Architecture and functions of a multipartite genome of the methylotrophic bacterium Paracoccus aminophilus JCM 7686, containing primary and secondary chromids

Dziewit L, Czarnecki J, Wibberg D, Radlinska M, Mrozek P, Szymczak M, Schlüter A, Pühler A, Bartosik D (2014)
BMC Genomics 15(1): 124.

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BACKGROUND: Paracoccus aminophilus JCM 7686 is a methylotrophic α-Proteobacterium capable of utilizing reduced one-carbon compounds as sole carbon and energy source for growth, including toxic N,N-dimethylformamide, formamide, methanol, and methylamines, which are widely used in the industry. P. aminophilus JCM 7686, as many other Paracoccus spp., possesses a genome representing a multipartite structure, in which the genomic information is split between various replicons, including chromids, essential plasmid-like replicons, with properties of both chromosomes and plasmids. In this study, whole-genome sequencing and functional genomics approaches were applied to investigate P. aminophilus genome information. RESULTS: The P. aminophilus JCM 7686 genome has a multipartite structure, composed of a single circular chromosome and eight additional replicons ranging in size between 5.6 and 438.1 kb. Functional analyses revealed that two of the replicons, pAMI5 and pAMI6, are essential for host viability, therefore they should be considered as chromids. Both replicons carry housekeeping genes, e.g. responsible for de novo NAD biosynthesis and ammonium transport. Other mobile genetic elements have also been identified, including 20 insertion sequences, 4 transposons and 10 prophage regions, one of which represents a novel, functional serine recombinase-encoding bacteriophage, ϕPam-6. Moreover, in silico analyses allowed us to predict the transcription regulatory network of the JCM 7686 strain, as well as components of the stress response, recombination, repair and methylation machineries. Finally, comparative genomic analyses revealed that P. aminophilus JCM 7686 has a relatively distant relationship to other representatives of the genus Paracoccus. CONCLUSIONS: P. aminophilus genome exploration provided insights into the overall structure and functions of the genome, with a special focus on the chromids. Based on the obtained results we propose the classification of bacterial chromids into two types: "primary" chromids, which are indispensable for host viability and "secondary" chromids, which are essential, but only under some environmental conditions and which were probably formed quite recently in the course of evolution. Detailed genome investigation and its functional analysis, makes P. aminophilus JCM 7686 a suitable reference strain for the genus Paracoccus. Moreover, this study has increased knowledge on overall genome structure and composition of members within the class Alphaproteobacteria.
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BMC Genomics
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15
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124
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Dziewit L, Czarnecki J, Wibberg D, et al. Architecture and functions of a multipartite genome of the methylotrophic bacterium Paracoccus aminophilus JCM 7686, containing primary and secondary chromids. BMC Genomics. 2014;15(1): 124.
Dziewit, L., Czarnecki, J., Wibberg, D., Radlinska, M., Mrozek, P., Szymczak, M., Schlüter, A., et al. (2014). Architecture and functions of a multipartite genome of the methylotrophic bacterium Paracoccus aminophilus JCM 7686, containing primary and secondary chromids. BMC Genomics, 15(1), 124. doi:10.1186/1471-2164-15-124
Dziewit, L., Czarnecki, J., Wibberg, D., Radlinska, M., Mrozek, P., Szymczak, M., Schlüter, A., Pühler, A., and Bartosik, D. (2014). Architecture and functions of a multipartite genome of the methylotrophic bacterium Paracoccus aminophilus JCM 7686, containing primary and secondary chromids. BMC Genomics 15:124.
Dziewit, L., et al., 2014. Architecture and functions of a multipartite genome of the methylotrophic bacterium Paracoccus aminophilus JCM 7686, containing primary and secondary chromids. BMC Genomics, 15(1): 124.
L. Dziewit, et al., “Architecture and functions of a multipartite genome of the methylotrophic bacterium Paracoccus aminophilus JCM 7686, containing primary and secondary chromids”, BMC Genomics, vol. 15, 2014, : 124.
Dziewit, L., Czarnecki, J., Wibberg, D., Radlinska, M., Mrozek, P., Szymczak, M., Schlüter, A., Pühler, A., Bartosik, D.: Architecture and functions of a multipartite genome of the methylotrophic bacterium Paracoccus aminophilus JCM 7686, containing primary and secondary chromids. BMC Genomics. 15, : 124 (2014).
