Social behavior and decision making in bacterial conjugation

Abstract

Bacteria frequently acquire novel genes by horizontal gene transfer (HGT). HGT through the process of bacterial conjugation is highly efficient and depends on the presence of conjugative plasmids (CPs) or integrated conjugative elements (ICEs) that provide the necessary genes for DNA transmission. This review focuses on recent advancements in our understanding of ssDNA transfer systems and regulatory networks ensuring timely and spatially controlled DNA transfer (tra) gene expression. As will become obvious by comparing different systems, by default, tra genes are shut off in cells in which conjugative elements are present. Only when conditions are optimal, donor cells—through epigenetic alleviation of negatively acting roadblocks and direct stimulation of DNA transfer genes—become transfer competent. These transfer competent cells have developmentally transformed into specialized cells capable of secreting ssDNA via a T4S (type IV secretion) complex directly into recipient cells. Intriguingly, even under optimal conditions, only a fraction of the population undergoes this transition, a finding that indicates specialization and cooperative, social behavior. Thereby, at the population level, the metabolic burden and other negative consequences of tra gene expression are greatly reduced without compromising the ability to horizontally transfer genes to novel bacterial hosts. This undoubtedly intelligent strategy may explain why conjugative elements—CPs and ICEs—have been successfully kept in and evolved with bacteria to constitute a major driving force of bacterial evolution.

Regulation of conjugative transfer of plasmids and integrative conjugative elements

“…The relaxase, with the DNA strand attached, transfers to the recipient cell through the pore formed by the T4SS, finally the plasmid needs to be established in the recipient, with the help of ssDNA binding, anti-restriction and SOS inhibition proteins to generate stable transconjugants. (Alvarez-Martinez and Christie, 2009;Ding and Hynes, 2009;Frost et al, 2005;Koraimann and Wagner, 2014). It is interesting to note that expression of transfer genes is induced in a subset of the bacterial population, maybe diminishing the negative effects of the associated energy cost (Koraimann and Wagner, 2014).…”

“…Conjugative transfer requires the expression of transfer (tra) genes involved in DNA transfer and replication (Dtr) and in Mating pair formation (Mpf). Dtr genes are required for processing the DNA with a relaxase, which cuts the DNA molecule at the nic site of the origin of transfer (oriT), and remains attached to the single strand of DNA, which will be transferred responding to an undefined signal (Koraimann and Wagner, 2014). This complex, together with other proteins, makes up the relaxosome, A C C E P T E D M A N U S C R I P T 6 which directs the strand to the type 4 secretion system (T4SS), a multiprotein complex located in the membrane of the cell.…”

Fitness Costs of Plasmids: a Limit to Plasmid Transmission

“…To minimize this cost, plasmids tightly control the expression of conjugative systems (41,(61)(62)(63). The result is a general repression of conjugation genes, with only a few cells in the population expressing the conjugative machinery (63). Conjugation can, however, be derepressed, either through chemical signaling (61,62) or through transcriptional overshooting of conjugative genes in new recipient cells (41,42), enabling a wave of plasmid transfer when there are recipient bacteria available in the population.…”

“…The fitness cost associated with conjugation comes primarily from the high ATP demand for mating-channel formation and plasmid DNA translocation (58). To minimize this cost, plasmids tightly control the expression of conjugative systems (41,(61)(62)(63). The result is a general repression of conjugation genes, with only a few cells in the population expressing the conjugative machinery (63).…”

csrT Represents a New Class of csrA -Like Regulatory Genes Associated with Integrative Conjugative Elements of Legionella pneumophila

“…ICEs have expanded the genetic repertoire of a number of bacterial pathogens by carrying a variety of cargo genes that confer advantageous traits for their hosts, enhancing fitness in specific environments. Some ICEs provide resistance to antibiotics, metal ions, and oxidative stress; others enhance nitrogen and chlorobenzoate metabolism, biofilm formation, and host cell infection (2)(3)(4)(5). In addition to cargo genes are those encoding the elements' structural components.…”