scholarly journals A bistable orthogonal prokaryotic differentiation system underlying development of conjugative transfer competence

2021 ◽  
Author(s):  
Sandra Sulser ◽  
Andrea Vucicevic ◽  
Veronica Bellini ◽  
Roxane Moritz ◽  
Francois Delavat ◽  
...  

The mechanisms and impact of horizontal gene transfer processes to distribute gene functions with potential adaptive benefit among prokaryotes have been well documented. In contrast, little is known about the life-style of mobile elements mediating horizontal gene transfer, whereas this is the ultimate determinant for their transfer fitness. Here, we investigate the life-style of an integrative and conjugative element (ICE) within the genus Pseudomonas that stands model for a widespread family transmitting genes for xenobiotic compound metabolism and antibiotic resistances. The ICE only transfers from a small fraction of cells in a population, which we uncover here, results from a dedicated transfer competence program imposed by the ICE. Transfer competence is orthogonally maintained in individual cells in which it is activated, making them the centerpiece of ICE conjugation. The components mediating transfer competence are widely conserved, underscoring their selected fitness for efficient transfer of this class of mobile elements.

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Joshua M Jones ◽  
Ilana Grinberg ◽  
Avigdor Eldar ◽  
Alan D Grossman

Horizontal gene transfer is a major force in bacterial evolution. Mobile genetic elements are responsible for much of horizontal gene transfer and also carry beneficial cargo genes. Uncovering strategies used by mobile genetic elements to benefit host cells is crucial for understanding their stability and spread in populations. We describe a benefit that ICEBs1, an integrative and conjugative element of Bacillus subtilis, provides to its host cells. Activation of ICEBs1 conferred a frequency-dependent selective advantage to host cells during two different developmental processes: biofilm formation and sporulation. These benefits were due to inhibition of biofilm-associated gene expression and delayed sporulation by ICEBs1-containing cells, enabling them to exploit their neighbors and grow more prior to development. A single ICEBs1 gene, devI (formerly ydcO), was both necessary and sufficient for inhibition of development. Manipulation of host developmental programs allows ICEBs1 to increase host fitness, thereby increasing propagation of the element.


2007 ◽  
Vol 24 (12) ◽  
pp. 2802-2815 ◽  
Author(s):  
L. A. S. Snyder ◽  
S. McGowan ◽  
M. Rogers ◽  
E. Duro ◽  
E. O'Farrell ◽  
...  

2016 ◽  
Vol 113 (48) ◽  
pp. 13875-13880 ◽  
Author(s):  
Jun Ling ◽  
Hui Wang ◽  
Ping Wu ◽  
Tao Li ◽  
Yu Tang ◽  
...  

Horizontal gene transfer (HGT) of genomic islands is a driving force of bacterial evolution. Many pathogens and symbionts use this mechanism to spread mobile genetic elements that carry genes important for interaction with their eukaryotic hosts. However, the role of the host in this process remains unclear. Here, we show that plant compounds inducing the nodulation process in the rhizobium-legume mutualistic symbiosis also enhance the transfer of symbiosis islands. We demonstrate that the symbiosis island of theSesbania rostratasymbiont,Azorhizobium caulinodans, is an 87.6-kb integrative and conjugative element (ICEAc) that is able to excise, form a circular DNA, and conjugatively transfer to a specific site of gly-tRNA gene of other rhizobial genera, expanding their host range. The HGT frequency was significantly increased in the rhizosphere. An ICEAc-located LysR-family transcriptional regulatory protein AhaR triggered the HGT process in response to plant flavonoids that induce the expression of nodulation genes through another LysR-type protein, NodD. Our study suggests that rhizobia may sense rhizosphere environments and transfer their symbiosis gene contents to other genera of rhizobia, thereby broadening rhizobial host-range specificity.


