Extrachromosomal circular elements targeted by CRISPR-Cas in Dehalococcoides mccartyi are linked to mobilization of reductive dehalogenase genes.
Journal
The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086
Informations de publication
Date de publication:
01 2019
01 2019
Historique:
received:
16
03
2018
accepted:
19
06
2018
revised:
13
06
2018
pubmed:
15
8
2018
medline:
1
8
2019
entrez:
15
8
2018
Statut:
ppublish
Résumé
Dehalococcoides mccartyi are obligate organohalide-respiring bacteria that play an important detoxifying role in the environment. They have small genomes (~1.4 Mb) with a core region interrupted by two high plasticity regions (HPRs) containing dozens of genes encoding reductive dehalogenases involved in organohalide respiration. The genomes of eight new strains of D. mccartyi were closed from metagenomic data from a related set of enrichment cultures, bringing the total number of genomes to 24. Two of the newly sequenced strains and three previously sequenced strains contain CRISPR-Cas systems. These D. mccartyi CRISPR-Cas systems were found to primarily target prophages and genomic islands. The genomic islands were identified either as integrated into D. mccartyi genomes or as circular extrachromosomal elements. We observed active circularization of the integrated genomic island containing vcrABC operon encoding the dehalogenase (VcrA) responsible for the transformation of vinyl chloride to non-toxic ethene. We interrogated archived DNA from established enrichment cultures and found that the CRISPR array acquired three new spacers in 11 years. These data provide a glimpse into dynamic processes operating on the genomes distinct to D. mccartyi strains found in enrichment cultures and provide the first insights into possible mechanisms of lateral DNA exchange in D. mccartyi.
Identifiants
pubmed: 30104577
doi: 10.1038/s41396-018-0254-2
pii: 10.1038/s41396-018-0254-2
pmc: PMC6299113
doi:
Substances chimiques
DNA, Bacterial
0
DNA, Circular
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Pagination
24-38Subventions
Organisme : CIHR
ID : MOP-136845
Pays : Canada
Références
Löffler FE, Yan J, Ritalahti KM, Adrian L, Edwards EA, Konstantinidis KT, et al. Dehalococcoides mccartyi gen. nov., sp. nov., obligately organohalide-respiring anaerobic bacteria relevant to halogen cycling and bioremediation, belong to a novel bacterial class, Dehalococcoidia classis nov., order Dehalococcoidales ord. nov. and family Dehalococcoidaceae fam. nov., within the phylum Chloroflexi. Int J Syst Evol Microbiol. 2013;63:625–35.
doi: 10.1099/ijs.0.034926-0
Langille MGI, Hsiao WWL, Brinkman FSL. Detecting genomic islands using bioinformatics approaches. Nat Rev Microbiol. 2010;8:373–82.
doi: 10.1038/nrmicro2350
Müller JA, Rosner BM, Von Abendroth G, Meshulam-Simon G, McCarty PL, Spormann AM. Molecular identification of the catabolic vinyl chloride reductase from Dehalococcodies sp. strain VS and its environmental distribution. Appl Environ Microbiol. 2004;70:4880–8.
doi: 10.1128/AEM.70.8.4880-4888.2004
Ritalahti KM, Hatt JK, Lugmayr V, Henn K, Petrovskis EA, Ogles DM, et al. Comparing on-site to off-site biomass collection for Dehalococcoides biomarker gene quantification to predict in situ chlorinated ethene detoxification potential. Environ Sci Technol. 2010;44:5127–33.
doi: 10.1021/es100408r
Lee PK, Johnson DR, Holmes VF, He J, Alvarez-Cohen L. Reductive dehalogenase gene expression as a biomarker for physiological activity of Dehalococcoides spp. Appl Environ Microbiol. 2006;72:6161–8.
doi: 10.1128/AEM.01070-06
McMurdie PJ, Behrens SF, Müller JA, Goke J, Ritalahti KM, Wagner R, et al. Localized plasticity in the streamlined genomes of vinyl chloride respiring Dehalococcoides. PLoS Genet. 2009;5:e1000714.
doi: 10.1371/journal.pgen.1000714
McMurdie PJ, Hug LA, Edwards EA, Holmes S, Spormann AA. Site-specific mobilization of vinyl-chloride respiration islands by a mechanism common in Dehalococcoides. BMC Genom. 2011;12:287–302.
doi: 10.1186/1471-2164-12-287
Makarova KS, Haft DH, Barrangou R, Brouns SJJ, Charpentier E, Horvath P, et al. Evolution and classification of the CRISPR–Cas systems. Nat Rev Microbiol. 2011;9:467–77.