Dziewit, Lukasz, Czarnecki, Jakub, Wibberg, Daniel, Radlinska, Monika, Mrozek, Paulina, Szymczak, Michal, Schlüter, Andreas, Pühler, Alfred, and Bartosik, Dariusz. “Architecture and functions of a multipartite genome of the methylotrophic bacterium Paracoccus aminophilus JCM 7686, containing primary and secondary chromids”. BMC Genomics 15.1 (2014): 124.

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PMID: 30131796
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PMID: 30410477
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PMID: 30459725
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PMID: 28794225
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PMID: 28856785
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PMID: 27233797
Three novel bacteriophages isolated from the East African Rift Valley soda lakes.
van Zyl LJ, Nemavhulani S, Cass J, Cowan DA, Trindade M., Virol J 13(1), 2016
PMID: 27912769
Why There Are No Essential Genes on Plasmids.
Tazzyman SJ, Bonhoeffer S., Mol Biol Evol 32(12), 2015
PMID: 25540453
Diversity and role of plasmids in adaptation of bacteria inhabiting the Lubin copper mine in Poland, an environment rich in heavy metals.
Dziewit L, Pyzik A, Szuplewska M, Matlakowska R, Mielnicki S, Wibberg D, Schlüter A, Pühler A, Bartosik D., Front Microbiol 6(), 2015
PMID: 26074880
Metagenomic insights into the bioaerosols in the indoor and outdoor environments of childcare facilities.
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PMID: 26020512
Genome-guided insight into the methylotrophy of Paracoccus aminophilus JCM 7686.
Dziewit L, Czarnecki J, Prochwicz E, Wibberg D, Schlüter A, Pühler A, Bartosik D., Front Microbiol 6(), 2015
PMID: 26347732

93 References

Daten bereitgestellt von Europe PubMed Central.

Molecular genetics of the genus Paracoccus: metabolically versatile bacteria with bioenergetic flexibility.
Baker SC, Ferguson SJ, Ludwig B, Page MD, Richter OM, van Spanning RJ., Microbiol. Mol. Biol. Rev. 62(4), 1998
PMID: 9841665
Nitrate-dependent [Fe(II)EDTA]2- oxidation by Paracoccus ferrooxidans sp. nov., isolated from a denitrifying bioreactor.
Kumaraswamy R, Sjollema K, Kuenen G, van Loosdrecht M, Muyzer G., Syst. Appl. Microbiol. 29(4), 2005
PMID: 16682296
Paracoccus methylutens sp. nov. - a new aerobic facultatively methylotrophic bacterium utilizing dichloromethane
AUTHOR UNKNOWN, 1998
Genome sequence of Paracoccus sp. Strain TRP, a Chlorpyrifos Biodegrader.
Li K, Wang S, Shi Y, Qu J, Zhai Y, Xu L, Xu Y, Song J, Liu L, Rahman MA, Yan Y., J. Bacteriol. 193(7), 2011
PMID: 21257769
Genome of a novel isolate of Paracoccus denitrificans capable of degrading N,N-dimethylformamide.
Siddavattam D, Karegoudar TB, Mudde SK, Kumar N, Baddam R, Avasthi TS, Ahmed N., J. Bacteriol. 193(19), 2011
PMID: 21914898
Plasmid occurrence and diversity in the genus Paracoccus.
Baj J, Piechucka E, Bartosik D, Wlodarczyk M., Acta Microbiol. Pol. 49(3-4), 2000
PMID: 11293660
Transposable modules generated by a single copy of insertion sequence ISPme1 and their influence on structure and evolution of natural plasmids of Paracoccus methylutens DM12.
Bartosik D, Putyrski M, Dziewit L, Malewska E, Szymanik M, Jagiello E, Lukasik J, Baj J., J. Bacteriol. 190(9), 2008
PMID: 18296518
Molecular characterization of functional modules of plasmid pWKS1 of Paracoccus pantotrophus DSM 11072.
Bartosik D, Baj J, Sochacka M, Piechucka E, Wlodarczyk M., Microbiology (Reading, Engl.) 148(Pt 9), 2002
PMID: 12213930
Molecular and functional analysis of pTAV320, a repABC-type replicon of the Paracoccus versutus composite plasmid pTAV1.
Bartosik D, Baj J, Wlodarczyk M., Microbiology (Reading, Engl.) 144 ( Pt 11)(), 1998
PMID: 9846751
Characterization of the replicator region of megaplasmid pTAV3 of Paracoccus versutus and search for plasmid-encoded traits.
Bartosik D, Baj J, Bartosik AA, Wlodarczyk M., Microbiology (Reading, Engl.) 148(Pt 3), 2002
PMID: 11882723
Identification and characterization of transposable elements of Paracoccus pantotrophus.
Bartosik D, Sochacka M, Baj J., J. Bacteriol. 185(13), 2003
PMID: 12813068
Identification and distribution of insertion sequences of Paracoccus solventivorans.
Bartosik D, Szymanik M, Baj J., Appl. Environ. Microbiol. 69(12), 2003
PMID: 14660342
Insights into the transposable mobilome of Paracoccus spp. (Alphaproteobacteria).
Dziewit L, Baj J, Szuplewska M, Maj A, Tabin M, Czyzkowska A, Skrzypczyk G, Adamczuk M, Sitarek T, Stawinski P, Tudek A, Wanasz K, Wardal E, Piechucka E, Bartosik D., PLoS ONE 7(2), 2012
PMID: 22359677
Identification of a transposable genomic island of Paracoccus pantotrophus DSM 11072 by its transposition to a novel entrapment vector pMMB2.
Mikosa M, Sochacka-Pietal M, Baj J, Bartosik D., Microbiology (Reading, Engl.) 152(Pt 4), 2006
PMID: 16549670
Isolation and characterization of a novel insertion sequence element, IS1248, in Paracoccus denitrificans.
Van Spanning RJ, De Boer AP, Slotboom DJ, Reijnders WN, Stouthamer AH., Plasmid 34(1), 1995
PMID: 7480167
Paracoccus aminophilus sp. nov. and Paracoccus aminovorans sp. nov., which utilize N,N-dimethylformamide.
Urakami T, Araki H, Oyanagi H, Suzuki K, Komagata K., Int. J. Syst. Bacteriol. 40(3), 1990
PMID: 2397196
DIY series of genetic cassettes useful in construction of versatile vectors specific for Alphaproteobacteria.
Dziewit L, Adamczuk M, Szuplewska M, Bartosik D., J. Microbiol. Methods 86(2), 2011
PMID: 21569803
Functional characterization of the type II PamI restriction-modification system derived from plasmid pAMI7 of Paracoccus aminophilus JCM 7686.
Dziewit L, Kuczkowska K, Adamczuk M, Radlinska M, Bartosik D., FEMS Microbiol. Lett. 324(1), 2011
PMID: 22092764
Identifying global regulators in transcriptional regulatory networks in bacteria.
Martinez-Antonio A, Collado-Vides J., Curr. Opin. Microbiol. 6(5), 2003
PMID: 14572541
Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins.
Maddocks SE, Oyston PC., Microbiology (Reading, Engl.) 154(Pt 12), 2008
PMID: 19047729
LuxR-family 'solos': bachelor sensors/regulators of signalling molecules.
Subramoni S, Venturi V., Microbiology (Reading, Engl.) 155(Pt 5), 2009
PMID: 19383698
Histidine protein kinases: key signal transducers outside the animal kingdom
AUTHOR UNKNOWN, 2002
Cross-talk towards the response regulator NtrC controlling nitrogen metabolism in Rhodobacter capsulatus.
Drepper T, Wiethaus J, Giaourakis D, Gross S, Schubert B, Vogt M, Wiencek Y, McEwan AG, Masepohl B., FEMS Microbiol. Lett. 258(2), 2006
PMID: 16640581
CheA-receptor interaction sites in bacterial chemotaxis.
Wang X, Vu A, Lee K, Dahlquist FW., J. Mol. Biol. 422(2), 2012
PMID: 22659323
The phosphate regulon and bacterial virulence: a regulatory network connecting phosphate homeostasis and pathogenesis.
