Skip to main content Accessibility help
×
Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-25T06:55:56.947Z Has data issue: false hasContentIssue false

1 - Genomes in Motion: Gene Transfer as a Catalyst for Genome Change

from PART I - Theoretical Considerations on the Evolution of Bacterial Pathogens

Published online by Cambridge University Press:  16 September 2009

Michael Hensel
Affiliation:
Friedrich-Alexander-Universität Erlangen-Nürnberg, Germany
Herbert Schmidt
Affiliation:
Universität Hohenheim, Stuttgart
Get access

Summary

The change from species to species is not a change involving more and more additional atomistic changes, but a complete change of the primary pattern or reaction system into a new one, which afterwards may again produce intraspecific variation by micromutation.

– Richard Goldschmidt, 1940

INTRODUCTION

Despite our interest and motivation, bacteria are not particularly easy organisms to study; their niches are complex and poorly understood and the vast majority of these species are difficult to culture or to manipulate in the laboratory. Of all bacteria, it is pathogens whose physical, social, and economic impact on our day-to-day lives garners the most attention, from both scientists and non-scientists alike. As a result, pathogens are among the best-studied bacteria, and lessons we learn from them are often generalized to other, non-pathogenic bacteria. Not surprisingly, the first lessons learned in the so-called genomic era came from pathogens, which were the first organisms with fully sequenced genomes. The promise of genomics was that the limitations of conventional microbiology could be overcome by studies of genome sequences and careful analysis of the genes contained therein. Here we examine how genomics has shaped our understanding of microbial genome evolution and ask how extensible these lessons may be. Among the notions that attracted widespread attention was the finding that certain clusters of genes are specifically responsible for virulence and that these loci are often obviously of foreign origin, having been introduced by the then under-appreciated process of lateral gene transfer or LGT. Coming more than a decade after these findings, this volume is focused on the hugely influential role of LGT in the evolution of genomes, particularly those of pathogenic bacteria.

