Comparative genome analysis of <scp><i>P</i></scp><i>seudomonas knackmussii</i> <scp>B</scp>13, the first bacterium known to degrade chloroaromatic compounds

Miyazaki, Ryo; Bertelli, Claire; Benaglio, Paola; Canton, Jonas; Coi, N De; Gharib, Walid H.; Gjoksi, Bebeka; Goesmann, Alexander; Greub, Gilbert; Harshman, Keith; Linke, Burkhard; Mikulic, Josip; Mueller, Linda; Nicolas, Damien; Robinson‐Rechavi, Marc; Rivolta, Carlo; Roggo, Clémence; Roy, Shantanu; Sentchilo, Vladimir; Siebenthal, Alexandra Von; Falquet, Laurent; Meer, Jan Roelof van der

doi:10.1111/1462-2920.12498

Cited by 53 publications

(66 citation statements)

References 84 publications

(111 reference statements)

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“…ICEs are still remarkably poorly understood considering their wide distribution in bacterial genomes and importance among conjugative systems (7). The system we study here, ICEclc, is an example of an abundant ICE family in a wide variety of γ-and β-proteobacteria (14,17), among which are several P. aeruginosa isolates (10,11,41). Our results enable us to draw a number of conclusions about the basic steps in the behavior of the ICEclc family.…”

Section: Discussionmentioning

confidence: 85%

“…It has been estimated that conjugative systems of ICEs are more abundant among bacteria than those of plasmids (7), yet we know far less about ICE behavior because they are difficult to follow and isolate. ICEs have attracted interest because they can transmit antibiotic resistance genes (8) and suspected virulence factors (9)(10)(11), but also genes for toxic compound degradation (12,13) and heavy metal resistance (14). Several evolutionary distinct families of ICEs have been described, which have a mechanistically similar lifestyle (4,6,15).…”

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confidence: 99%

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Highly variable individual donor cell fates characterize robust horizontal gene transfer of an integrative and conjugative element

Delavat

Mitri

Pelet

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

104

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Horizontal gene transfer is an important evolutionary mechanism for bacterial adaptation. However, given the typical low transfer frequencies in a bacterial population, little is known about the fate and interplay of donor cells and the mobilized DNA during transfer. Here we study transfer of an integrative and conjugative element (ICE) among individual live bacterial cells. ICEs are widely distributed mobile DNA elements that are different than plasmids because they reside silent in the host chromosome and are maintained through vertical descent. Occasionally, ICEs become active, excise, and transmit their DNA to a new recipient, where it is reintegrated. We develop a fluorescent tool to differentiate excision, transfer, and reintegration of a model ICE named ICEclc (for carrying the clc genes for chlorocatechol metabolism) among single Pseudomonas cells by using timelapse microscopy. We find that ICEclc activation is initiated in stationary phase cells, but excision and transfer predominantly occur only when such cells have been presented with new nutrients. Donors with activated ICE develop a number of different states, characterized by reduced cell division rates or growth arrest, persistence, or lysis, concomitant with ICE excision, and likely, ICE loss or replication. The donor cell state transitions can be described by using a stochastic model, which predicts that ICE fitness is optimal at low initiation rates in stationary phase. Despite highly variable donor cell fates, ICE transfer is remarkably robust overall, with 75% success after excision. Our results help to better understand ICE behavior and shed a new light on bacterial cellular differentiation during horizontal gene transfer.

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Section: Discussionmentioning

confidence: 85%

mentioning

confidence: 99%

Highly variable individual donor cell fates characterize robust horizontal gene transfer of an integrative and conjugative element

