Skip to main content
Log in

Phylogeny and compatibility: plasmid classification in the genomics era

  • Mini-Review
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Whole genome sequences are present-day bonanzas for taxonomists. Comparative genomics provides a promising perspective to reveal the evolutionary relationship between organisms, but this strategy is not applicable for extrachromosomal elements due to their high recombination frequencies. Classification of plasmids is based on their compatibility, i.e., the ability to coexist within the same cell. Compatibility testing is a laborious experimental discipline of pairwise comparisons developed for a small set of replicons. Thus, novel approaches are urgently required to deal with the exponentially increasing amount of sequence data. In this minireview, a short overview about the functional role and distribution of plasmids as well as a summary of recent strategies to classify the replicons via phylogenetic analyses is given. Our own work essentially bases on genes of the replication module, i.e., the replicase and two conserved partitioning genes and we exemplified this approach for the four different plasmid types from Alphaproteobacteria. It is suitable for a reliable classification of these replicons and allows in silico predictions about their compatibility. The development of a general classification scheme for plasmids from all microbial lineages will ensure a systematic assessment of the upcoming data flood and help to understand the distribution of extrachromosomal elements.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Bartosik D, Baj J, Wlodarczyk M (1998) Molecular and functional analysis of pTAV320, a repABC-type replicon of the Paracoccus versutus composite plasmid pTAV1. Microbiology 144:3149–3157

    Article  PubMed  CAS  Google Scholar 

  • Bartosik D, Szymanik M, Wysocka E (2001a) Identification of the partitioning site within the repABC-type replicon of the composite Paracoccus versutus plasmid pTAV1. J Bacteriol 183:6234–6243

    Article  PubMed  CAS  Google Scholar 

  • Bartosik D, Witkowska M, Baj J, Wlodarczyk M (2001b) Characterization and sequence analysis of the replicator region of the novel plasmid pALC1 from Paracoccus alcaliphilus. Plasmid 45:222–226

    Article  PubMed  CAS  Google Scholar 

  • Brinkhoff T, Giebel HA, Simon M (2008) Diversity, ecology, and genomics of the Roseobacter clade: a short overview. Arch Microbiol 189:531–539

    Article  PubMed  CAS  Google Scholar 

  • Carattoli A, Bertini A, Villa L, Falbo V, Hopkins KL, Threlfall EJ (2005) Identification of plasmids by PCR-based replicon typing. J Microbiol Methods 63:219–228

    Article  PubMed  CAS  Google Scholar 

  • Cevallos MA, Cervantes-Rivera R, Gutiérrez-Ríos RM (2008) The repABC plasmid family. Plasmid 60:19–37

    Article  PubMed  CAS  Google Scholar 

  • Chattoraj DK (2000) Control of plasmid DNA replication by iterons: no longer paradoxical. Mol Microbiol 37:467–476

    Article  PubMed  CAS  Google Scholar 

  • Couturier M, Bex F, Bergquist PL, Maas WK (1988) Identification and classification of bacterial plasmids. Microbiol Rev 52:375–395

    PubMed  CAS  Google Scholar 

  • Datta N (1985) Plasmids as organisms. In: Helinski DR, Cohen SN, Clewell DB, Jackson DA, Hollaender A (eds) Plasmids in bacteria. Plenum Publishing Corp, New York, pp 3–16

    Google Scholar 

  • Datta N, Hedges RW (1971) Compatibility groups among fi—R factors. Nature 234:222–223

    Article  PubMed  CAS  Google Scholar 

  • Doolittle WF, Papke RT (2006) Genomics and the bacterial species problem. Genome Biol 7:116

    Article  PubMed  Google Scholar 

  • Ebersbach G, Gerdes K (2005) Plasmid segregation mechanisms. Annu Rev Genet 39:453–479

    Article  PubMed  CAS  Google Scholar 

  • Figge RM, Easter J, Gober JW (2003) Productive interaction between the chromosome partitioning proteins, ParA and ParB, is required for the progression of the cell cycle in Caulobacter crescentus. Mol Microbiol 47:1225–1237