2016 ◽  
Vol 198 (8) ◽  
pp. 1241-1249 ◽  
Author(s):  
Christopher M. Johnson ◽  
Alan D. Grossman

ABSTRACTConjugation in bacteria is the contact-dependent transfer of DNA from one cell to another via donor-encoded conjugation machinery. It is a major type of horizontal gene transfer between bacteria. Conjugation of the integrative and conjugative element ICEBs1intoBacillus subtilisis affected by the composition of phospholipids in the cell membranes of the donor and recipient. We found that reduction (or elimination) of lysyl-phosphatidylglycerol caused by loss ofmprFcaused a decrease in conjugation efficiency. Conversely, alterations that caused an increase in lysyl-phosphatidylglycerol, including loss ofugtPor overproduction ofmprF, caused an increase in conjugation efficiency. In addition, we found that mutations that alter production of other phospholipids, e.g., loss ofclsAandyfnI, also affected conjugation, apparently without substantively altering levels of lysyl-phosphatidylglycerol, indicating that there are multiple pathways by which changes to the cell envelope affect conjugation. We found that the contribution ofmprFto conjugation was affected by the chemical environment. Wild-type cells were generally more responsive to addition of anions that enhanced conjugation, whereasmprFmutant cells were more sensitive to combinations of anions that inhibited conjugation at pH 7. Our results indicate thatmprFand lysyl-phosphatidylglycerol allow cells to maintain relatively consistent conjugation efficiencies under a variety of ionic conditions.IMPORTANCEHorizontal gene transfer is a driving force in microbial evolution, enabling cells that receive DNA to acquire new genes and phenotypes. Conjugation, the contact-dependent transfer of DNA from a donor to a recipient by a donor-encoded secretion machine, is a prevalent type of horizontal gene transfer. Although critically important, it is not well understood how the recipient influences the success of conjugation. We found that the composition of phospholipids in the membranes of donors and recipients influences the success of transfer of the integrative and conjugative element ICEBs1inBacillus subtilis. Specifically, the presence of lysyl-phosphatidylglycerol enables relatively constant conjugation efficiencies in a range of diverse chemical environments.


2019 ◽  
Author(s):  
Başak Öztürk ◽  
Johannes Werner ◽  
Jan P. Meier-Kolthoff ◽  
Boyke Bunk ◽  
Cathrin Spröer ◽  
...  

AbstractBiodegradation of the phenylurea herbicide linuron appears a specialization within a specific clade of the Variovorax genus. The linuron catabolic ability is likely acquired by horizontal gene transfer but the mechanisms involved are not known. The full genome sequences of six linuron degrading Variovorax strains isolated from geographically distant locations were analyzed to acquire insight in the mechanisms of genetic adaptation towards linuron metabolism in Variovorax. Whole genome sequence analysis confirmed the phylogenetic position of the linuron degraders in a separate clade within Variovorax and indicated their unlikely origin from a common ancestral linuron degrader. The linuron degraders differentiated from non-degraders by the presence of multiple plasmids of 20 to 839 kb, including plasmids of unknown plasmid groups. The linuron catabolic gene clusters showed (i) high conservation and synteny and (ii) strain-dependent distribution among the different plasmids. All were bordered by IS1071 elements forming composite transposon structures appointing IS1071 as key for catabolic gene recruitment. Most of the strain carried at least one broad host range plasmid that might have been a second instrument for catabolic gene acquisition. We conclude that clade 1Variovorax strains, despite their different geographical origin, made use of a limited genetic repertoire to acquire linuron biodegradation.ImportanceThe genus Variovorax and especially a clade of strains that phylogenetically separates from the majority of Variovorax species, appears to be a specialist in the biodegradation of the phenyl urea herbicide linuron. Horizontal gene transfer (HGT) likely played an essential role in the genetic adaptation of those strain to acquire the linuron catabolic genotype. However, we do not know the genetic repertoire involved in this adaptation both regarding catabolic gene functions as well as gene functions that promote HGT neither do we know how this varies between the different strains. These questions are addressed in this paper by analyzing the full genome sequences of six linuron degrading Variovorax strains. This knowledge is important for understanding the mechanisms that steer world-wide genetic adaptation in a particular species and this for a particular phenotypic trait as linuron biodegradation.