Type
Chapter
Information
Publisher: Cambridge University Press
Print publication year: 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andersson, J. O. (2000). Evolutionary genomics: Is Buchnera a bacterium or an organelle?Curr Biol, 10, R866–8.CrossRefGoogle ScholarPubMed
Andersson, J. O., and Andersson, S. G. (1999a). Genome degradation is an ongoing process in Rickettsia. Mol Biol Evol, 16, 1178–91.CrossRefGoogle ScholarPubMed
Andersson, J. O., and Andersson, S. G. (1999b). Insights into the evolutionary process of genome degradation. Curr Opin Genet Dev, 9, 664–71.CrossRefGoogle ScholarPubMed
Beiko, R. G., Harlow, T. J., and Ragan, M. A. (2005). Highways of gene sharing in prokaryotes. Proc Natl Acad Sci USA, 102, 14332–7.CrossRefGoogle ScholarPubMed
Bigot, S., Saleh, , Lesterlin, O. A., , C., et al. (2005). KOPS: DNA motifs that control E. coli chromosome segregation by orienting the FtsK translocase. EMBO J, 24, 3770–80.CrossRefGoogle ScholarPubMed
Blum, G., Ott, , Lischewski, M., , A., et al. (1994). Excision of large DNA regions termed pathogenicity islands from tRNA-specific loci in the chromosome of an Escherichia coli wild-type pathogen. Infect Immun, 62, 606–14.Google ScholarPubMed
Brown, J. R., Douady, C. J., Italia, M. J., Marshall, W. E., and Stanhope, M. J. (2001). Universal trees based on large combined protein sequence data sets. Nat Genet, 28, 281–5.CrossRefGoogle ScholarPubMed
Capiaux, H., Lesterlin, C., Perals, K., Louarn, J. M., and Cornet, F. (2002). A dual role for the FtsK protein in Escherichia coli chromosome segregation. EMBO Rep, 3, 532–6.CrossRefGoogle ScholarPubMed
Chapman, T. A., Wu, , Barchia, X. Y., , I., et al. (2006). Comparison of virulence gene profiles of Escherichia coli strains isolated from healthy and diarrheic swine. Appl Environ Microbiol, 72, 4782–95.CrossRefGoogle ScholarPubMed
Chistoserdova, L., Vorholt, J. A., Thauer, R. K., and Lidstrom, M. E. (1998). C1 transfer enzymes and coenzymes linking methylotrophic bacteria and methanogenic Archaea. Science, 281, 99–102.CrossRefGoogle ScholarPubMed
Cole, S. T., Eiglmeier, , Parkhill, K., , J., et al. (2001). Massive gene decay in the leprosy bacillus. Nature, 409, 1007–11.CrossRefGoogle ScholarPubMed
Day, W. A., Fernandez, R. E., and Maurelli, A. T. (2001). Pathoadaptive mutations that enhance virulence: genetic organization of the cadA regions of Shigella spp. Infect Immun, 69, 7471–80.CrossRefGoogle ScholarPubMed
Dobrindt, U., Hochhut, B., Hentschel, U., and Hacker, J. (2004). Genomic islands in pathogenic and environmental microorganisms. Nat Rev Microbiol, 2, 414–24.CrossRefGoogle ScholarPubMed
Doolittle, W. F. (1999a). Lateral genomics. Trends Cell Biol, 9, M5–8.CrossRefGoogle ScholarPubMed
Doolittle, W. F. (1999b). Phylogenetic classification and the universal tree. Science, 284, 2124–9.CrossRefGoogle ScholarPubMed
Fidopiastis, P. M., Sorum, H., and Ruby, E. G. (1999). Cryptic luminescence in the cold-water fish pathogen Vibrio salmonicida. Arch Microbiol, 171, 205–9.CrossRefGoogle ScholarPubMed
Fitz-Gibbon, S. T., and House, C. H. (1999). Whole genome-based phylogenetic analysis of free-living microorganisms. Nucleic Acids Res, 27, 4218–22.CrossRefGoogle ScholarPubMed
Friesen, T. L., Stukenbrock, , Liu, E. H., , Z., et al. (2006). Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet, 38, 953–6.CrossRefGoogle ScholarPubMed
Gogarten, J. P., Doolittle, W. F., and Lawrence, J. G. (2002). Prokaryotic evolution in light of gene transfer. Mol Biol Evol, 19, 2226–38.CrossRefGoogle ScholarPubMed
Goldschmidt, R. (1940). The material basis of evolution. New Haven, CT: Yale University Press.Google Scholar
Groisman, E. A., and Ochman, H. (1994). How to become a pathogen. Trends Microbiol, 2, 289–94.CrossRefGoogle ScholarPubMed
Groisman, E. A., and Ochman, H. (1997). How Salmonella became a pathogen. Trends Microbiol, 5, 343–9.CrossRefGoogle ScholarPubMed
Hacker, J., and Kaper, J. B. (2000). Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol, 54, 641–79.CrossRefGoogle ScholarPubMed
