Presence of SXT integrating conjugative element in marine bacteria isolated from the mucus of the coral<i>Fungia echinata</i>from Andaman Sea

Badhai, Jhasketan; Kumari, Prabla; Krishnan, P.; Ramamurthy, Thandavarayan; Das, Subrata K.

doi:10.1111/1574-6968.12033

Cited by 26 publications

(16 citation statements)

References 31 publications

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“…SXT/R391 ICEs seem to have emerged in Asian V. cholerae clinical isolates in the early 1990s, subsequently spread in environmental and clinical strains in Asia and Africa, and have recently been found in all isolates recovered from cholera patients in Haiti (32,34,35,36). SXT/R391 ICEs are also naturally occurring in non-Vibrio pathogens (37,38,39).…”

Section: The Sxt/r391 Familymentioning

confidence: 99%

Biology of Three ICE Families: SXT/R391, ICE Bs1 , and ICE St1 /ICE St3

Carraro

Burrus

2014

Microbiol Spectr

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Integrative and Conjugative Elements (ICEs) are bacterial mobile genetic elements that play a key role in bacterial genomes dynamics and evolution. ICEs are widely distributed among virtually all bacterial genera. Recent extensive studies have unraveled their high diversity and complexity. The present review depicts the general conserved features of ICEs and describes more precisely three major families of ICEs that have been extensively studied in the past decade for their biology, their evolution and their impact on genomes dynamics. First, the large SXT/R391 family of ICEs disseminates antibiotic resistance genes and drives the exchange of mobilizable genomic islands (MGIs) between many enteric pathogens such as Vibrio cholerae. Second, ICEBs1 of Bacillus subtilis is the most well understood ICE of Gram-positive bacteria, notably regarding the regulation of its dissemination and its initially unforeseen extrachromosomal replication, which could be a common feature of ICEs of both Gram-positive and Gram-negative bacteria. Finally, ICESt1 and ICESt3 of Streptococcus thermophilus are the prototypes of a large family of ICEs widely distributed among various streptococci. These ICEs carry an original regulation module that associates regulators related to those of both SXT/R391 and ICEBs1. Study of ICESt1 and ICESt3 uncovered the cis-mobilization of related genomic islands (CIMEs) by a mechanism called accretion-mobilization, which likely represents a paradigm for the evolution of many ICEs and genomic islands. These three major families of ICEs give a glimpse about ICEs dynamics and their high impact on bacterial adaptation.

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Section: The Sxt/r391 Familymentioning

confidence: 99%

Biology of Three ICE Families: SXT/R391, ICE Bs1 , and ICE St1 /ICE St3

Carraro

Burrus

2014

Microbiol Spectr

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“…SXT integrates itself into the chromosome of V. cholerae in a site-specific manner at the 5= end of prfC, a gene coding for the peptide release factor RF3 (6). Since the discovery of SXT, SXT or related ICEs have been found to be prevalent in the seventh pandemic isolates of V. cholerae and sporadically present in other Vibrio species (7)(8)(9) and other Gammaproteobacteria of clinical origin or isolated from the aquatic environment, such as Photobacterium (10), Proteus (11), Alteromonas (12), Marinomonas (13), and Shewanella (9,14) species. SXT is closely related to R391, an ICE conferring resistance to kanamycin and mercury, originally detected in a 1967 South African isolate of Providencia rettgeri (15,16).…”

mentioning

confidence: 99%

A λ Cro-Like Repressor Is Essential for the Induction of Conjugative Transfer of SXT/R391 Elements in Response to DNA Damage