doi: 10.1038/nrmicro2577
van der Oost J, Jore MM, Westra ER, Lundgren M, Brouns SJJ. CRISPR-based adaptive and heritable immunity in prokaryotes. Trends Biochem Sci. 2009;34:401–7.
doi: 10.1016/j.tibs.2009.05.002
Fineran PC, Gerritzen MJH, Suárez-Diez M, Künne T, Boekhorst J, van Hijum SAFT, et al. Degenerate target sites mediate rapid primed CRISPR adaptation. Proc Natl Acad Sci USA. 2014;111:E1629–38.
doi: 10.1073/pnas.1400071111
Hatoum-Aslan A, Maniv I, Marraffini LA. Mature clustered, regularly interspaced, short palindromic repeats RNA (crRNA) length is measured by a ruler mechanism anchored at the precursor processing site. Proc Natl Acad Sci USA. 2011;108:21218–22.
doi: 10.1073/pnas.1112832108
Fineran PC, Charpentier E. Memory of viral infections by CRISPR-Cas adaptive immune systems: acquisition of new information. Virology . 2012;434:202–9.
doi: 10.1016/j.virol.2012.10.003
Duhamel M, Wehr SD, Yu L, Rizvi H, Seepersad D, Dworatzek S, et al. Comparison of anaerobic dechlorinating enrichment cultures maintained on tetrachloroethene, trichloroethene, cis-dichloroethene and vinyl chloride. Water Res. 2002;36:4193–202.
doi: 10.1016/S0043-1354(02)00151-3
Duhamel M, Edwards EA. Growth and yields of dechlorinators, acetogens, and methanogens during reductive dechlorination of chlorinated ethenes and dihaloelimination of 1, 2-dichloroethane. Environ Sci Technol. 2007;41:2303–10.
doi: 10.1021/es062010r
Major DJ, McMaster ML, Cox EE, Edwards EA, Dwortzek SM, Hendrickson ER, et al. Field demonstration of sucessful bioaugmentation to achieve dechlorination of tetrachloroethene to ethene. Environ Sci Technol. 2000;36:5106–16.
doi: 10.1021/es0255711
Major DW, McMaster ML, Cox EE, Edwards EA, Dworatzek SM, Hendrickson ER, et al. Field demonstration of successful bioaugmentation to achieve dechlorination of tetrachloroethene to ethene. Environ Sci Technol. 2002;36:5106–16.
doi: 10.1021/es0255711
Stroo HF, Leeson A, Ward CH. Bioaugmentation for Groundwater Remediation. New York, NY: Springer; 2012.
SiREM. http://www.siremlab.com . Accessed 14-June-2018.
Duhamel M, Mo K, Edwards EA. Characterization of a highly enriched Dehalococcoides-containing culture that grows on vinyl chloride and trichloroethene. Appl Environ Microbiol. 2004;70:5538–45.
doi: 10.1128/AEM.70.9.5538-5545.2004
Waller AS, Krajmalnik-Brown R, Loeffler FE, Edwards EA. Multiple reductive-dehalogenase-homologous genes are simultaneously transcribed during dechlorination by Dehalococcoides-containing cultures. Appl Environ Microbiol. 2005;71:8257–64.
doi: 10.1128/AEM.71.12.8257-8264.2005
Molenda O, Tang S, Lomheim L, Edwards EA. Eight new genomes of organohalide-respiring Dehalococcoides mccartyi reveal evolutionary trends in reductive dehalogenases. 2018;bioRxiv 345173; https://doi.org/10.1101/345173 .
Kocur CMD, Lomheim L, Molenda O, Weber KP, Austrins LM, Sleep BE, et al. Long-term field study of microbial community and dechlorinating activity following carboxymethyl cellulose-stabilized nanoscale zero-valent iron injection. Environ Sci Technol. 2016;50:7658–70.
doi: 10.1021/acs.est.6b01745
van der Zaan B, Hannes F, Hoekstra N, Rijnaarts H, de Vos WM, Smidt H, et al. Correlation of Dehalococcoides 16S rRNA and chloroethene-reductive dehalogenase genes with geochemical conditions in chloroethene-contaminated groundwater. Appl Environ Microbiol. 2010;76:843–50.
doi: 10.1128/AEM.01482-09
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.
doi: 10.1093/bioinformatics/btu170
Tang S, Gong Y, Edwards EA. Semi-automatic in silico gap closure enabled de novoassembly of two Dehalobacter genomes from metagenomic data. PLOS ONE. 2012;7:e52038 https://doi.org/10.1371/journal.pone.0052038 .
