We present here the complete genome sequence of Trueperella pyogenes UFV1. The 2.3-Mbp genome contains an extremely interesting AI-2 transporter and processing system related to the quorum-sensing signal response. This specific feature is described in this species for the first time and might be responsible for a new pathogenic behavior

Campanaro, Stefano

Corich, Viviana

de Paula, Sergio Oliveira

Dias, Roberto Sousa

Duarte, Vinicius da Silva

Giacomini, Alessio

Silva, Cynthia Canedo da

Treu, Laura

ABSTRACT
          
            We present here the complete genome sequence of
            Trueperella pyogenes
            UFV1. The 2.3-Mbp genome contains an extremely interesting AI-2 transporter and processing system related to the quorum-sensing signal response. This specific feature is described in this species for the first time and might be responsible for a new pathogenic behavior.
          </jats:p

Vinícius da Silva Duarte

Laura Treu

Stefano Campanaro

Roberto Sousa Dias

Cynthia Canedo da Silva

Alessio Giacomini

Viviana Corich

Sérgio Oliveira de Paula

Crossref

Genome Announcements

The Complete Genome Sequence of Trueperella pyogenes UFV1 Reveals a Processing System Involved in the Quorum-Sensing Signal Response

Duarte, VinÃ­cius da Silva

Archivio istituzionale della ricerca - Università di Padova

Original Citation:The complete genome sequence of Trueperella pyogenes UFV1 reveals a processing system involvedin the quorumsensing signal responseAmerican Society for MicrobiologyPublisher:Published version:DOI:Terms of use:Open Access(Article begins on next page)This article is made available under terms and conditions applicable to Open Access Guidelines, as described athttp://www.unipd.it/download/file/fid/55401 (Italian only)Availability:This version is available at: 11577/3249024 since: 2017-12-02T12:40:56Z10.1128/genomeA.00639-17Università degli Studi di PadovaPadua Research Archive - Institutional RepositoryThe Complete Genome Sequence ofTrueperella pyogenes UFV1 Reveals aProcessing System Involved in theQuorum-Sensing Signal ResponseVinícius da Silva Duarte,a Laura Treu,b,e Stefano Campanaro,cRoberto Sousa Dias,d Cynthia Canedo da Silva,a Alessio Giacomini,bViviana Corich,b Sérgio Oliveira de PauladDepartment of Microbiology, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazila; Department ofAgronomy Food Natural Resources Animals and Environment, University of Padova, Legnaro, Italyb;Department of Biology, University of Padova, Padua, Italyc; Department of General Biology, UniversidadeFederal de Viçosa, Viçosa, Minas Gerais, Brazild; Department of Environmental Engineering, Technical Universityof Denmark, Lyngby, DenmarkeABSTRACT We present here the complete genome sequence of Trueperella pyo-genes UFV1. The 2.3-Mbp genome contains an extremely interesting AI-2 transporterand processing system related to the quorum-sensing signal response. This speciﬁcfeature is described in this species for the ﬁrst time and might be responsible for anew pathogenic behavior.Trueperella pyogenes, formerly Arcanobacterium pyogenes, is a worldwide opportu-nistic pathogen possessing a broad range of virulence factors which have beeninvolved in economic losses due to diseases, like mastitis and metritis, in dairy cows (1,2). The capability of this species to generate bioﬁlms by growing as a sessile bacterialcommunity is key in determining chronic infections. Bioﬁlm formation, in fact, allowsmicroorganisms to have better resistance in selective environments, which are deter-mined by exposure to antibiotics or the immune defense system (3, 4). In T. pyogenes,little is known about the gene expression of the principal virulence factor pyolisin (PLO)in vivo; however, its transcription is related to bioﬁlm formation and is positivelyregulated in the beginning of stationary phase by the response regulator ploR (3).Here, we present the complete genome sequence of T. pyogenes UFV1, a strainisolated from a dairy cow affected by metritis that was raised in a dairy farm (Viçosa,Minas Gerais, Brazil). This strain was used in these studies of bioﬁlm control and as aphage host.DNA extraction was performed using the protocol described by Pospiech andNeumann (5) and sent to MR DNA. Sequencing was performed with the Illumina MiSeqplatform using paired-end (PE) reads (2  300 bp) and Nextera library preparation. Thesequences were assembled de novo using the CLC Genomics Workbench software(version 9.5), and scaffolds were ordered and oriented using strain T. pyogenes TP6375as the reference with CONTIguator (6). The RAST server (7) and the NCBI ProkaryoticGenome Annotation Pipeline (PGAP) were used for gene ﬁnding and annotation.After quality ﬁltering and merging of the overlapping PE reads, a total of 2,626,752sequences, with an average length of 314 bp, were obtained, providing nearly 360-foldgenome coverage. The assembly resulted in 23 scaffolds, with a total length of2,333,212 bp and average GC content of 59.5%. Alignment of the scaffolds with thereference strain suggests they are arranged in a single circular chromosome. PGAPpredicted 2,199 genes classiﬁed into 2,142 coding sequences (CDSs), 2 clusteredregularly interspaced short palindromic repeat (CRISPR) arrays, 2 rRNAs, 51 tRNAs, 4Received 23 May 2017 Accepted 25 May2017 Published 20 July 2017Citation Duarte VDS, Treu L, Campanaro S,Dias RS, Silva CCD, Giacomini A, Corich V, dePaula SO. 2017. The complete genomesequence of Trueperella pyogenes UFV1 revealsa processing system involved in the quorum-sensing signal response. Genome Announc5:e00639-17. https://doi.org/10.1128/genomeA.00639-17.Copyright © 2017 Duarte et al. This is an open-access article distributed under the terms ofthe Creative Commons Attribution 4.0International license.Address correspondence to Sérgio Oliveira dePaula, depaula@ufv.br.PROKARYOTEScrossmVolume 5 Issue 29 e00639-17 genomea.asm.org 1noncoding RNAs (ncRNAs), and 40 pseudogenes. Additionally, 47% of the CDSs wereassigned to 308 subsystems using the RAST server.The genome analysis revealed a new feature of T. pyogenes, the lsrACDBFGE operon,which is related to the quorum-sensing signal response AI-2, described here for the ﬁrsttime for this species. This system is known to mediate interspecies communication (8),and we hypothesize it is involved in the newly described pathogenic ability of T. pyo-genes, since bioﬁlm formation and virulence factors are regulated by this mechanism.Additionally, a broad range of virulence factors were found speciﬁcally related to genesthat confer resistance to antibiotics (vancomycin, streptothricin, ﬂuoroquinolones,beta-lactams, and aminoglycosides) and cell wall attachment (nanH, nanP, cbpA, ﬁm,and plo).In this work, we present the complete genome sequence of T. pyogenes UFV1, whichwill serve as a phage host and a new model in order to understand the role of quorumsensing in this species.Accession number(s). This whole-genome shotgun project has been deposited atDDBJ/ENA/GenBank under the accession number MVGS00000000. The version de-scribed in this paper is version MVGS01000000.ACKNOWLEDGMENTSWe are grateful for the ﬁnancial support from the following Brazilian agencies: Fundaçãode Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), Coordenacão de Aperfeiçoa-mento de Pessoal de Nível Superior (CAPES), Conselho Nacional de DesenvolvimentoCientíﬁco e Tecnológico (CNPq), and Financiadora de Estudos e Projetos (Finep). We arealso grateful to the Programa de Desenvolvimento da Pecuária Leiteira (PDPL), Viçosa,Minas Gerais, Brazil, that kindly provided us with uterine lochial secretions.REFERENCES1. Bicalho MLS, Lima FS, Machado VS, Meira EB, Jr, Ganda EK, Foditsch C,Bicalho RC, Gilbert RO. 2016. Associations among Trueperella pyogenes,endometritis diagnosis, and pregnancy outcomes in dairy cows. Theriog-enology 85:267–274. https://doi.org/10.1016/j.theriogenology.2015.09.043.2. Zhao K, Li W, Kang C, Du L, Huang T, Zhang X, Wu M, Yue Bl. 2014.Phylogenomics and evolutionary dynamics of the family Actinomycetaceae.Genome Biol Evol 6:2625–2633. https://doi.org/10.1093/gbe/evu211.3. Jost BH, Billington SJ. 2005. Arcanobacterium pyogenes: molecular patho-genesis of an animal opportunist. Antonie Van Leeuwenhoek 88:87–102.https://doi.org/10.1007/s10482-005-2316-5.4. Donlan RM. 2002. Bioﬁlms: microbial life on surfaces. Emerg Infect Dis J8:881–890. https://doi.org/10.3201/eid0809.020063.5. Pospiech A, Neumann B. 1995. A versatile quick-prep of genomic DNAfrom gram-positive bacteria. Trends Genet 11:217–218. https://doi.org/10.1016/S0168-9525(00)89052-6.6. Galardini M, Biondi EG, Bazzicalupo M, Mengoni A. 2011. CONTIGuator: abacterial genomes ﬁnishing tool for structural insights on draft genomes.Source Code Biol Med 6:11. https://doi.org/10.1186/1751-0473-6-11.7. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA,Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam AR, Xia F, Stevens R.2014. The SEED and the Rapid annotation of microbial genomes usingsubsystems technology (RAST). Nucleic Acids Res 42:D206–D214. https://doi.org/10.1093/nar/gkt1226.8. Majumdar S, Pal S. 2017. Cross-species communication in bacterial world. JCell Commun Signal 11:1–4. https://doi.org/10.1007/s12079-017-0383-9.Duarte et al.Volume 5 Issue 29 e00639-17 genomea.asm.org 2