Poulin-Laprade

Burrus

2015

J Bacteriol

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Integrative and conjugative elements (ICEs) of the SXT/R391 family are the main contributors to acquired multidrug resistance in the seventh pandemic lineage of Vibrio cholerae, the etiological agent of the diarrheal disease cholera. Conjugative transfer of SXT/R391 ICEs is triggered by antibiotics and agents promoting DNA damage through RecA-dependent autoproteolysis of SetR, an ICE-encoded CI-like repressor. Here, we describe the role of CroS, a distant Cro homolog, as a key component contributing to the regulation of expression of the activator SetCD that orchestrates the expression of the conjugative transfer genes. We show that deletion of croS abolishes the SOS response-dependent induction of SXT despite the presence of a functional setR gene. Using quantitative reverse transcription-PCR and lacZ reporter assays, we also show that CroS represses setR and setCD expression by binding to operator sites shared with SetR. Furthermore, we provide evidence of an additional operator site bound by SetR and CroS. Finally, we show that SetCD expression generates a positive feedback loop due to SXT excision and replication in a fraction of the cell population. Together, these results refine our understanding of the genetic regulation governing the propagation of major vectors of multidrug resistance. IMPORTANCEHealthcare systems worldwide are challenged by an alarming drug resistance crisis caused by the massive and rapid propagation of antibiotic resistance genes and the associated emergence of multidrug-resistant pathogenic bacteria. SXT/R391 ICEs contribute to this phenomenon not only in clinical and environmental vibrios but also in several members of the family Enterobacteriaceae. We have identified and characterized here the regulator CroS as a key factor in the stimulation of conjugative transfer of these ICEs in response to DNA-damaging agents. We have also untangled conflicting evidence regarding autoactivation of transfer by the master activator of SXT/R391 ICEs, SetCD. Discovery of CroS provides a clearer and more complete understanding of the regulatory network that governs the dissemination of SXT/R391 ICEs in bacterial populations. Cholera is a severe infectious disease caused by the ingestion of food or water contaminated by Vibrio cholerae. This disease remains widespread in regions with limited access to clean water and where poor sanitation allows easy dissemination of the bacterium in drinking water sources. Cholera is characterized by a profuse watery diarrhea that rapidly induces massive fluid loss, causing severe dehydration of the patient, which may lead to death within 24 h of symptom onset. Although epidemic cholera is usually caused by V. cholerae O1, the unusual serogroup O139 emerged in the early 1990s as the cause of a cholera outbreak in India (1). O139 clinical isolates were found to be resistant to sulfamethoxazole and trimethoprim, two antibiotics commonly used for the treatment of severe cases of cholera (2). This resistance was found to be transmissible and linked to an integ...

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“…Marinomonas fungiae JCM 18476 T positive for SXT/R391 family related ICEs was used for genomic analysis (Badhai et al, 2013). The bacterium was routinely grown in marine agar 2216 (MA; Difco) at 28°C (Kumari et al, 2014).…”

Section: Methodsmentioning

confidence: 99%

Characterization of Three Novel SXT/R391 Integrating Conjugative Elements ICEMfuInd1a and ICEMfuInd1b, and ICEMprChn1 Identified in the Genomes of Marinomonas fungiae JCM 18476T and Marinomonas profundimaris Strain D104

Badhai

Das

2016

Front. Microbiol.

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The genus Marinomonas comprises Gram negative bacteria which are widespread in the marine environment and there is no report on the genomic analysis of SXT/R391 ICEs derived from this group of bacteria. This study describes the genomic features of three new SXT/R391 integrating conjugating elements (ICEs) identified in the genome of Marinomonas fungiae JCM 18476T (ICEMfuInd1a and ICEMfuInd1b) and in Marinomonas profundimaris strain D104 (ICEMprChn1). Structural organizations of the three ICEs were similar to the typical SXT/R391 family of ICEs and showed high degree of conservation in the core genes. Sequence analysis revealed ICEMfuInd1b and ICEMprChn1 were inserted into the genome at 5′-end of an typical host prfC gene, while ICEMfuInd1a was inserted at 5′-end of an atypical hipA-like gene. Despite their coexistence, the ICEMfuInd1a and ICEMfuInd1b were not present in a tandem fashion in the genome of M. fungiae. Phylogenetic analyses revealed the three ICEs either evolved independently or high degrees of recombination events had masked their evolution from a common SXT ancestor. Further, we found that the typical entry exclusion mechanism mediated by the TraG/EeX protein pair was likely defective in preventing the conjugative transfer of a second copy of the same S (SXT) group ICE into the M. fungiae genome due to mutations. Our analysis showed the presence of 16, 25, and 27 variable genes in the hotspots of ICEMfuInd1a, ICEMfuInd1b, and ICEMprChn1, respectively, many of which were not reported earlier for SXT/R391 ICEs. Sequence analysis predicted these hotspot regions were shaped by acquisition of genes through homologous recombination between the SXT and R391 related ICEs or mobile genetic elements present in disparate marine bacteria. Multidrug resistance genes which are hallmark feature of SXT/R391 ICEs were not present in either of the two ICEs from M. fungiae but were present within a transposon cassette in the HS-1 of the ICEMprChn1 from M. profundimaris. Finally, our data provided information on the genetic diversity and predicted functions encoded by variable genes present in the hotspot regions of these new ICEs.

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Presence of SXT integrating conjugative element in marine bacteria isolated from the mucus of the coralFungia echinatafrom Andaman Sea

Cited by 26 publications

References 31 publications

Biology of Three ICE Families: SXT/R391, ICE Bs1 , and ICE St1 /ICE St3

Biology of Three ICE Families: SXT/R391, ICE Bs1 , and ICE St1 /ICE St3

A λ Cro-Like Repressor Is Essential for the Induction of Conjugative Transfer of SXT/R391 Elements in Response to DNA Damage

Characterization of Three Novel SXT/R391 Integrating Conjugative Elements ICEMfuInd1a and ICEMfuInd1b, and ICEMprChn1 Identified in the Genomes of Marinomonas fungiae JCM 18476T and Marinomonas profundimaris Strain D104

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