doi: 10.1371/journal.pone.0052038
Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJ, Birol I. ABySS: a parallel assembler for short read sequence data. Genome Res. 2009;19:1117–23.
doi: 10.1101/gr.089532.108
Gnerre SMI, Przybylski D, Ribeiro F, Burton J, Walker B, Sharpe T, et al. High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc Natl Acad Sci USA. 2011;108:1513–8.
doi: 10.1073/pnas.1017351108
Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics. 2011;27:578–9.
doi: 10.1093/bioinformatics/btq683
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–9.
doi: 10.1093/bioinformatics/bts199
Frank A, Lobry J. Oriloc: prediction of replication boundaries in unannotated bacterial chromosomes. Bioinformatics . 2000;16:566–7.
doi: 10.1093/bioinformatics/16.6.560
Aziz R, Bartels D, Best AD, M Disz T, Edwards R, Forsma K et al. The RAST server: rapid annotations using subsystems technology. BMC Genomics. 2008;9:1–75.
doi: 10.1186/1471-2164-9-75
Van Domselaar GH, Stothard P, Shrivastava S, Cruz JA, Guo A, Dong X, et al. BASys: a web server for automated bacterial genome annotation. Nucleic Acids Res. 2005;33:W455–W9. Web Server issue
doi: 10.1093/nar/gki593
Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP, Zaslavsky L, et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res. 2016;44:6614–24.
doi: 10.1093/nar/gkw569
Alikhan N-F, Petty NK, Ben Zakour NL, Beatson SA. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genom. 2011;12:402.
doi: 10.1186/1471-2164-12-402
Waller AS, Hug LA, Mo K, Radford DR, Maxwell KL, Edwards EA. Transcriptional analysis of a Dehalococcoides-containing microbial consortium reveals prophage activation. Appl Environ Microbiol. 2012;78:1178–86.
doi: 10.1128/AEM.06416-11
Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS. PHAST: a fast phage search tool. Nucleic Acids Res. 2011;39:W347–W52.
doi: 10.1093/nar/gkr485
Fouts DE. Phage_Finder: automated identification and classification of prophage regions in complete bacterial genome sequences. Nucleic Acids Res. 2006;34:5839–51.
doi: 10.1093/nar/gkl732
Zhao S, Ding C, He J. Genomic characterization of Dehalococcoides mccartyi strain 11a5 reveals a circular extrachromosomal genetic element and a new tetrachloroethene reductive dehalogenase gene. FEMS Microbiol Ecol. 2017;93:fiw235-fiw.
Dhillon BK, Laird MR, Shay JA, Winsor GL, Lo R, Nizam F, et al. IslandViewer 3: more flexible, interactive genomic island discovery, visualization and analysis. Nucleic Acids Res. 2015;43:W104–W8.
doi: 10.1093/nar/gkv401
Guy L, Kultima JR, Andersson SGE. genoPlotR: comparative gene and genome visualization in R. Bioinformatics . 2010;26:2334–5.
doi: 10.1093/bioinformatics/btq413
Hendrickson ER, Payne JA, Young RM, Starr MG, Perry MP, Fahnestock S, et al. Molecular analysis of Dehalococcoides 16S Ribosomal DNA from chloroethene-contaminated sites throughout North America and Europe. Appl Environ Microbiol. 2002;68:485–95.
doi: 10.1128/AEM.68.2.485-495.2002
Molenda O, Quaile AT, Edwards EA. Dehalogenimonas sp. strain WBC-2 genome and identification of its trans-dichloroethene reductive dehalogenase, TdrA. Appl Environ Microbiol. 2016;82:40–50.
doi: 10.1128/AEM.02017-15
Krajmalnik-Brown R, Holscher T, Thomson IN, Saunders FM, Ritalahti KM, Löffler FE. Genetic identification of a putative vinyl chloride reductase in Dehalococcoides sp. strain BAV1. Appl Environ Microbiol. 2004;70:6347–51.
doi: 10.1128/AEM.70.10.6347-6351.2004
Sung Y, Ritalahti KM, Apkarian RP, Löffler FE. Quantitative PCR confirms purity of strain GT, a novel trichloroethene-to-ethene-respiring Dehalococcoides isolate. Appl Environ Microbiol. 2006;72:1980–7.
doi: 10.1128/AEM.72.3.1980-1987.2006
Kube M, Beck A, Zinder SH, Kuhl H, Reinhardt R, Adrian L. Genome sequence of the chlorinated compound-respiring bacterium Dehalococcoides species strain CBDB1. Nat Biotech. 2005;23:1269–73.