Lamarche MG, Wanner BL, Crepin S, Harel J., FEMS Microbiol. Rev. 32(3), 2008
PMID: 18248418
C4-dicarboxylate carriers and sensors in bacteria.
Janausch IG, Zientz E, Tran QH, Kroger A, Unden G., Biochim. Biophys. Acta 1553(1-2), 2002
PMID: 11803016
The QseC adrenergic signaling cascade in Enterohemorrhagic E. coli (EHEC).
Hughes DT, Clarke MB, Yamamoto K, Rasko DA, Sperandio V., PLoS Pathog. 5(8), 2009
PMID: 19696934
The bacterial LexA transcriptional repressor.
Butala M, Zgur-Bertok D, Busby SJ., Cell. Mol. Life Sci. 66(1), 2009
PMID: 18726173
The stringent response and cell cycle arrest in Escherichia coli.
Ferullo DJ, Lovett ST., PLoS Genet. 4(12), 2008
PMID: 19079575
RelE, a global inhibitor of translation, is activated during nutritional stress.
Christensen SK, Mikkelsen M, Pedersen K, Gerdes K., Proc. Natl. Acad. Sci. U.S.A. 98(25), 2001
PMID: 11717402
Microbial molecular chaperones.
Lund PA., Adv. Microb. Physiol. 44(), 2001
PMID: 11407116
Cycling of RNAs on Hfq.
Wagner EG., RNA Biol 10(4), 2013
PMID: 23466677
Genome analysis of DNA repair genes in the alpha proteobacterium Caulobacter crescentus.
Martins-Pinheiro M, Marques RC, Menck CF., BMC Microbiol. 7(), 2007
PMID: 17352799
Shining a light on photolyases.
Menck CF., Nat. Genet. 32(3), 2002
PMID: 12410227
AlkB-mediated oxidative demethylation reverses DNA damage in Escherichia coli.
Falnes PO, Johansen RF, Seeberg E., Nature 419(6903), 2002
PMID: 12226668
Epigenetic regulation of the bacterial cell cycle.
Collier J., Curr. Opin. Microbiol. 12(6), 2009
PMID: 19783470
Novel non-specific DNA adenine methyltransferases.
Drozdz M, Piekarowicz A, Bujnicki JM, Radlinska M., Nucleic Acids Res. 40(5), 2011
PMID: 22102579
DNA repair by bacterial AlkB proteins.
Falnes PO, Rognes T., Res. Microbiol. 154(8), 2003
PMID: 14527653
Identification of the CysB-regulated gene, hslJ, related to the Escherichia coli novobiocin resistance phenotype.
Lilic M, Jovanovic M, Jovanovic G, Savic DJ., FEMS Microbiol. Lett. 224(2), 2003
PMID: 12892888
Insights into the 1.59-Mbp largest plasmid of Azospirillum brasilense CBG497.
Acosta-Cruz E, Wisniewski-Dye F, Rouy Z, Barbe V, Valdes M, Mavingui P., Arch. Microbiol. 194(9), 2012
PMID: 22481309
Introducing the bacterial 'chromid': not a chromosome, not a plasmid.
Harrison PW, Lower RP, Kim NK, Young JP., Trends Microbiol. 18(4), 2010
PMID: 20080407
Housekeeping genes essential for pantothenate biosynthesis are plasmid-encoded in Rhizobium etli and Rhizobium leguminosarum.
Villasenor T, Brom S, Davalos A, Lozano L, Romero D, Los Santos AG., BMC Microbiol. 11(), 2011
PMID: 21463532
Plasmids with a chromosome-like role in rhizobia.
Landeta C, Davalos A, Cevallos MA, Geiger O, Brom S, Romero D., J. Bacteriol. 193(6), 2011
PMID: 21217003
Type IV secretion: the Agrobacterium VirB/D4 and related conjugation systems.
Christie PJ., Biochim. Biophys. Acta 1694(1-3), 2004
PMID: 15546668
How proteins form disulfide bonds.
Depuydt M, Messens J, Collet JF., Antioxid. Redox Signal. 15(1), 2011
PMID: 20849374
Bacteriophages and pathogenicity: more than just providing a toxin?
Tinsley CR, Bille E, Nassif X., Microbes Infect. 8(5), 2006
PMID: 16698301
Importance of widespread gene transfer agent genes in alpha-proteobacteria.
