Skip to main content
SpringerLink
Log in

Interdomain Transfers of Sugar Transporters Overcome Barriers to Gene Expression

  • Protocol
Horizontal Gene Transfer

Part of the book series: Methods in Molecular Biology ((MIMB,volume 532))

Abstract

Horizontal gene transfer (HGT) is nature’s mechanism for sharing evolved physiological traits among the members of microbial communities. The extent to which such transfers can be successful is best illustrated by the fact that Archaea-derived genes are found in many bacterial genomes, particularly those in the hyperthermophile Thermotoga maritima. The success of these intergenomic transfers depends upon the successful transcription of the newly acquired archaeal genes using a bacterial transcription machinery that does not recognize archaeal transcriptional signals. To examine how nature solves this problem, we looked to the T. maritima genome for examples of interdomain transfers. Here we lay the groundwork to examine this problem by more clearly delineating the phylogenetic history of Archaea-derived transporter genes in this genome. We find that five of these polysaccharide transporters were derived from the Archaea and one came from the Archaea after that lineage inherited it from the Bacteria. These data can be used for more detailed examinations of the recombinations that allowed these transporters to be expressed in a bacterial host. This work will guide examinations of the genome sequences from other members of the Thermotogales, which will become available.

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

Access this chapter

Log in via an institution
Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Lawrence, J. G., Hendrickson, H. (2003) Lateral gene transfer: When will adolescence end? Mol Microbiol 50, 739–49.

    Article  CAS  PubMed  Google Scholar 

  2. Koonin, E. V. (2003) Horizontal gene transfer: The path to maturity. Mol Microbiol 50, 725–7.

    Article  CAS  PubMed  Google Scholar 

  3. Eisen, J. A. (2000) Horizontal gene transfer among microbial genomes: New insights from complete genome analysis. Curr Opin Genet Dev 10, 606–11.

    Article  CAS  PubMed  Google Scholar 

  4. Ochman, H., Lawrence, J. G., Groisman, E. A. (2000) Lateral gene transfer and the nature of bacterial innovation. Nature Rev Genet 405, 299–304.

    CAS  Google Scholar 

  5. Philippe, H., Douady, C. J. (2003) Horizontal gene transfer and phylogenetics. Curr Opin Microbiol 6, 498–505.

    Article  CAS  PubMed  Google Scholar 

  6. Gogarten, J. P., Doolittle, W. F., Lawrence, J. G. (2002) Prokaryotic evolution in light of gene transfer. Mol Biol Evol 19, 2226–38.

    CAS  PubMed  Google Scholar 

  7. Lawrence, J. G., Ochman, H. (1997) Amelioration of bacterial genomes: Rates of change and exchange. Mol Evol 44, 383–97.

    Article  CAS  Google Scholar 

  8. Bell, S. D., Magill, C. P., Jackson, S. P. (2001) Basal and regulated transcription in archaea. Biochem Soc Trans 29, 392–5.

    Article  CAS  PubMed  Google Scholar 

  9. Brochier-Armanet, C., Forterre, P. (2007) Widespread distribution of archaeal reverse gyrase in thermophilic bacteria suggests a complex history of vertical inheritance and lateral gene transfers. Archaea 2, 83–93.

    Article  CAS  PubMed  Google Scholar 

  10. Longstaff, D. G., Larue, R. C., Faust, J. E., Mahapatra, A., Zhang, L., Green-Church, K. B., Krzycki, J. A. (2007) A natural genetic code expansion cassette enables transmissible biosynthesis and genetic encoding of pyrrolysine. Proc Natl Acad Sci USA 104, 1021–6.

    Article  CAS  PubMed  Google Scholar 

  11. Frigaard, N. U., Martinez, A., Mincer, T. J., Delong, E. F. (2006) Proteorhodopsin lateral gene transfer between marine planktonic bacteria and archaea. Nature 439, 847–50.

    Article  CAS  PubMed  Google Scholar 

  12. Chistoserdova, L., Vorholt, J. A., Lidstrom, M. E. (1998) C1 transfer enzymes and coenzymes linking methylotrophic bacteria and methanogenic archaea. Science 281, 99–102.

    Article  CAS  PubMed  Google Scholar 

  13. Nelson, K. E., Clayton, R. A., Gill, S. R., Gwinn, M. L., Dodson, R. J., Haft, D. H., Hickey, E. K., Peterson, J. D., Nelson, W. C., Ketchum, K. A., Mcdonald, L., Utterback, T. R., Malek, J. A., Linher, K. D., Garrett, M. M., Stewart, A. M., Cotton, M. D., Pratt, M. S., Phillips, C. A., Richardson, D., Heidelberg, J., Sutton, G. G., Fleischmann, R. D., Eisen, J. A., White, O., Salzberg, S. L., Smith, H. O., Venter, J. C., Fraser, C. M. (1999) Evidence for lateral gene transfer between archaea and bacteria from the genome sequence of Thermotoga maritima. Nature 399, 323–9.