    Article  PubMed  CAS  Google Scholar 

  • Fornari CS, Watkins M, Kaplan S (1984) Plasmid distribution and analyses in Rhodopseudomonas sphaeroides. Plasmid 11:39–47

    Article  PubMed  CAS  Google Scholar 

  • Fredericq P (1963) On the nature of colicinogenic factors: a review. J Theoret Biol 4:159–165

    Article  CAS  Google Scholar 

  • Frost LS, Leplae R, Summers AO, Toussaint A (2005) Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol 3:722–732

    Article  PubMed  CAS  Google Scholar 

  • Garcillán-Barcia MP, Francia MV, de la Cruz F (2009) The diversity of conjugative relaxases and its application in plasmid classification. FEMS Microbiol Rev 33:657–687

    Article  PubMed  Google Scholar 

  • Gelvin SB (2003) Agrobacterium-mediated plant transformation: the biology behind the “gene-jockeying” tool. Microbiol Mol Biol Rev 67:16–37

    Article  PubMed  CAS  Google Scholar 

  • Goodner B, Hinkle G, Gattung S, Miller N, Blanchard M, Qurollo B et al (2001) Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294:2323–2328

    Article  PubMed  CAS  Google Scholar 

  • Jensen LB, Garcia-Migura L, Valenzuela AJS, Løhr M, Hasman H, Aarestrup FM (2010) A classification system for plasmids from enterococci and other Gram-positive bacteria. J Microbiol Methods 80:25–43

    Article  PubMed  CAS  Google Scholar 

  • MacLellan SR, Smallbone LA, Sibley CD, Finan TM (2005) The expression of a novel antisense gene mediates incompatibility within the large repABC family of alpha-proteobacterial plasmids. Mol Microbiol 55:611–623

    Article  PubMed  CAS  Google Scholar 

  • MacLellan SR, Zaheer R, Sartor AL, MacLean AM, Finan TM (2006) Identification of a megaplasmid centromere reveals genetic structural diversity within the repABC family of basic replicons. Mol Microbiol 59:1559–1575

    Article  PubMed  CAS  Google Scholar 

  • Messer W (2002) The bacterial replication initiator DnaA. DnaA and oriC, the bacterial mode to initiate DNA replication. FEMS Microbiol Rev 26:355–374

    PubMed  CAS  Google Scholar 

  • Moran MA, Belas R, Schell MA, González JM, Sun F, Sun S et al (2007) Ecological genomics of marine Roseobacters. Appl Environ Microbiol 73:4559–4569

    Article  PubMed  CAS  Google Scholar 

  • Moscoso M, Eritja R, Espinosa M (1997) Initiation of replication of plasmid pMV158: mechanisms of DNA strand-transfer reactions mediated by the initiator RepB protein. J Mol Biol 268:840–856

    Article  PubMed  CAS  Google Scholar 

  • Novick RP (1987) Plasmid incompatibility. Microbiol Rev 51:381–395

    PubMed  CAS  Google Scholar 

  • Petersen J, Brinkmann H, Pradella S (2009) Diversity and evolution of repABC type plasmids in Rhodobacterales. Environ Microbiol 11:2627–2638

    Article  PubMed  CAS  Google Scholar 

  • Petersen J, Brinkmann H, Berger M, Brinkhoff T, Päuker O, Pradella S (2010) Origin and evolution of a novel DnaA-like plasmid replication type in Rhodobacterales. Mol Biol Evol (in press)

  • Phillips G, Funnell B (2004). In: Funnel BE, Phillips JG (eds) Plasmid biology. ASM Press, Washington

  • Pistorio M, Giusti MA, Del Papa MF, Draghi WO, Lozano MJ, Tejerizo GT, Lagares A (2008) Conjugal properties of the Sinorhizobium meliloti plasmid mobilome. FEMS Microbiol Ecol 65:372–382