doi: 10.1038/nbt1131
Pöritz M, Goris T, Wubet T, Tarkka MT, Buscot F, Nijenhuis I, et al. Genome sequences of two dehalogenation specialists - Dehalococcoides mccartyi strains BTF08 and DCMB5 enriched from the highly polluted Bitterfeld region. FEMS Microbiol Lett. 2013;343:101–4.
doi: 10.1111/1574-6968.12160
Gong B, Shin M, Sun J, Jung C-H, Bolt EL, van der Oost J, et al. Molecular insights into DNA interference by CRISPR-associated nuclease-helicase Cas3. Proc Natl Acad Sci USA. 2014;111:16359–64.
doi: 10.1073/pnas.1410806111
Makarova KS, Wolf YI, Alkhnbashi OS, Costa F, Shah SA, Saunders SJ, et al. An updated evolutionary classification of CRISPR-Cas systems. Nat Rev Micro. 2015;13:722–36.
doi: 10.1038/nrmicro3569
Huo Y, Nam KH, Ding F, Lee H, Wu L, Xiao Y, et al. Structures of CRISPR Cas3 offer mechanistic insights into Cascade-activated DNA unwinding and degradation. Nat Struct Mol Biol. 2014;21:771–7.
doi: 10.1038/nsmb.2875
Canchaya C, Proux C, Fournous G, Bruttin A, Brüssow H. Prophage genomics. Microbiol Mol Biol Rev. 2003;67:238–76.
doi: 10.1128/MMBR.67.2.238-276.2003
Wozniak RA, Waldor MK. Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat Rev Microbiol. 2010;8:552–63.
doi: 10.1038/nrmicro2382
Roberts AP, Chandler M, Courvalin P, Guedon G, Mullany P, Pembroke T, et al. Revised nomenclature for transposable genetic elements. Plasmid. 2008;60:167–73.
doi: 10.1016/j.plasmid.2008.08.001
Daccord A, Ceccarelli D, Rodrigue S, Burrus V. Comparative analysis of mobilizable genomic islands. J Bacteriol. 2013;195:606–14.
doi: 10.1128/JB.01985-12
Rankin DJ, Rocha EPC, Brown SP. What traits are carried on mobile genetic elements, and why? Heredity. 2011;106:1–10.
doi: 10.1038/hdy.2010.24
Zhao S, Ding C, He J. Genomic characterization of Dehalococcoides mccartyi strain 11a5 reveals a circular extrachromosomal genetic element and a new tetrachloroethene reductive dehalogenase gene. FEMS Microbiol Ecol. 2016;93:fiw235.
McDonnell GE, McConnell DJ. Overproduction, isolation, and DNA-binding characteristics of Xre, the repressor protein from the Bacillus subtilis defective prophage PBSX. J Bacteriol. 1994;176:5831–4.
doi: 10.1128/jb.176.18.5831-5834.1994
Ibarra JA, Pérez-Rueda E, Carroll RK, Shaw LN. Global analysis of transcriptional regulators in Staphylococcus aureus. BMC Genom. 2013;14:126.
doi: 10.1186/1471-2164-14-126
Barragan MJ, Blazquez B, Zamarro MT, Mancheno JM, Garcia JL, Diaz E et al. BzdR, a repressor that controls the anaerobic catabolism of benzoate in Azoarcus sp. CIB, is the first member of a new subfamily of transcriptional regulators. J Biol Chem. 2005;280:10683–94.
doi: 10.1074/jbc.M412259200
Tocchetti A, Galimberti G, Dehò G, Ghisotti D. Characterization of the oriI and oriII Origins of Replication in Phage-Plasmid P4. J Virol. 1999;73:7308–16.
pubmed: 10438819
pmcid: 104256
Ziegelin G, Scherzinger E, Lurz R, Lanka E. Phage P4 alpha protein is multifunctional with origin recognition, helicase and primase activities. EMBO J. 1993;12:3703–8.
doi: 10.1002/j.1460-2075.1993.tb06045.x
Briani F, Deho G, Forti F, Ghisotti D. The plasmid status of satellite bacteriophage P4. Plasmid. 2001;45:1–17.
doi: 10.1006/plas.2000.1497
Rojowska A, Lammens K, Seifert FU, Direnberger C, Feldmann H, Hopfner K-P. Structure of the Rad50 DNA double-strand break repair protein in complex with DNA. EMBO J. 2014;33:2847–59.
