Abstract
ABSTRACTThe discovery of integrative conjugative elements (ICEs) in wall-less mycoplasmas and the demonstration of their role in massive gene flows within and across species have shed new light on the evolution of these minimal bacteria. Of these, the ICE of the ruminant pathogen Mycoplasma agalactiae (ICEA) represents a prototype and belongs to a new clade of the Mutator-like superfamily that has no preferential insertion site and often occurs as multiple chromosomal copies. Here, functional genomics and mating experiments were combined to address ICEA functions and define the minimal ICEA chassis conferring conjugative properties to M. agalactiae. Data further indicated a complex interaction among coresident ICEAs, since the minimal ICEA structure was influenced by the occurrence of additional ICEA copies that can trans-complement conjugation-deficient ICEAs. However, this cooperative behavior was limited to the CDS14 surface lipoprotein, which is constitutively expressed by coresident ICEAs, and did not extend to other ICEA proteins, including the cis-acting DDE recombinase and components of the mating channel whose expression was detected only sporadically. Remarkably, conjugation-deficient mutants containing a single ICEA copy knocked out in cds14 can be complemented by neighboring cells expressing CDS14. This result, together with those revealing the conservation of CDS14 functions in closely related species, may suggest a way for mycoplasma ICEs to extend their interaction outside their chromosomal environment. Overall, this report provides a first model of conjugative transfer in mycoplasmas and offers valuable insights into understanding horizontal gene transfer in this highly adaptive and diverse group of minimal bacteria.
Highlights
The discovery of integrative conjugative elements (ICEs) in wall-less mycoplasmas and the demonstration of their role in massive gene flows within and across species have shed new light on the evolution of these minimal bacteria
Evidence for horizontal gene transfer (HGT) in these minimal bacteria came from the identification of putative Integrative conjugative elements (ICEs) in several species together with in silico data suggesting that mycoplasma species of distant phylogenetic groups have exchanged a significant amount of chromosomal DNA [14]
To elucidate the molecular mechanisms underlying ICE conjugative transfer in M. agalactiae, a library of 1,440 individual mutants was generated by random insertion of a minitransposon into the genome of strain 5632, which contains three nearly identical copies of a functional ICE of the ruminant pathogen Mycoplasma agalactiae (ICEA) (Fig. 1)
Summary
The discovery of integrative conjugative elements (ICEs) in wall-less mycoplasmas and the demonstration of their role in massive gene flows within and across species have shed new light on the evolution of these minimal bacteria. Conjugative properties of mycoplasmas were further demonstrated using the ruminant pathogen Mycoplasma agalactiae as a model organism [7, 12] In this species, mating experiments and associated next-generation sequencing analyses established that mycoplasma ICEs (MICEs) are self-transmissible mobile elements conferring to recipient cells the capacity to conjugate (Fig. 1). These uncovered at the same time an unconventional conjugative mechanism of chromosomal transfers (CTs) which involved large chromosomal regions and were independent of their genomic locations [12]. While ICE and CTs appeared to represent two independent events, CTs most likely rely on ICE factors for providing the conjugative pore
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