    Article  CAS  PubMed  Google Scholar 

  14. Logsdon, J. M., Jr (1999) Evolutionary genomics: Thermotoga heats up lateral gene transfer. Curr Biol 9, R747–51.

    Article  CAS  PubMed  Google Scholar 

  15. Huber, R., Langworthy, T. A., König, H., Thomm, M., Woese, C. R., Sleytr, U. B., Stetter, K. O. (1986) Thermotoga maritima sp. nov. represents a new genus of unique extremely thermophilic eubacteria growing up to \(90^{\circ}{\rm C}\). Arch Microbiol 144, 324–33.

    Article  CAS  Google Scholar 

  16. Belkin, S., Wirsen, C. O., Jannasch, H. W. (1986) A new sulfur-reducing, extremely thermophilic eubacterium from a submarine thermal vent. Appl Environ Microbiol 51, 1180–5.

    CAS  PubMed  Google Scholar 

  17. Chhabra, S. R., Shockley, K. R., Conners, S. B., Scott, K. L., Wolfinger, R. D., Kelly, R. M. (2003) Carbohydrate-induced differential gene expression patterns in the hyperthermophilic bacterium Thermotoga maritima. J Biol Chem 278, 7540–52.

    Article  CAS  PubMed  Google Scholar 

  18. Nanavati, D. A., Thirangoon, K., Noll, K. M. (2006) Several archaeal homologs of putative oligopeptide-binding proteins encoded by Thermotoga maritima bind sugars. Appl Environ Microbiol 72, 1336–45.

    Article  CAS  PubMed  Google Scholar 

  19. Elferink, M. G. L., Albers, S. V., Konings, W. N., Driessen, A. J. M. (2001) Sugar transport in Sulfolobus solfataricus is mediated by two families of binding protein-dependent ABC transporters. Mol Microbiol 39, 1494–503.

    Article  CAS  PubMed  Google Scholar 

  20. Nesbo, C. L., L’haridon, S., Stetter, K. O., Doolittle, W. F. (2001) Phylogenetic analyses of two “archaeal” genes in Thermotoga maritima reveal multiple transfers between Archaea and Bacteria. Mol Biol Evol 18, 362–75.

    CAS  PubMed  Google Scholar 

  21. Tomii, K., Kanehisa, M. (1998) A comparative analysis of ABC transporters in complete microbial genomes. Genome Res 8, 1048–59.

    CAS  PubMed  Google Scholar 

  22. Tam, R., Saier, M. H., Jr. (1993) Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol Rev 57, 320–46.

    CAS  PubMed  Google Scholar 

  23. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., Lipman, D. J. (1990) Basic local alignment search tool. J Mol Biol 215, 403–10.

    CAS  PubMed  Google Scholar 

  24. Gish, W., States, D. J. (1993) Identification of protein coding regions by database similarity search. Nature Genet 3, 266–72.

    Article  CAS  PubMed  Google Scholar 

  25. Higgins, D., Sharp, P. (1988) Clustal: A package for performing multiple sequence alignments on a microcomputer. Genetics 73, 237–44.

    CAS  Google Scholar 

  26. Thompson, J., Higgins, D., Gibson, T. J. (1994) Clustal W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22, 4673–80.

    Article  CAS  PubMed  Google Scholar 

  27. Felsenstein, J. (2004) Phylip (Phylogenetic Inference Package). Department of Genetics, University of Washington Seattle, Seattle.

    Google Scholar 

  28. Guindon, S., Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52, 696–704.

    Article  PubMed  Google Scholar 

  29. Huelsenbeck, J. P., Ronquist, F. (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–5.

    Article  CAS  PubMed  Google Scholar 

  30. Holder, M. E., Roger, A. J. (1999) Puzzleboot. Bioinformatic Center, The University of British Columbia Place.

    Google Scholar 

  31. Kyte, J., Doolittle, R. F. (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157, 105–32.

    Article  CAS  PubMed  Google Scholar 

  32. Persson, B., Argos, P. (1994) Prediction of transmembrane segments in proteins utilising multiple sequence alignments. J Mol Biol 237, 182–92.

    Article  CAS  PubMed  Google Scholar 

  33. Albers, S.-V., Van De Vossenberg, J. L. C. M., Driessen, A. J. M., Konings, W. N. (2001) Bioenergetics and solute uptake under extreme conditions. Extremophiles 5, 285–94.

