Abstract
Horizontal gene transfer greatly facilitates rapid genetic adaptation of bacteria to shifts in environmental conditions and colonization of new niches by allowing one-step acquisition of novel functions. Conjugation is a major mechanism of horizontal gene transfer mediated by conjugative plasmids and integrating conjugative elements (ICEs). While in most bacterial conjugative systems DNA translocation requires the assembly of a complex type IV secretion system (T4SS), in Actinobacteria a single DNA FtsK/SpoIIIE-like translocation protein is required. To date, the role and diversity of ICEs in Actinobacteria have received little attention. Putative ICEs were searched for in 275 genomes of Actinobacteria using HMM-profiles of proteins involved in ICE maintenance and transfer. These exhaustive analyses revealed 144 putative FtsK/SpoIIIE-type ICEs and 17 putative T4SS-type ICEs. Grouping of the ICEs based on the phylogenetic analyses of maintenance and transfer proteins revealed extensive exchanges between different sub-families of ICEs. 17 ICEs were found in Actinobacteria from the genus Frankia, globally important nitrogen-fixing microorganisms that establish root nodule symbioses with actinorhizal plants. Structural analysis of ICEs from Frankia revealed their unexpected diversity and a vast array of predicted adaptive functions. Frankia ICEs were found to excise by site-specific recombination from their host's chromosome in vitro and in planta suggesting that they are functional mobile elements whether Frankiae live as soil saprophytes or plant endosymbionts. Phylogenetic analyses of proteins involved in ICEs maintenance and transfer suggests that active exchange between ICEs cargo-borne and chromosomal genes took place within the Actinomycetales order. Functionality of Frankia ICEs in vitro as well as in planta lets us anticipate that conjugation and ICEs could allow the development of genetic manipulation tools for this challenging microorganism and for many other Actinobacteria.
Highlights
Actinobacteria are found in many different ecological niches
Repartition and diversity of AICEs in Actinobacteria, we carried out a large-scale in silico analysis using data extracted from the RefSeq database [21]
The predicted proteomes encoded by 275 genomes of Actinobacteria were screened using HHM profiles of protein orthologs associated with the functions of core modules of integrating conjugative elements (ICEs) previously identified in actinomycetes [9] (Figure 1 and Table 1): (i) integrases (Int) of the tyrosine or serine family of recombinases that are involved in ICE integration and excision, (ii) replication initiator proteins (Rep) of the RepSA- and RepAM-type, and putative polymerases of the Prim-Pol-type, and (iii) FtsK/SpoIIIE domain-containing proteins (Tra) that are involved in translocation of double-stranded chromosomal DNA
Summary
Actinobacteria are found in many different ecological niches. These high G+C Gram-positive bacteria are soil and aquatic inhabitants (e.g., Streptomyces, Micromonospora, Rhodococcus), plant symbionts (e.g., Frankia), plant and animal pathogens (e.g., Corynebacterium, Mycobacterium, Nocardia), or gastrointestinal commensals (e.g., Bifidobacterium). Nitrogen-fixing actinobacteria belonging to genus Frankia live as soil saprophytes and as endophytic symbionts in over 200 plant species [1]. These host plants (actinorhizal plants) are found on most continents, and the contribution of Frankia and actinorhizal plants to global nitrogen fixation is estimated at 25% [2,3]. The global environmental importance of Frankiae command more research to better understand their interactions with other microorganisms, and host plants
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