English

The complete genome sequence of Trueperella pyogenes UFV1 reveals a processing system involved in the quorumsensing signal response

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Downloaded from orbit.dtu.dk on: Dec 20, 2017The complete genome sequence of Trueperella pyogenes UFV1 reveals a processingsystem involved in the quorumsensing signal responseDuarte, Vinicius da Silva; Treu, Laura; Campanaro, Stefano; Dias, Roberto Sousa; Silva, Cynthia Canedoda; Giacomini, Alessio; Corich, Viviana; de Paula, Sergio OliveiraPublished in:Genome AnnouncementsLink to article, DOI:10.1128/genomeA.00639-17Publication date:2017Document VersionPublisher's PDF, also known as Version of recordLink back to DTU OrbitCitation (APA):Duarte, V. D. S., Treu, L., Campanaro, S., Dias, R. S., Silva, C. C. D., Giacomini, A., ... de Paula, S. O. (2017).The complete genome sequence of Trueperella pyogenes UFV1 reveals a processing system involved in thequorumsensing signal response. Genome Announcements, 5(29), [e00639-17]. DOI: 10.1128/genomeA.00639-17The Complete Genome Sequence ofTrueperella pyogenes UFV1 Reveals aProcessing System Involved in theQuorum-Sensing Signal ResponseVinícius da Silva Duarte,a Laura Treu,b,e Stefano Campanaro,cRoberto Sousa Dias,d Cynthia Canedo da Silva,a Alessio Giacomini,bViviana Corich,b Sérgio Oliveira de PauladDepartment of Microbiology, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazila; Department ofAgronomy Food Natural Resources Animals and Environment, University of Padova, Legnaro, Italyb;Department of Biology, University of Padova, Padua, Italyc; Department of General Biology, UniversidadeFederal de Viçosa, Viçosa, Minas Gerais, Brazild; Department of Environmental Engineering, Technical Universityof Denmark, Lyngby, DenmarkeABSTRACT We present here the complete genome sequence of Trueperella pyo-genes UFV1. The 2.3-Mbp genome contains an extremely interesting AI-2 transporterand processing system related to the quorum-sensing signal response. This speciﬁcfeature is described in this species for the ﬁrst time and might be responsible for anew pathogenic behavior.Trueperella pyogenes, formerly Arcanobacterium pyogenes, is a worldwide opportu-nistic pathogen possessing a broad range of virulence factors which have beeninvolved in economic losses due to diseases, like mastitis and metritis, in dairy cows (1,2). The capability of this species to generate bioﬁlms by growing as a sessile bacterialcommunity is key in determining chronic infections. Bioﬁlm formation, in fact, allowsmicroorganisms to have better resistance in selective environments, which are deter-mined by exposure to antibiotics or the immune defense system (3, 4). In T. pyogenes,little is known about the gene expression of the principal virulence factor pyolisin (PLO)in vivo; however, its transcription is related to bioﬁlm formation and is positivelyregulated in the beginning of stationary phase by the response regulator ploR (3).Here, we present the complete genome sequence of T. pyogenes UFV1, a strainisolated from a dairy cow affected by metritis that was raised in a dairy farm (Viçosa,Minas Gerais, Brazil). This strain was used in these studies of bioﬁlm control and as aphage host.DNA extraction was performed using the protocol described by Pospiech andNeumann (5) and sent to MR DNA. Sequencing was performed with the Illumina MiSeqplatform using paired-end (PE) reads (2  300 bp) and Nextera library preparation. Thesequences were assembled de novo using the CLC Genomics Workbench software(version 9.5), and scaffolds were ordered and oriented using strain T. pyogenes TP6375as the reference with CONTIguator (6). The RAST server (7) and the NCBI ProkaryoticGenome Annotation Pipeline (PGAP) were used for gene ﬁnding and annotation.After quality ﬁltering and merging of the overlapping PE reads, a total of 2,626,752sequences, with an average length of 314 bp, were obtained, providing nearly 360-foldgenome coverage. The assembly resulted in 23 scaffolds, with a total length of2,333,212 bp and average GC content of 59.5%. Alignment of the scaffolds with thereference strain suggests they are arranged in a single circular chromosome. PGAPpredicted 2,199 genes classiﬁed into 2,142 coding sequences (CDSs), 2 clusteredregularly interspaced short palindromic repeat (CRISPR) arrays, 2 rRNAs, 51 tRNAs, 4Received 23 May 2017 Accepted 25 