Delavat

Mitri

Pelet

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

104

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show abstract

“…Although mostly located on the bacterial chromosome (1), genes for efflux systems can be transmitted via mobile genetic elements like plasmids or integrative and conjugative elements (ICE) (4)(5)(6). Recently, we described a class of widespread ICE among beta-and gammaproteobacteria, which, through a region permissive for gene insertions, can carry a wide range of auxiliary gene functions (7)(8)(9). The currently best-studied model of this family, ICEclc, was originally found in Pseudomonas knackmussii B13 (9,10) and confers the ability to degrade 3-chlorocatechol and 2-aminophenol (7).…”

mentioning

confidence: 99%

“…Recently, we described a class of widespread ICE among beta-and gammaproteobacteria, which, through a region permissive for gene insertions, can carry a wide range of auxiliary gene functions (7)(8)(9). The currently best-studied model of this family, ICEclc, was originally found in Pseudomonas knackmussii B13 (9,10) and confers the ability to degrade 3-chlorocatechol and 2-aminophenol (7). Homologs to ICEclc, identifiable by a conserved "core" gene region, occur in a range of proteobacterial species, such as Ralstonia sp.…”

mentioning

confidence: 99%

The TetR-Type MfsR Protein of the Integrative and Conjugative Element (ICE) ICE clc Controls both a Putative Efflux System and Initiation of ICE Transfer

et al. 2014

Self Cite

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Integrative and conjugating elements (ICE) are self-transferable DNAs widely present in bacterial genomes, which often carry a variety of auxiliary genes of potential adaptive benefit. One of the model ICE is ICEclc, an element originally found in Pseudomonas knackmussii B13 and known for its propensity to provide its host with the capacity to metabolize chlorocatechols and 2-aminophenol. In this work, we studied the mechanism and target of regulation of MfsR, a TetR-type repressor previously found to exert global control on ICEclc horizontal transfer. By using a combination of ICEclc mutant and transcriptome analysis, gene reporter fusions, and DNA binding assays, we found that MfsR is a repressor of both its own expression and that of a gene cluster putatively coding for a major facilitator superfamily efflux system on ICEclc (named mfsABC). Phylogenetic analysis suggests that mfsR was originally located immediately adjacent to the efflux pump genes but became displaced from its original cis target DNA by a gene insertion. This resulted in divergence of the original bidirectional promoters into two separated individual regulatory units. Deletion of mfsABC did not result in a strong phenotype, and despite screening a large number of compounds and conditions, we were unable to define the precise current function or target of the putative efflux pump. Our data reconstruct how the separation of an ancestor mfsR-mfsABC system led to global control of ICEclc transfer by MfsR.

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“…Previous BRIG-based analyses only used target bacteria as the reference genome to compare closely related organisms [38,39]. This comparative analysis has been effectively applied to identify all the regions contained by the target bacterial genome.…”

Section: The Pz-ii Region With a Phosphoenolpyruvatecarbohydrate Phosmentioning

confidence: 99%

Comparative genome analysis of Streptococcus iniae DX09 reveals new insights into niche adaptation and competitive host colonisation ability

Liu¹,

Wang²,

Wang³

2017

Oncotarget

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Streptococcus iniae is a significant pathogen in a variety of marine and freshwater cultured fish species. Previous investigations on S. iniae have been limited to a single virulence gene or genome. However, different strains are associated with varying pathogenicity and niche adaptation properties. For comprehensive characterization of the genetic variations in S. iniae, whole-genome sequencing of S. iniae DX09 (isolated from diseased catfish) was performed and comparative genome analysis with eight S. iniae strains conducted to determine the virulence evolution patterns. Comparative analysis of all sequenced S. iniae revealed genome-genome variations, mainly in two plasticity zones, within genes encoding specific functions, such as the Ess/type VII secretion system and phosphoenolpyruvate-carbohydrate phosphotransferase system, reflecting adaptation to colonisation of specific host habitats. The plasticity zones analyzed in the S. iniae genome may be a paradigm rather than a unique combination of horizontal gene transfer and underlie the emergence of pathogenic Gram-positive bacteria.

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Comparative genome analysis of Pseudomonas knackmussii B13, the first bacterium known to degrade chloroaromatic compounds

Cited by 53 publications

References 84 publications

Highly variable individual donor cell fates characterize robust horizontal gene transfer of an integrative and conjugative element

Highly variable individual donor cell fates characterize robust horizontal gene transfer of an integrative and conjugative element

The TetR-Type MfsR Protein of the Integrative and Conjugative Element (ICE) ICE clc Controls both a Putative Efflux System and Initiation of ICE Transfer

Comparative genome analysis of Streptococcus iniae DX09 reveals new insights into niche adaptation and competitive host colonisation ability

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