Hacker, J., Blum-Oehler, G., Mühldorfer, I., and Tschäpe, H. (1997). Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol Microbiol, 23, 1089–97.CrossRefGoogle ScholarPubMed
Hejnova, J., Dobrindt, , Nemcova, U., , R., et al. (2005). Characterization of the flexible genome complement of the commensal Escherichia coli strain A0 34/86 (O83 : K24 : H31). Microbiology, 151, 385–98.CrossRefGoogle Scholar
Hendrickson, H., and Lawrence, J. G. (2006). Selection for chromosome architecture in bacteria. J Mol Evol, 62, 615–29.CrossRefGoogle ScholarPubMed
Jain, R., Rivera, M. C., and Lake, J. A. (1999). Horizontal gene transfer among genomes: the complexity hypothesis. Proc Natl Acad Sci USA, 96, 3801–6.CrossRefGoogle ScholarPubMed
Kirkup, B. C., and Riley, M. A. (2004). Antibiotic-mediated antagonism leads to a bacterial game of rock-paper-scissors in vivo. Nature, 428, 412–4.CrossRefGoogle ScholarPubMed
Konstantinidis, K. T., and Tiedje, J. M. (2005). Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci USA, 102, 2567–72.CrossRefGoogle ScholarPubMed
Kurland, C. G. (2000). Something for everyone. Horizontal gene transfer in evolution. EMBO Rep, 1, 92–5.CrossRefGoogle Scholar
Lawrence, J. G. (1997). Selfish operons and speciation by gene transfer. Trends Microbiol, 5, 355–9.CrossRefGoogle ScholarPubMed
Lawrence, J. G. (1999). Selfish operons: the evolutionary impact of gene clustering in the prokaryotes and eukaryotes. Curr Opin Genet Dev, 9, 642–8.CrossRefGoogle ScholarPubMed
Lawrence, J. G. (2001). Catalyzing bacterial speciation: correlating lateral transfer with genetic headroom. Syst Biol, 50, 479–96.CrossRefGoogle ScholarPubMed
Lawrence, J. G. (2002). Gene transfer in bacteria: speciation without species? Theor Popul Biol, 61, 449–60.CrossRefGoogle ScholarPubMed
Lawrence, J. G. (2003). Gene organization: selection, selfishness, and serendipity. Annu Rev Microbiol, 57, 419–40.CrossRefGoogle ScholarPubMed
Lawrence, J. G. (2005). Horizontal and vertical gene transfer: the life history of pathogens. Contrib Microbiol, 12, 255–71.CrossRefGoogle ScholarPubMed
Lawrence, J. G., and Hendrickson, H. (2003). Lateral gene transfer: when will adolescence end? Mol Microbiol, 50, 739–49.CrossRefGoogle ScholarPubMed
Lawrence, J. G., and Hendrickson, H. (2004). Chromosome structure and constraints on lateral gene transfer. Dyn Genet, 2004, 319–36.Google Scholar
Lawrence, J. G., and Ochman, H. (1997). Amelioration of bacterial genomes: rates of change and exchange. J Mol Evol, 44, 383–97.CrossRefGoogle Scholar
Lawrence, J. G., and Ochman, H. (1998). Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci USA, 95, 9413–7.CrossRefGoogle ScholarPubMed
Lawrence, J. G., and Roth, J. R. (1996a). Evolution of coenzyme B12 synthesis among enteric bacteria: evidence for loss and reacquisition of a multigene complex. Genetics, 142, 11–24.Google ScholarPubMed
Lawrence, J. G., and Roth, J. R. (1996b). Selfish operons: horizontal transfer may drive the evolution of gene clusters. Genetics, 143, 1843–60.Google ScholarPubMed
Lawrence, J. G., Roth, J. R., and Charlebois, R. L. (1999). Genomic flux: genome evolution by gene loss and acquisition. Washington, DC: American Society for Microbiology.Google Scholar
Levy, O., Ptacin, J. L., Pease, P. J., et al. (2005). Identification of oligonucleotide sequences that direct the movement of the Escherichia coli FtsK translocase. Proc Natl Acad Sci USA, 102, 17618–23.CrossRefGoogle ScholarPubMed
Lobry, J. R., and Sueoka, N. (2002). Asymmetric directional mutation pressures in bacteria. Genome Biol, 3, RESEARCH0058.CrossRefGoogle ScholarPubMed
Lovegrove, F. E., Pena-Castillo, L., Mohammad, N., et al. (2006). Simultaneous host and parasite expression profiling identifies tissue-specific transcriptional programs associated with susceptibility or resistance to experimental cerebral malaria. BMC Genomics, 7, 295.CrossRefGoogle ScholarPubMed
Majewski, J., and Cohan, F. M. (1998). The effect of mismatch repair and heteroduplex formation on sexual isolation in Bacillus. Genetics, 148, 13–8.Google ScholarPubMed
Majewski, J., and Cohan, F. M. (1999). DNA sequence similarity requirements for interspecific recombination in Bacillus. Genetics, 153, 1525–33.Google ScholarPubMed