May2017 Published 20 July 2017Citation Duarte VDS, Treu L, Campanaro S,Dias RS, Silva CCD, Giacomini A, Corich V, dePaula SO. 2017. The complete genomesequence of Trueperella pyogenes UFV1 revealsa processing system involved in the quorum-sensing signal response. Genome Announc5:e00639-17. https://doi.org/10.1128/genomeA.00639-17.Copyright © 2017 Duarte et al. This is an open-access article distributed under the terms ofthe Creative Commons Attribution 4.0International license.Address correspondence to Sérgio Oliveira dePaula, depaula@ufv.br.PROKARYOTEScrossmVolume 5 Issue 29 e00639-17 genomea.asm.org 1 on October 16, 2017 by DTU Libraryhttp://genomea.asm.org/Downloaded from noncoding RNAs (ncRNAs), and 40 pseudogenes. Additionally, 47% of the CDSs wereassigned to 308 subsystems using the RAST server.The genome analysis revealed a new feature of T. pyogenes, the lsrACDBFGE operon,which is related to the quorum-sensing signal response AI-2, described here for the ﬁrsttime for this species. This system is known to mediate interspecies communication (8),and we hypothesize it is involved in the newly described pathogenic ability of T. pyo-genes, since bioﬁlm formation and virulence factors are regulated by this mechanism.Additionally, a broad range of virulence factors were found speciﬁcally related to genesthat confer resistance to antibiotics (vancomycin, streptothricin, ﬂuoroquinolones,beta-lactams, and aminoglycosides) and cell wall attachment (nanH, nanP, cbpA, ﬁm,and plo).In this work, we present the complete genome sequence of T. pyogenes UFV1, whichwill serve as a phage host and a new model in order to understand the role of quorumsensing in this species.Accession number(s). This whole-genome shotgun project has been deposited atDDBJ/ENA/GenBank under the accession number MVGS00000000. The version de-scribed in this paper is version MVGS01000000.ACKNOWLEDGMENTSWe are grateful for the ﬁnancial support from the following Brazilian agencies: Fundaçãode Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), Coordenacão de Aperfeiçoa-mento de Pessoal de Nível Superior (CAPES), Conselho Nacional de DesenvolvimentoCientíﬁco e Tecnológico (CNPq), and Financiadora de Estudos e Projetos (Finep). We arealso grateful to the Programa de Desenvolvimento da Pecuária Leiteira (PDPL), Viçosa,Minas Gerais, Brazil, that kindly provided us with uterine lochial secretions.REFERENCES1. Bicalho MLS, Lima FS, Machado VS, Meira EB, Jr, Ganda EK, Foditsch C,Bicalho RC, Gilbert RO. 2016. Associations among Trueperella pyogenes,endometritis diagnosis, and pregnancy outcomes in dairy cows. Theriog-enology 85:267–274. https://doi.org/10.1016/j.theriogenology.2015.09.043.2. Zhao K, Li W, Kang C, Du L, Huang T, Zhang X, Wu M, Yue Bl. 2014.Phylogenomics and evolutionary dynamics of the family Actinomycetaceae.Genome Biol Evol 6:2625–2633. https://doi.org/10.1093/gbe/evu211.3. Jost BH, Billington SJ. 2005. Arcanobacterium pyogenes: molecular patho-genesis of an animal opportunist. Antonie Van Leeuwenhoek 88:87–102.https://doi.org/10.1007/s10482-005-2316-5.4. Donlan RM. 2002. Bioﬁlms: microbial life on surfaces. Emerg Infect Dis J8:881–890. https://doi.org/10.3201/eid0809.020063.5. Pospiech A, Neumann B. 1995. A versatile quick-prep of genomic DNAfrom gram-positive bacteria. Trends Genet 11:217–218. https://doi.org/10.1016/S0168-9525(00)89052-6.6. Galardini M, Biondi EG, Bazzicalupo M, Mengoni A. 2011. CONTIGuator: abacterial genomes ﬁnishing tool for structural insights on draft genomes.Source Code Biol Med 6:11. https://doi.org/10.1186/1751-0473-6-11.7. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA,Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam AR, Xia F, Stevens R.2014. The SEED and the Rapid annotation of microbial genomes usingsubsystems technology (RAST). Nucleic Acids Res 42:D206–D214. https://doi.org/10.1093/nar/gkt1226.8. Majumdar S, Pal S. 2017. Cross-species communication in bacterial world. JCell Commun Signal 11:1–4. https://doi.org/10.1007/s12079-017-0383-9.Duarte et al.Volume 5 Issue 29 e00639-17 genomea.asm.org 2 on October 16, 2017 by DTU Libraryhttp://genomea.asm.org/Downloaded from 

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The complete genome sequence of Trueperella pyogenes UFV1 reveals a processing system involved in the quorumsensing signal response

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