    Article  PubMed  CAS  Google Scholar 

  • Pradella S, Allgaier M, Hoch C, Päuker O, Stackebrandt E, Wagner-Döbler I (2004) Genome organization and localization of the pufLM genes of the photosynthesis reaction center in phylogenetically diverse marine Alphaproteobacteria. Appl Environ Microbiol 70:3360–3369

    Article  PubMed  CAS  Google Scholar 

  • Pradella S, Päuker O, Petersen J (2010) Genome organization of the marine Roseobacter clade member Marinovum algicola. Arch Microbiol 192:115–126

    Article  PubMed  CAS  Google Scholar 

  • Ramírez-Romero MA, Soberón N, Pérez-Oseguera A, Téllez-Sosa J, Cevallos MA (2000) Structural elements required for replication and incompatibility of the Rhizobium etli symbiotic plasmid. J Bacteriol 182:3117–3124

    Article  PubMed  Google Scholar 

  • Riley MA, Lizotte-Waniewski M (2009) Population genomics and the bacterial species concept. Methods Mol Biol 532:367–377

    Article  PubMed  CAS  Google Scholar 

  • Schumann W et al. (2008). In: Lipps G (ed). Plasmids: current research and future trends. Caister Academic Press, Norfolk, pp 1–263

  • Soberón N, Venkova-Canova T, Ramírez-Romero MA, Téllez-Sosa J, Cevallos MA (2004) Incompatibility and the partitioning site of the repABC basic replicon of the symbiotic plasmid from Rhizobium etli. Plasmid 51:203–216

    Article  PubMed  Google Scholar 

  • Swingley WD, Sadekar S, Mastrian SD, Matthies HJ, Hao J, Ramos H et al (2007) The complete genome sequence of Roseobacter denitrificans reveals a mixotrophic rather than photosynthetic metabolism. J Bacteriol 189:683–690

    Article  PubMed  CAS  Google Scholar 

  • Thomas CM (2000) Paradigms of plasmid organization. Mol Microbiol 37:485–491

    Article  PubMed  CAS  Google Scholar 

  • van den Ent F, Møller-Jensen J, Amos LA, Gerdes K, Löwe J (2002) F-actin-like filaments formed by plasmid segregation protein ParM. EMBO J 21:6935–6943

    Article  PubMed  Google Scholar 

  • Wagner-Döbler I, Ballhausen B, Berger M, Brinkhoff T, Buchholz I, Bunk B et al (2010) The complete genome sequence of the algal symbiont Dinoroseobacter shibae–a hitchhiker`s guide to life in the sea. ISME J. 4:61–77

    Article  PubMed  Google Scholar 

  • Wang Z, Jin L, Yuan Z, Wegrzyn G, Wegrzyn A (2009) Classification of plasmid vectors using replication origin, selection marker and promoter as criteria. Plasmid 61:47–51

    Article  PubMed  CAS  Google Scholar 

  • Zhong Z, Caspi R, Helinski D, Knauf V, Sykes S, O’Byrne C, Shea TP, Wilkinson JE, DeLoughery C, Toukdarian A (2003) Nucleotide sequence based characterizations of two cryptic plasmids from the marine bacterium Ruegeria isolate PR1b. Plasmid 49:233–252

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

I thank Henner Brinkmann for very helpful comments on the manuscript; Daniela Kalhöfer and Sebastian Thole for supplemental information about Roseobacter genomes; as well as two anonymous reviewers for their constructive criticism. This work was supported by the Volkswagen-Stiftung, VW-Vorab, Lower Saxony 11-7651-13-4/06 (ZN2235), and by the Transregional Collaborative Research Centre “Roseobacter” (Transregio TRR 51) of the Deutsche Forschungsgemeinschaft.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jörn Petersen.

Additional information

Communicated by Erko Stackebrandt.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Petersen, J. Phylogeny and compatibility: plasmid classification in the genomics era. Arch Microbiol 193, 313–321 (2011). https://doi.org/10.1007/s00203-011-0686-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-011-0686-9

Keywords

Navigation