Mira, A., Ochman, H., and Moran, N. A. (2001). Deletional bias and the evolution of bacterial genomes. Trends Genet, 17, 589–96.CrossRefGoogle ScholarPubMed
Nakabachi, A., Yamashita, , Toh, A., , H., et al. (2006). The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science, 314, 267.CrossRefGoogle ScholarPubMed
Nakata, N., Tobe, T., Fukuda, I., et al. (1993). The absence of a surface protease, OmpT, determines the intercellular spreading ability of Shigella: the relationship between the ompT and kcpA loci. Mol Microbiol, 9, 459–68.CrossRefGoogle ScholarPubMed
Ochman, H., Soncini, F. C., Solomon, F., and Groisman, E. A. (1996). Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci USA, 93, 7800–4.CrossRefGoogle ScholarPubMed
Oliver, J. D., Roberts, D. M., White, V. K., Dry, M. A., and Simpson, L. M. (1986). Bioluminescence in a strain of the human pathogenic bacterium Vibrio vulnificus. Appl Environ Microbiol, 52, 1209–11.Google Scholar
Parkhill, J., Sebaihia, M., Preston, A., et al. (2003). Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet, 35, 32–40.CrossRefGoogle ScholarPubMed
Paulsen, I. T., Seshadri, R., Nelson, K. E., et al. (2002). The Brucella suis genome reveals fundamental similarities between animal and plant pathogens and symbionts. Proc Natl Acad Sci USA, 99, 13148–53.CrossRefGoogle ScholarPubMed
Rashid, R. A., Tabata, T. A., Oatley, M. J., et al. (2006). Expression of putative virulence factors of Escherichia coli O157:H7 differs in bovine and human infections. Infect Immun, 74, 4142–8.CrossRefGoogle ScholarPubMed
Razin, S. (1997). The minimal cellular genome of Mycoplasma. Indian J Biochem Biophys, 34, 124–30.Google ScholarPubMed
Schoolnik, G. K. (2002). Functional and comparative genomics of pathogenic bacteria. Curr Opin Microbiol, 5, 20–6.CrossRefGoogle ScholarPubMed
Skyberg, J. A., Johnson, T. J., Johnson, J. R., et al. (2006). Acquisition of avian pathogenic Escherichia coli plasmids by a commensal E. coli isolate enhances its abilities to kill chicken embryos, grow in human urine, and colonize the murine kidney. Infect Immun, 74, 6287–92.CrossRefGoogle ScholarPubMed
Snel, B., Bork, P., and Huynen, M. A. (1999). Genome phylogeny based on gene content. Nat Genet, 21, 108–10.CrossRefGoogle ScholarPubMed
Sonnenburg, J. L., Chen, C. T., and Gordon, J. I. (2006). Genomic and metabolic studies of the impact of probiotics on a model gut symbiont and host. PLoS Biol, 4, e413.CrossRefGoogle Scholar
Sueoka, N. (1988). Directional mutation pressure and neutral molecular evolution. Proc Natl Acad Sci USA, 85, 2653–7.CrossRefGoogle ScholarPubMed
Sueoka, N. (1992). Directional mutation pressure, selective constraints, and genetic equilibria. J Mol Evol, 34, 95–114.CrossRefGoogle ScholarPubMed
Tekaia, F., Lazcano, A., and Dujon, B. (1999). The genomic tree as revealed from whole proteome comparisons. Genome Res, 9, 550–7.Google ScholarPubMed
Tettelin, H., Masignani, V., Cieslewicz, M. J., et al. (2005). Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome”. Proc Natl Acad Sci USA, 102, 13950–5.CrossRefGoogle ScholarPubMed
Toth, I. K., Pritchard, L., and Birch, P. R. (2006). Comparative genomics reveals what makes an enterobacterial plant pathogen. Annu Rev Phytopathol, 44, 305–36.CrossRefGoogle ScholarPubMed
Visick, K. L., and Ruby, E. G. (2006). Vibrio fischeri and its host: it takes two to tango. Curr Opin Microbiol, 9, 632–8.CrossRefGoogle ScholarPubMed
Vulic, M., Lenski, R. E., and Radman, M. (1999). Mutation, recombination, and incipient speciation of bacteria in the laboratory. Proc Natl Acad Sci USA, 96, 7348–51.CrossRefGoogle ScholarPubMed
Yan, F., and Polk, D. B. (2004). Commensal bacteria in the gut: learning who our friends are. Curr Opin Gastroenterol, 20, 565–71.CrossRefGoogle Scholar
Zareie, M., Riff, J., Donato, K., et al. (2005). Novel effects of the prototype translocating Escherichia coli, strain C25 on intestinal epithelial structure and barrier function. Cell Microbiol, 7, 1782–97.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×