, Vieites A Alvarez P, Yang L, Vauterin phytosphere. the in transfer gene Horizontal (2003) MJ Bailey S, Turner JD, Elsas Van Z Rouy L, Labarre D, Vallenet the covering transposon a Tn4653, of characterization and Identification (1988) T Iino M, Tsuda T Campillo V, Verdier LR, Triplett Chemother coli Escherichia resolution full for required segment the and activity. site crossover of determination Tn4651: elements enabling dynamic lateral genef Appl Environ Microbiol gall the of populations diverse in pPATH plasmid Journal ofBacteriology Halobacterium arsenals? systems microbiology. associated with plants. 157 by syntenyresults. toluene transposon Tn4651 on TOL plasmid pWW0. Van Leeuwenhoek rice from isolated - 31 , 525 u R Shaz S Schwarz XR, Xu n MLVA and Plasmid - 537. Microbiology
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This article isprotected rights by All copyright. reserved. Accepted Article manuscript. and OP CV, AC, conducted PL and DR analyses. helped AR and biology IR BF, analyses. population data genomic conducted VR and CV OP, experiments. the produced BIC study. the designed and conceived OP and CV VR, PL, AuthorContributions phenotypic data phenotypic
L rt te aucit All manuscript. the wrote PL
on Argentinian strainsArgentinian on
to
. DR, CB, KB, PG, SJ, MT, BIC, CV and OP carried out carried OP and CV BIC, MT, SJ, PG, KB, CB, DR, . design and design
the
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ed n apoe te final the approved and read essential bacterial strains bacterial essential study. DR, VR, AR, BF, IR, BF, AR, VR, DR, study.
and This article isprotected rights by All copyright. reserved. JS749 LH201 LH276 LH3 LJ207 LL074 LM159 LM180 LM199 LM091 LMG911 LMG930
Accepted ArticleStrain
- - -
7 3 4
Bv A44† Xcc Xcc 15 - Other numbersOther 5 03 -
4a (INTA)4a - - 1638 (INTA); 4632 (INTA)
CP018850 CP018849 CP018847 CP018471 CP018468 MSQW00000000 MSQV00000000 CP017483 CP018727 CP018725 CP018467 CP018463 CP018728 CP018860 CP018858 CP018857 CP018854 CP018476 CP018472 CP018853 Accession
------
Xanthomonas Xanthomonas Xanthomonas Xanthomonas Xanthomonas Xanthomonas Xanthomonas Xanthomonas Xanthomonas Stenotrophomonas Xanthomonas Xanthomonas Genus
gardneri citri citri 'perforans'‡ citri citri vesicatoria citri citri sp. vesicatoria euvesicatoria
Species
citri citri citri citri citri citri Pathovar
plasmid plasmid plasmid plasmid plasmid plasmid plasmid plasmid plasmid chromosome plasmid plasmid resistance location Copper
Réunion Réunion Réunion Maurice Réunion Martinique Argentina Argentina Argentina Réunion Zealand New USA Country
Date 1997 2010 2010 2010 2012 2014 1987 2003 2015 2015 1955 1969
Tomato Kaffir lime Kaffir lime Tomato Kaffir lime Grapefruit Pepper Pomelo Orange Tangor Tomato Pepper Host
This article isprotected rights by All copyright. reserved. Table Tables ‡ As designated† by Behlau al.(2011).et Microorganisms, University Ghent, of Belgium), INTA (Instituto Nacional ICMP (International Collection of Microorganisms from Plants, Landcare Research, Auckland, New Zealand), BCCM/LMG (Belgian Co ICMP7383
AcceptedX. 'perforans' Article
1 Characteristics of
was reclassifiedwas as copper - resistant bacterial strains usedfor long X. euvesicatoria CP018734 CP018731 CP018730
-
Xanthomonas
de. Tecnología Agropecuaria) - read sequencing gardneri
plasmid
Zealand New ordinated Collections of
1980
Tomato
This article isprotected rights by All copyright. reserved. copper copper = red Argentina; copper Argentina;= susceptibledarkgreen ( haplotype. complex per clonal single a as organized singlebyhaplotypeslinked were strains These data. minisatellite Réu Fig. the with shared genes in coloured of number the to proportional Node is (A) nodes pLH201.1. the of diameter and higher is share identity Fig. skew using4 a 2 a in content GC of % pLH201.1’s and LH201 ( represent Fig. varies according to genetic distancebetween homologous blocksdefined by a the to according prediction. gene Prodigal (Mage uncurated prediction gene curated represent sequenced Fig. of complex epidemic copper clonal main the to closest genetically strain historical the as identified was which D07, localizes arrow black The respectively. variation, total the of 14.8% and 27.5% represented 2 included assupplementary Réunion copper among (MDS) scaling multidimensional respectively system, respectively. variation, total axes showing plot MDS The Réunion. and Martinique copper among (MDS) scaling multidimensional by represented in differing Fig. Figure Accepted* by followed are genes putative Article y arey
nion 3 2 1 S1 4
lgmns ewe pH0. ad eune cryn pLH201.1 carrying sequences and pLH201.1 between Alignments
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resistant Réunion. aeoia mnmm pnig re f AC sris rm retn, atnqe and Martinique Argentina, from strains DAPC1 of tree spanning minimum Categorical >
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niae te tan rgn n cpe peoye lgt re = copper = green light phenotype: copper and origin strain the indicates - resistant M resistant Te oprsn oe hw hmlgu ncetd sequences. nucleotide homologous shows zone comparison The .
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This article isprotected rights by All copyright. reserved. euvesicatoria axonopodisXanthomonas nitritireducens Stenotrophomonas Sac: G parenta the of species the indicate line each of left the at names The of level their to according homolog represent sequences Fig. divergence the between the chromosomes,upper the triangle representsdivergenc represents triangle lower the Whereas regions. homologous all of comparison the Divergencevalues Fig. the tree computation was obtained after the concatenation alignmentsof of each gene. representa graphical and copper known for coding sequences Fig. defineda by sequences. nucleotide the to according groups several into categorized genomes On otherwise. s Fig. double single no complexes ( clonal five as organized were strains These data. microsatellite on based Réunion from Fig. i.e trains sequenced AcceptedenB Article .
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resistance systems extracted from public database public from extracted systems resistance maltophilia identity with pLH201.1 with identity represent ; ; Xor: r homologous are
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; Xci: ; . The comparison zone shows homologous shows zone comparison The . pLH201.1 sequence. Squares are Squares sequence. pLH201.1 sp tntohmns maltophilia Stenotrophomonas
o t least at to .; ,
as indicated on the scale on the right the on scale the on indicated as Xanthomonas citriXanthomonas
Xar: organisation Xanthomonas e betweene theplasmids. atooa arboricol Xanthomonas Each l Each ; Xpe: . Psp: Psp: . Tn 10 l sequence of the cluster, its cluster, the of sequence l pLH201.1
The ine L211 genes. pLH201.1 Xanthomonasperforans Pseudoxanthomonas .
The alignment used for used alignment The
represent L211 ee are genes pLH201.1 )
, ; Xeu: ; were obtainedfromwere cit i.e
hra o other on whereas homolog ri . ,
haplotypes with haplotypes
unless , pv.
respectively. Xanthomonas
a citri along with along cluster of cluster ue
specified colo Sni: ; Squares a
s strains Xax ; blocks
from u sp red
. .;
: .
This article isprotected rights by All copyright. reserved. Accepted Article
This article isprotected rights by All copyright. reserved. Accepted Article
This article isprotected rights by All copyright. reserved. Accepted Article
This article isprotected rights by All copyright. reserved. Accepted Article