Identification, characterization and benefits of an exclusion system in an integrative and conjugative element of <i>Bacillus subtilis</i>

Avello, Monika; Davis, Kathleen P.; Grossman, Alan D.

doi:10.1111/mmi.14359

Cited by 25 publications

(43 citation statements)

References 62 publications

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“…1) Inhibition of development (described here) provides a growth advantage in biofilms and during sporulation. 2) Exclusion, mediated by yddJ , blocks the conjugation machinery and protects the host cell from lethal excessive transfer (Avello et al ., 2019). 3) An abortive infection mechanism, mediated by spbK ( yddK ) protects populations of ICE Bs1 host cells from predation by the lysogenic phage SPβ (Johnson et al ., 2020, manuscript in preparation).…”

Section: Discussionmentioning

confidence: 99%

“…It encodes an exclusion protein that enables ICE Bs1 -containing cells to block incoming transfer of additional copies of ICE Bs1 from other would-be donor cells (Avello et al ., 2019). Without YddJ, excessive attempted conjugation from surrounding cells can be lethal (Avello et al ., 2019). 2) spbK ( yddK ) is also expressed even when the conjugation genes are repressed.…”

Section: Introductionmentioning

confidence: 99%

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A mobile genetic element increases bacterial host fitness by manipulating development

Jones

Grinberg

Eldar

et al. 2020

Preprint

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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.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

A mobile genetic element increases bacterial host fitness by manipulating development

Jones

Grinberg

Eldar

et al. 2020

Preprint

Self Cite

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“…Any ICEBs1 donor strains containing a deletion of conG, ΔconG(5-805), were derived from MMB1283 (27). KPD210, a donor strain containing a complete deletion of yddJ, was derived from MA11 (12). For all Pspank(hy)-conG constructs, the conG PCR fragments were joined together, and then joined to two fragments amplified from pMMB1341 (27) by isothermal assembly.…”

Section: Strains and Allelesmentioning

confidence: 99%

Specificity and selective advantage of an exclusion system in the integrative and conjugative element ICEBs1 of Bacillus subtilis

Davis

Grossman

2021

Preprint

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Integrative and conjugative elements (ICEs) are mobile genetic elements capable of transferring their own and other DNA. They contribute to the spread of antibiotic resistances and other important traits for bacterial evolution. Exclusion is a mechanism used by many conjugative plasmids and a few ICEs to prevent their host cell from acquiring a second copy of the cognate element. ICEBs1 of Bacillus subtilis has an exclusion mechanism whereby the exclusion protein YddJ in a potential recipient inhibits the activity of the ICEBs1-encoded conjugation machinery in a potential donor. The target of YddJ-mediated exclusion is the conjugation protein ConG (a VirB6 homolog). Here we defined the regions of YddJ and ConG that confer exclusion specificity and determined the importance of exclusion to host cells. Using chimeras that had parts of ConG from ICEBs1 and the closely related ICEBat1 we identified a putative extracellular loop of ConG that conferred specificity for exclusion by the cognate YddJ. Using chimeras of YddJ from ICEBs1 and ICEBat1 we identified two regions in YddJ needed for exclusion specificity. We also found that YddJ-mediated exclusion reduced death of donor cells following conjugation into recipients. Donor death was dependent on the ability of transconjugants to themselves become donors and was reduced under osmo-protective conditions, indicating that death was likely due to alterations in the donor cell envelope caused by excessive conjugation. We postulate that elements that can have high frequencies of transfer likely evolved exclusion mechanisms to protect the host cells from excessive death.ImportanceHorizontal gene transfer is a driving force in bacterial evolution, responsible for the spread of many traits, including antibiotic and heavy metal resistances. Conjugation, one type of horizontal gene transfer, involves DNA transfer from donor to recipient cells through conjugation machinery and direct cell-cell contact. Exclusion mechanisms allow conjugative elements to prevent their host from acquiring additional copies of the element, and are highly specific enabling hosts to acquire heterologous elements. We defined regions of the exclusion protein and its target in the conjugation machinery that convey high specificity of exclusion. We found that exclusion protects donors from cell death during periods of high transfer. This is likely important for the element to enter new populations of cells.

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“…To mitigate the concerns of horizontal gene transfer, these methods of bioremediation would be utilized under circumstances where a pesticide has been discontinued. Additionally, if utilizing bioengineered or optimized bacteria there may be potential to include an exclusion system to prevent subsequent conjugation events and limit lateral gene transfer to other bacteria in the environment (Avello et al, 2019).…”

Section: Potential Strategies For Using Insect-associated Bacteria Fomentioning

confidence: 99%

Symbiont-Mediated Insecticide Detoxification as an Emerging Problem in Insect Pests

Blanton

Peterson

2020

Front. Microbiol.

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Pesticide use is prevalent with applications from the backyard gardener to large-scale agriculture and combatting pests in homes and industrial settings. Alongside the need to control unwanted pests comes the selective pressure generated by sustained pesticide use has become a concern leading to environmental contamination, pest resistance, and, thus, reduced pesticide efficacy. Despite efforts to improve the environmental impact and reduce off-target effects, chemical pesticides are relied on and control failures are costly. Though pesticide resistance mechanisms vary, one pattern that has recently emerged is symbiont-mediated detoxification within insect pests. The localization within the insect host, the identity of the symbiotic partner, and the stability of the associations across different systems vary. The diversity of insects and ecological settings linked to this phenomenon are broad. In this mini-review, we summarize the recent trend of insecticide detoxification modulated by symbiotic associations between bacteria and insects, as well as highlight the implications for pesticide development, pest management strategies, and pesticide bioremediation.

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Identification, characterization and benefits of an exclusion system in an integrative and conjugative element of Bacillus subtilis

Cited by 25 publications

References 62 publications

A mobile genetic element increases bacterial host fitness by manipulating development

A mobile genetic element increases bacterial host fitness by manipulating development

Specificity and selective advantage of an exclusion system in the integrative and conjugative element ICEBs1 of Bacillus subtilis

Symbiont-Mediated Insecticide Detoxification as an Emerging Problem in Insect Pests

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