doi: 10.15252/embj.201488889
Ayora S, Carrasco B, Cardenas PP, Cesar CE, Canas C, Yadav T, et al. Double-strand break repair in bacteria: a view from Bacillus subtilis. FEMS Microbiol Rev. 2011;35:1055–81.
doi: 10.1111/j.1574-6976.2011.00272.x
Peeters N, Guidot A, Vailleau F, Valls M. Ralstonia solanacearum, a widespread bacterial plant pathogen in the post-genomic era. Mol Plant Pathol. 2013;14:651–62.
doi: 10.1111/mpp.12038
Krajmalnik-Brown R, Sung Y, Ritalahti KM, Saunders FM, Löffler FE. Environmental distribution of the trichloroethene reductive dehalogenase gene (tceA) suggests lateral gene transfer among Dehalococcoides. FEMS Microbiol Ecol. 2007;59:206–14.
doi: 10.1111/j.1574-6941.2006.00243.x
Hug LA, Maphosa F, Leys D, Löffler FE, Smidt H, Edwards EA, et al. Overview of organohalide-respiring bacteria and a proposal for a classification system for reductive dehalogenases. Philos Trans R Soc Biol Sci. 2013;368:1–10.
doi: 10.1098/rstb.2012.0322
Maphosa F, Smidt H, de Vos WM, Röling WFM. Microbial community- and metabolite dynamics of an anoxic dechlorinating bioreactor. Environ Sci Technol. 2010;44:4884–90.
doi: 10.1021/es903721s
Biswas A, Staals RHJ, Morales SE, Fineran PC, Brown CM. CRISPRDetect: a flexible algorithm to define CRISPR arrays. BMC Genom. 2016;17:356.
doi: 10.1186/s12864-016-2627-0
Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, et al. CRISPR provides acquired resistance against viruses in prokaryotes. Science. 2007;315:1709–12.
doi: 10.1126/science.1138140
Nuñez JK, Harrington LB, Kranzusch PJ, Engelman AN, Doudna JA. Foreign DNA capture during CRISPR–Cas adaptive immunity. Nature. 2015;527:535–8.
doi: 10.1038/nature15760
Ghinet MG, Bordeleau E, Beaudin J, Brzezinski R, Roy S, Burrus V. Uncovering the prevalence and diversity of integrating conjugative elements in Actinobacteria. PLOS One. 2011;6:e27846.
doi: 10.1371/journal.pone.0027846
Poele EMt, Bolhuis H, Dijkhuizen L. Actinomycete integrative and conjugative elements. Antonie Leeuwenhoek. 2008;94:127–43.
doi: 10.1007/s10482-008-9255-x
Possoz C, Ribard C, Gagnat J, Pernodet JL, Guerineau M. The integrative element pSAM2 from Streptomyces: kinetics and mode of conjugal transfer. Mol Microbiol. 2001;42:159–66.
doi: 10.1046/j.1365-2958.2001.02618.x
Vogelmann J, Ammelburg M, Finger C, Guezguez J, Linke D, Flötenmeyer M, et al. Conjugal plasmid transfer in Streptomyces resembles bacterial chromosome segregation by FtsK/SpoIIIE. EMBO J. 2011;30:2246–54.
doi: 10.1038/emboj.2011.121
Sezonov G, Duchene AM, Friedmann A, Guerineau M, Pernodet JL. Replicase, excisionase, and integrase genes of the Streptomyces element pSAM2 constitute an operon positively regulated by the pra gene. J Bacteriol. 1998;180:3056–61.
pubmed: 9620953
pmcid: 107804
Sezonov G, Hagege J, Pernodet JL, Friedmann A, Guerineau M. Characterization of pra, a gene for replication control in pSAM2, the integrating element of Streptomyces ambofaciens. Mol Microbiol. 1995;17:533–44.
doi: 10.1111/j.1365-2958.1995.mmi_17030533.x
Jiang W, Maniv I, Arain F, Wang Y, Levin BR, Marraffini LA. Dealing with the evolutionary downside of CRISPR immunity: bacteria and beneficial plasmids. PLoS Genet. 2013;9:e1003844.
doi: 10.1371/journal.pgen.1003844
Westra ER, Staals RHJ, Gort G, Høgh S, Neumann S, de la Cruz F, et al. CRISPR-Cas systems preferentially target the leading regions of MOBF conjugative plasmids. RNA Biol. 2013;10:749–61.
doi: 10.4161/rna.24202
Weinberger AD, Gilmore MS. CRISPR-Cas: to take up DNA or not, that is the question. Cell Host Microbe. 2012;12:125–6.
doi: 10.1016/j.chom.2012.07.007