    CAS  PubMed  Google Scholar 

  34. Doolittle, W. F. (1999) Phylogenetic classification and the universal tree. Science 284, 2124–8.

    Article  CAS  PubMed  Google Scholar 

  35. Woese, C. R. (1998) The universal ancestor. Proc Natl Acad Sci USA 95, 6854–9.

    Article  CAS  PubMed  Google Scholar 

  36. Woese, C. R. (2000) Interpreting the universal phylogenetic tree. Proc Natl Acad Sci USA 97, 8392–6.

    Article  CAS  PubMed  Google Scholar 

  37. Frank, A. C., Amiri, H., Andersson, S. G. (2002) Genome deterioration: Loss of repeated sequences and accumulation of junk DNA. Genetica 115, 1–12.

    Article  PubMed  Google Scholar 

  38. Snel, B., Bork, P., Huynen, M. A. (2002) Genomes in flux: The evolution of archaeal and proteobacterial gene content. Genomic Research 12, 17–25.

    Article  CAS  Google Scholar 

  39. Lawrence, J. G., Roth, J. R. (1996) Selfish operons: Horizontal transfer may drive the evolution of gene clusters. Genetics 143, 1843–60.

    CAS  PubMed  Google Scholar 

  40. Lawrence, J. (1999) Selfish operons: The evolutionary impact of gene clustering in prokaryotes and eukaryotes. Curr Opin Genet Dev 9, 642–8.

    Article  CAS  PubMed  Google Scholar 

  41. Omelchenko, M. V., Makarova, K. S., Wolf, Y. I., Rogozin, I. B., Koonin, E. V. (2003) Evolution of mosaic operons by horizontal gene transfer and gene displacement in situ. Genome Biol 4, R55. Epub.

    Article  PubMed  Google Scholar 

  42. Hickey, A. J., De Macario, E. C., Macario, A. J. L. (2002) Transcription in the Archaea: Basal factors, regulation, and stress-gene expression. Crit Rev Biochem Mol Biol 37, 537–99.

    Article  CAS  PubMed  Google Scholar 

  43. Lobry, J. R., Sueoka, N. (2002) Asymmetric directional mutation pressures in bacteria. Genome Biol 3, RESEARCH0058.

    Article  PubMed  Google Scholar 

  44. Sorek, R., Zhu, Y., Creevey, C. J., Francino, M. P., Bork, P., Rubin, E. M. (2007) Genome-wide experimental determination of barriers to horizontal gene transfer. Science 318, 1449–52.

    Article  CAS  PubMed  Google Scholar 

  45. Wood, A. G., Redborg, A. H., Cue, D. R., Whitman, W. B., Konisky, J. (1983) Complementation of ArgG and HisA mutations of Escherichia coli by DNA cloned from the archaebacterium Methanococcus voltae. J Bacteriol 156, 19–29.

    CAS  PubMed  Google Scholar 

  46. Yang, Y., Huang, Y. P., Shen, P. (2003) The 492-bp rm07 DNA fragment from the halophilic archaea confers promoter activity in all three domains of life. Curr Microbiol 47, 388–94.

    Article  CAS  PubMed  Google Scholar 

  47. De Vries, J., Herzfeld, T., Wackernagel, W. (2004) Transfer of plastid DNA from tobacco to the soil bacterium Acinetobacter sp. by natural transformation. Mol Microbiol 53, 323–34.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT, USA

    Kenneth M. Noll

  2. Department of Molecular and Cell Biology, University of Connecticut, CT, USA

    Kamolwan Thirangoon

Authors
  1. Kenneth M. Noll
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kamolwan Thirangoon
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. University of Connecticut, 968 Warrenville Road, Mansfield Center, CT 06250, USA

    Maria Boekels Gogarten

  2. Dept. Molecular & Cell Biology, University of Connecticut, 91 North Eagleville Rd., Storrs, CT 06269-3125, USA

    Johann Peter Gogarten

  3. Biology Department, St. Lawrence University, 23 Romoda Drive, Canton, NY 13617, USA

    Lorraine C. Olendzenski

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Humana Press, a part of Springer Science+Business Media, LLC

About this protocol

Cite this protocol

Noll, K.M., Thirangoon, K. (2009). Interdomain Transfers of Sugar Transporters Overcome Barriers to Gene Expression. In: Gogarten, M.B., Gogarten, J.P., Olendzenski, L.C. (eds) Horizontal Gene Transfer. Methods in Molecular Biology, vol 532. Humana Press. https://doi.org/10.1007/978-1-60327-853-9_18

Download citation

  • DOI: https://doi.org/10.1007/978-1-60327-853-9_18

  • Publisher Name: Humana Press

  • Print ISBN: 978-1-60327-852-2

  • Online ISBN: 978-1-60327-853-9

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation