Gene cassette transcription in a large integron-associated array

Michael, Carolyn A.; Labbate, Maurizio

doi:10.1186/1471-2156-11-82

Cited by 27 publications

(26 citation statements)

References 25 publications

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“…It would be interesting to test whether there is a CRP control of the integron cassettes as it has been shown that other extracellular stresses can influence cassette expression in the Vibrio superintegron (52).…”

Section: Discussionmentioning

confidence: 99%

Connecting Environment and Genome Plasticity in the Characterization of Transformation-Induced SOS Regulation and Carbon Catabolite Control of the Vibrio cholerae Integron Integrase

2012

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bThe human pathogen Vibrio cholerae carries a chromosomal superintegron (SI). The SI contains an array of hundreds of gene cassettes organized in tandem which are stable under conditions when no particular stress is applied to bacteria (such as during laboratory growth). Rearrangements of these cassettes are catalyzed by the activity of the associated integron integrase. Understanding the regulation of integrase expression is pivotal to fully comprehending the role played by this genetic reservoir for bacterial adaptation and its connection with the development of antibiotic resistance. Our previous work established that the integrase is regulated by the bacterial SOS response and that it is induced during bacterial conjugation. Here, we show that transformation, another horizontal gene transfer (HGT) mechanism, also triggers integrase expression through SOS induction, underlining the importance of HGT in genome plasticity. Moreover, we report a new cyclic AMP (cAMP)-cAMP receptor protein (CRP)-dependent regulation mechanism of the integrase, highlighting the influence of the extracellular environment on chromosomal gene content. Altogether, our data suggest an interplay between different stress responses and regulatory pathways for the modulation of the recombinase expression, thus showing how the SI remodeling mechanism is merged into bacterial physiology. Vibrio cholerae is a marine bacterium that in humans is the causative agent of cholera, a condition that can be deadly if not appropriately treated. V. cholerae carries a superintegron (SI) on chromosome 2 that has an array of up to 200 promoterless gene cassettes separated by site-specific recombination sites recognized by the integron integrase IntIA (formerly called IntI4 [49]). IntIA catalyzes cassette excision and integration and generates combinations allowing the expression of some cassettes. Unlike the plasmid multiresistance integrons which carry gene cassettes that code for multiple antibiotic resistance genes, the SI codes mostly for cassettes of unknown functions (12,48). Both types of integrons are extremely stable under laboratory conditions; however, the integron integrases are functional (6), suggesting the existence of conditions in nature where the integrons are rearranged. The V. cholerae life cycle alternates between planktonic growth, biofilm formation on crustacean shells, and colonization of the intestinal tract during infection. In all cases, it cohabits with a variety of other bacteria, thus offering ample opportunities for genetic exchange.The V. cholerae integron integrase expression, like that of most integron integrases, has been found to be regulated by the bacterial SOS response, which is induced when an abnormal amount of single-stranded DNA (ssDNA) is present in the cell (13, 33). Recently, we further showed that ssDNA entry into both Escherichia coli and V. cholerae during conjugation induces the bacterial SOS response and the expression of IntIA, the SI integrase. Moreover, we showed that SOS induction by the incoming DNA d...

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Section: Discussionmentioning

confidence: 99%

Connecting Environment and Genome Plasticity in the Characterization of Transformation-Induced SOS Regulation and Carbon Catabolite Control of the Vibrio cholerae Integron Integrase

2012

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“…Either these cassettes are transcriptionally silent or they carry their own internal promoters. In the very long cassette arrays that characterize many Vibrio species, it appears that most cassettes are transcribed and that this transcription is enhanced by some stress treatments (90). Consequently, it seems likely that gene cassettes with internal promoters are scattered throughout the Vibrio arrays and that these help drive the expression of downstream cassettes.…”

Section: Expression Of Gene Cassettesmentioning

confidence: 99%

Integrons: Past, Present, and Future

Gillings

2014

Microbiol Mol Biol Rev

572

472

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SUMMARY Integrons are versatile gene acquisition systems commonly found in bacterial genomes. They are ancient elements that are a hot spot for genomic complexity, generating phenotypic diversity and shaping adaptive responses. In recent times, they have had a major role in the acquisition, expression, and dissemination of antibiotic resistance genes. Assessing the ongoing threats posed by integrons requires an understanding of their origins and evolutionary history. This review examines the functions and activities of integrons before the antibiotic era. It shows how antibiotic use selected particular integrons from among the environmental pool of these elements, such that integrons carrying resistance genes are now present in the majority of Gram-negative pathogens. Finally, it examines the potential consequences of widespread pollution with the novel integrons that have been assembled via the agency of human antibiotic use and speculates on the potential uses of integrons as platforms for biotechnology.

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“…4B). However, a recent study demonstrated that some cassettes within the array can include a promoter that controls the transcription of several genes (198). To be able to maintain such large numbers of unused genes, superintegrons contain postsegregation killing systems (see "Postsegregation killing systems," below).…”

Section: Fig 3 Schematic Organization Of a Diversity-generating Retromentioning

confidence: 99%

Bacterial Genome Instability

Darmon

Leach

2014

Microbiol Mol Biol Rev

348

289

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SUMMARY Bacterial genomes are remarkably stable from one generation to the next but are plastic on an evolutionary time scale, substantially shaped by horizontal gene transfer, genome rearrangement, and the activities of mobile DNA elements. This implies the existence of a delicate balance between the maintenance of genome stability and the tolerance of genome instability. In this review, we describe the specialized genetic elements and the endogenous processes that contribute to genome instability. We then discuss the consequences of genome instability at the physiological level, where cells have harnessed instability to mediate phase and antigenic variation, and at the evolutionary level, where horizontal gene transfer has played an important role. Indeed, this ability to share DNA sequences has played a major part in the evolution of life on Earth. The evolutionary plasticity of bacterial genomes, coupled with the vast numbers of bacteria on the planet, substantially limits our ability to control disease.

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Gene cassette transcription in a large integron-associated array

Cited by 27 publications

References 25 publications

Connecting Environment and Genome Plasticity in the Characterization of Transformation-Induced SOS Regulation and Carbon Catabolite Control of the Vibrio cholerae Integron Integrase

Connecting Environment and Genome Plasticity in the Characterization of Transformation-Induced SOS Regulation and Carbon Catabolite Control of the Vibrio cholerae Integron Integrase

Integrons: Past, Present, and Future

Bacterial Genome Instability

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