Lang AS, Beatty JT., Trends Microbiol. 15(2), 2006
PMID: 17184993
Replicon-dependent bacterial genome evolution: the case of Sinorhizobium meliloti.
Galardini M, Pini F, Bazzicalupo M, Biondi EG, Mengoni A., Genome Biol Evol 5(3), 2013
PMID: 23431003
Phenotype profiling of Rhizobium leguminosarum bv. trifolii clover nodule isolates reveal their both versatile and specialized metabolic capabilities.
Mazur A, Stasiak G, Wielbo J, Koper P, Kubik-Komar A, Skorupska A., Arch. Microbiol. 195(4), 2013
PMID: 23417392
Why genes evolve faster on secondary chromosomes in bacteria.
Cooper VS, Vohr SH, Wrocklage SC, Hatcher PJ., PLoS Comput. Biol. 6(4), 2010
PMID: 20369015
Evolutionary effects of translocations in bacterial genomes.
Morrow JD, Cooper VS., Genome Biol Evol 4(12), 2012
PMID: 23160175
Intragenomic diversity of Rhizobium leguminosarum bv. trifolii clover nodule isolates.
Mazur A, Stasiak G, Wielbo J, Kubik-Komar A, Marek-Kozaczuk M, Skorupska A., BMC Microbiol. 11(), 2011
PMID: 21619713
Genome engineering in Vibrio cholerae: a feasible approach to address biological issues.
Val ME, Skovgaard O, Ducos-Galand M, Bland MJ, Mazel D., PLoS Genet. 8(1), 2012
PMID: 22253612
Extrachromosomal, extraordinary and essential--the plasmids of the Roseobacter clade.
Petersen J, Frank O, Goker M, Pradella S., Appl. Microbiol. Biotechnol. 97(7), 2013
PMID: 23435940

AUTHOR UNKNOWN, 2001
Rhizobium phaseoli symbiotic mutants with transposon Tn5 insertions.
Noel KD, Sanchez A, Fernandez L, Leemans J, Cevallos MA., J. Bacteriol. 158(1), 1984
PMID: 6325385
Heterotrophic growth of Thiobacillus A2 on sugars and organic acids.
Wood AP, Kelly DP., Arch. Microbiol. 113(3), 1977
PMID: 879963
Changes in the Rhizobium meliloti genome and the ability to detect supercoiled plasmids during bacteroid development
AUTHOR UNKNOWN, 1990
An improved method for transformation of E. coli with ColE1 derived plasmids
AUTHOR UNKNOWN, 1978
Basic phage electron microscopy.
Ackermann HW., Methods Mol. Biol. 501(), 2009
PMID: 19066816
GenDB--an open source genome annotation system for prokaryote genomes.
Meyer F, Goesmann A, McHardy AC, Bartels D, Bekel T, Clausen J, Kalinowski J, Linke B, Rupp O, Giegerich R, Puhler A., Nucleic Acids Res. 31(8), 2003
PMID: 12682369
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ., Nucleic Acids Res. 25(17), 1997
PMID: 9254694
Enzyme-specific profiles for genome annotation: PRIAM.
Claudel-Renard C, Chevalet C, Faraut T, Kahn D., Nucleic Acids Res. 31(22), 2003
PMID: 14602924
The COG database: an updated version includes eukaryotes.
Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA., BMC Bioinformatics 4(), 2003
PMID: 12969510
ISfinder: the reference centre for bacterial insertion sequences.
Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M., Nucleic Acids Res. 34(Database issue), 2006
PMID: 16381877
Artemis and ACT: viewing, annotating and comparing sequences stored in a relational database.
Carver T, Berriman M, Tivey A, Patel C, Bohme U, Barrell BG, Parkhill J, Rajandream MA., Bioinformatics 24(23), 2008
PMID: 18845581
EDGAR: a software framework for the comparative analysis of prokaryotic genomes.
Blom J, Albaum SP, Doppmeier D, Puhler A, Vorholter FJ, Zakrzewski M, Goesmann A., BMC Bioinformatics 10(), 2009
PMID: 19457249
PHYLIP - phylogeny inference package (version 3.2)
AUTHOR UNKNOWN, 1989

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