2019 ◽  
Author(s):  
Sotaro Takano ◽  
Akiko Koto ◽  
Ryo Miyazaki

AbstractThe integrative and conjugative element ICEclc, a prevalent mobile element in proteobacteria, is one of the experimental models for horizontal gene transfer. ICEclc is usually retained in a bacterial chromosome, but can be excised and transferred from the donor to other bacterial lineages. The horizontal transmission is accomplished by developing specialized transfer competent (tc) cells in the donor population. The tc cells entirely dedicate to the ICE transmission by sacrificing their proliferation, which results in an increase in the transfer frequency. The cell growth impairment is mediated by two specific genes, parA and shi, on ICEclc, but its mechanistic details and cellular dynamics are still unknown. We here developed fluorescence reporter strains to monitor intracellular behavior of ParA and Shi proteins as well as host cellular proliferation at the single-cell level. Superresolution imaging revealed that ParA colocalized with the host nucleoid while Shi diffused in cytoplasm during the growth impairment. Mutations in the Walker A motif of ParA diminished the inhibitory effect. Combining quantitative time-lapse microscopy and numerical simulations using mathematical models, we found that ParA and Shi initially blocked cell division and then, as time elapsed, inhibited cellular elongation. The parA-shi locus is highly conserved in other ICEs, and the ParA-Shi-mediated growth inhibition was still observed in different proteobacterial species, suggesting that the ICEs have evolved the system to efficiently distribute themselves in the niche. The results of our study provide mechanistic insight into the novel and unique system on ICEs and help to understand such epistatic interaction between ICE genes and host physiology that entails efficient horizontal gene transfer.Author summaryHorizontal gene transfer is a major diving force for bacterial evolution, which is frequently mediated by mobile DNA vectors, such as plasmids and bacteriophages. Integrative and conjugative elements (ICEs) are a relatively new class of mobile vectors, which normally integrate in a host chromosome but under certain conditions can be excised and transferred from the host to a new recipient cell via conjugation. Recent genomic studies estimated that ICEs are more abundant than plasmids among bacteria. Why so prevalent? One of the characteristics of ICEclc, an ICE model in proteobacteria, is that it develops specialized cells which entirely dedicate to the ICE horizontal transmission by repressing their proliferation. Here, we qualitatively and quantitatively describe two proteins, which are expressed from ICEclc when it transfers, and how they actually inhibit the host cell growth. Our results suggest that the system has evolved for the efficient horizontal transmission and is widely conserved in the ICE family.


2016 ◽  
Vol 113 (24) ◽  
pp. E3375-E3383 ◽  
Author(s):  
François Delavat ◽  
Sara Mitri ◽  
Serge Pelet ◽  
Jan Roelof van der Meer

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 theclcgenes for chlorocatechol metabolism) among singlePseudomonascells by using time-lapse microscopy. We find that ICEclcactivation 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.


2020 ◽  
Author(s):  
Joshua M. Jones ◽  
Ilana Grinberg ◽  
Avigdor Eldar ◽  
Alan D. Grossman

AbstractHorizontal gene transfer is a major force in bacterial evolution. Mobile genetic elements are responsible for much of horizontal gene transfer and also carry beneficial cargo genes. Uncovering strategies used by mobile genetic elements to benefit host cells is crucial for understanding their stability and spread in populations. We describe a benefit that ICEBs1, an integrative and conjugative element ofBacillus subtilis, provides to its host cells. Activation of ICEBs1conferred a frequency-dependent selective advantage to host cells during two different developmental processes: biofilm formation and sporulation. These benefits were due to inhibition of biofilm-associated gene expression and delayed sporulation by ICEBs1-containing cells, enabling them to exploit their neighbors and grow more prior to development. A single ICEBs1gene,devI(formerlyydcO), was both necessary and sufficient for inhibition of development. Manipulation of host developmental programs allows ICEBs1to increase host fitness, thereby increasing propagation of the element.


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