Timing of integration into the chromosome is critical for the fitness of an integrative and conjugative element and its bacterial host

Author:

McKeithen-Mead Saria A.,Grossman Alan D.ORCID

Abstract

AbstractIntegrative and conjugative elements (ICEs) are major contributors to genome plasticity in bacteria. ICEs reside integrated in the chromosome of a host bacterium and are passively propagated during chromosome replication and cell division. When activated, ICEs excise from the chromosome and may be transferred through the ICE-encoded conjugation machinery into a recipient cell. Integration into the chromosome of the new host generates a stable transconjugant. Although integration into the chromosome of a new host is critical for the stable acquisition of ICEs, few studies have directly investigated the molecular events that occur in recipient cells during generation of a stable transconjugant. We found that integration of ICEBs1, an ICE ofBacillus subtilis, occurred several generations after initial transfer to a new host. Premature integration in new hosts led to cell death and hence decreased fitness of the ICE and transconjugants. Host lethality due to premature integration was caused by rolling circle replication that initiated in the integrated ICEBs1and extended into the host chromosome, resulting in catastrophic genome instability. Our results demonstrate that the timing of integration of an ICE is linked to cessation of autonomous replication of the ICE, and that perturbing this linkage leads to a decrease in ICE and host fitness due to a loss of viability of transconjugants. Linking integration to cessation of autonomous replication appears to be a conserved regulatory scheme for mobile genetic elements that both replicate and integrate into the chromosome of their host.Author SummaryHorizontal gene transfer helps drive microbial evolution, enabling bacteria to rapidly acquire new genes and traits. Integrative and conjugative elements (ICEs) are mobile genetic elements that reside integrated in the chromosome of a host bacterium and can transfer to other cells via a contact-dependent mechanism called conjugation. Some ICEs contain genes that confer important traits to their bacterial hosts, including antibiotic resistances, metabolic capabilities, and pathogenicity. Central to the propagation of ICEs and other mobile genetic elements is the balance between dissemination to new hosts and maintenance within a host, while minimizing the fitness burden imposed on their hosts. We describe an underlying regulatory mechanism that allows for an ICE that has entered into a nascent host to replicate and potentially spread to other hosts before integration into the chromosome. Integration occurs shortly after or concomitant with cessation of ICE replication. Disruption of this regulatory link results in premature integration and fitness defects for both the host and the ICE; lethality for the host and reduced spread of the ICE.

Publisher

Cold Spring Harbor Laboratory

同舟云学术

1.学者识别学者识别

2.学术分析学术分析

3.人才评估人才评估

"同舟云学术"是以全球学者为主线,采集、加工和组织学术论文而形成的新型学术文献查询和分析系统,可以对全球学者进行文献检索和人才价值评估。用户可以通过关注某些学科领域的顶尖人物而持续追踪该领域的学科进展和研究前沿。经过近期的数据扩容,当前同舟云学术共收录了国内外主流学术期刊6万余种,收集的期刊论文及会议论文总量共计约1.5亿篇,并以每天添加12000余篇中外论文的速度递增。我们也可以为用户提供个性化、定制化的学者数据。欢迎来电咨询!咨询电话:010-8811{复制后删除}0370

www.globalauthorid.com

TOP

Copyright © 2019-2024 北京同舟云网络信息技术有限公司
京公网安备11010802033243号  京ICP备18003416号-3