Definition
An important vehicle for lateral (or horizontal) gene transfer in bacteria is the integron: it enables the capture and expression of genes as small mobile elements, or gene cassettes. These mobile gene cassettes encompass a vast pool of genetic novelty, ostensibly for purposes of adaptation. In most cases, their functional annotation is obscured by their characteristically high sequence novelty. Our isolation and solving of protein structures encoded by the cassette metagenome reveals a relatively high proportion of completely novel folds. These newly defined crystal structures are found to encompass diverse topologies and fold families and delineate new protein domains.
Introduction
Bacteria dominate the planet; they are omnipresent, inhabiting a wide range of environments, including those appearing too extreme or inhospitable for life (Rothschild and Mancinelli 2001). Lateral gene transfer...
References
Bornberg-Bauer E, Alba MM. Dynamics and adaptive benefits of modular protein evolution. Curr Opin Struct Biol. 2013;23(3):459–66.
Boucher Y, Stokes HW. The roles of lateral gene transfer and vertical descent in vibrio evolution. In: Fabiano Lopes Thompson BA, Swings JG, editors. The biology of vibrios. Washington, DC: ASM Press; 2006. p. 84–94.
Boucher Y, Nesbo CL, Joss MJ, Robinson A, Mabbutt BC, Gillings MR, et al. Recovery and evolutionary analysis of complete integron gene cassette arrays from Vibrio. BMC Evol Biol. 2006;6:3.
Boucher Y, Labbate M, Koenig JE, Stokes HW. Integrons: mobilizable platforms that promote genetic diversity in bacteria. Trends Microbiol. 2007;15(7):301–9.
Cambray G, Guerout A, Mazel D. Integrons. Annu Rev Genet. 2010;44:141–66.
Cohen O, Gophna U, Pupko T. The complexity hypothesis revisited: connectivity rather than function constitutes a barrier to horizontal gene transfer. Mol Biol Evol. 2011;28(4):1481–9.
Deshpande CN, Harrop SJ, Boucher Y, Hassan KA, Di Leo R, Xu X, et al. Crystal structure of an integron gene cassette-associated protein from Vibrio cholerae identifies a cationic drug-binding module. PLoS One. 2011;6(3):e16934.
Elsaied H, Stokes HW, Nakamura T, Kitamura K, Fuse H, Maruyama A. Novel and diverse integron integrase genes and integron-like gene cassettes are prevalent in deep-sea hydrothermal vents. Environ Microbiol. 2007;9(9):2298–312.
Hall RM. Integrons and gene cassettes: hotspots of diversity in bacterial genomes. Ann N Y Acad Sci. 2012;1267:71–8.
Joss MJ, Koenig JE, Labbate M, Polz MF, Gillings MR, Stokes HW, et al. ACID: annotation of cassette and integron data. BMC Bioinformatics. 2009;10:118.
Koenig JE, Boucher Y, Charlebois RL, Nesbo C, Zhaxybayeva O, Bapteste E, et al. Integron-associated gene cassettes in Halifax Harbour: assessment of a mobile gene pool in marine sediments. Environ Microbiol. 2008;10(4):1024–38.
Koonin EV, Wolf YI. Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Res. 2008;36(21):6688–719.
Labbate M, Boucher Y, Luu I, Chowdhury PR, Stokes HW. Integron associated mobile genes: Just a collection of plug in apps or essential components of cell network hardware? Mob Genet Elements. 2012;2(1):13–8.
Lehmann C, Lim K, Chalamasetty VR, Krajewski W, Melamud E, Galkin A, et al. The HI0073/HI0074 protein pair from Haemophilus influenzae is a member of a new nucleotidyltransferase family: structure, sequence analyses, and solution studies. Proteins. 2003;50(2):249–60.
Robinson A, Wu PS, Harrop SJ, Schaeffer PM, Dosztanyi Z, Gillings MR, et al. Integron-associated mobile gene cassettes code for folded proteins: the structure of Bal32a, a new member of the adaptable alpha + beta barrel family. J Mol Biol. 2005;346(5):1229–41.
Robinson A, Guilfoyle AP, Harrop SJ, Boucher Y, Stokes HW, Curmi PM, et al. A putative house-cleaning enzyme encoded within an integron array: 1.8 A crystal structure defines a new MazG subtype. Mol Microbiol. 2007;66(3):610–21.
Robinson A, Guilfoyle AP, Sureshan V, Howell M, Harrop SJ, Boucher Y, et al. Structural genomics of the bacterial mobile metagenome: an overview. Methods Mol Biol. 2008;426:589–95.
Rothschild LJ, Mancinelli RL. Life in extreme environments. Nature. 2001;409(6823):1092–101.
Rowe-Magnus DA, Guerout AM, Biskri L, Bouige P, Mazel D. Comparative analysis of superintegrons: engineering extensive genetic diversity in the Vibrionaceae. Genome Res. 2003;13(3):428–42.
Roy Chowdhury P, Boucher Y, Hassan KA, Paulsen IT, Stokes HW, Labbate M. Genome sequence of Vibrio rotiferianus strain DAT722. J Bacteriol. 2011;193(13):3381–2.
Stokes HW, Holmes AJ, Nield BS, Holley MP, Nevalainen KM, Mabbutt BC, et al. Gene cassette PCR: sequence-independent recovery of entire genes from environmental DNA. Appl Environ Microbiol. 2001;67(11):5240–6.
Sureshan V, Deshpande CN, Boucher Y, Koenig JE, Stokes HW, Harrop SJ, et al. Integron gene cassettes: a repository of novel protein folds with distinct interaction sites. PLoS One. 2013;8(1):e52934.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer Science+Business Media New York
About this entry
Cite this entry
Mabbutt, B., Deshpande, C., Sureshan, V., Harrop, S.J. (2013). Integrons as Repositories of Genetic Novelty. In: Nelson, K. (eds) Encyclopedia of Metagenomics. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-6418-1_146-2
Download citation
DOI: https://doi.org/10.1007/978-1-4614-6418-1_146-2
Received:
Accepted:
Published:
Publisher Name: Springer, New York, NY
Online ISBN: 978-1-4614-6418-1
eBook Packages: Springer Reference Biomedicine and Life SciencesReference Module Biomedical and Life Sciences