Structure, Diversity, and Mobility of the Salmonella Pathogenicity Island 7 Family of Integrative and Conjugative Elements within Enterobacteriaceae

Abstract

Integrative and conjugative elements (ICEs) are self-mobile genetic elements found in the genomes of some bacteria. These elements may confer a fitness advantage upon their host bacteria through the cargo genes that they carry. Salmonella pathogenicity island 7 (SPI-7), found within some pathogenic strains of Salmonella enterica, possesses features indicative of an ICE and carries genes implicated in virulence. We aimed to identify and fully analyze ICEs related to SPI-7 within the genus Salmonella and other Enterobacteriaceae. We report the sequence of two novel SPI-7-like elements, found within strains of Salmonella bongori, which share 97% nucleotide identity over conserved regions with SPI-7 and with each other. Although SPI-7 within Salmonella enterica serovar Typhi appears to be fixed within the chromosome, we present evidence that these novel elements are capable of excision and self-mobility. Phylogenetic analyses show that these Salmonella mobile elements share an ancestor which existed approximately 3.6 to 15.8 million years ago. Additionally, we identified more distantly related ICEs, with distinct cargo regions, within other strains of Salmonella as well as within Citrobacter, Erwinia, Escherichia, Photorhabdus, and Yersinia species. In total, we report on a collection of 17 SPI-7 related ICEs within enterobacterial species, of which six are novel. Using comparative and mutational studies, we have defined a core of 27 genes essential for conjugation. We present a growing family of SPI-7-related ICEs whose mobility, abundance, and cargo variability indicate that these elements may have had a large impact on the evolution of the Enterobacteriaceae. Bacterial genomes are often represented as a core of conserved genes interspersed with accessory regions which are variably present throughout members of a species. The ability of an organism to sample variation through accessing a pan-genome can be strongly associated with a change in lifestyle or adaptation to a new niche (29). In some cases, acquired accessory functions become fixed and go on to define a particular lineage (30). A classical example of this is the acquisition of the Salmonella pathogenicity islands (SPIs), considered to have been fundamental to the evolution of the genus Salmonella (26). The largest of these islands identified to date is SPI-7, found within the genomes of Salmonella enterica subsp. enterica serovar Typhi (S. Typhi) (52), Salmonella enterica subsp. enterica serovar Paratyphi C (S. Paratyphi C) (43), and some strains of Salmonella enterica subsp. enterica serovar Dublin (S. Dublin) (55). SPI-7 is 120 kb in length and encodes important virulence functions, including the major virulence antigen (Vi) and type IVB pili (24, 52). Additionally, integrated within SPI-7 from strains of S. Typhi is a prophage harboring the type 3 secretion system effector protein-encoding gene sopE (47).SPI-7 possesses many similarities to integrative and conjugative elements (ICEs), a class of self-transmissible elements (7) also known as conjugativ...

Salmonella Pathogenicity and Host Adaptation in Chicken-Associated Serovars

“…ICEs appear to be major players in the horizontal transfer of genetic material between bacterial species, as they carry genes required for their own excision and transfer to recipient bacteria (113). This is exemplified in Salmonella by SPI-7, an ICE that is present in Salmonella but also among a variety of other Enterobacteriaceae (114). SPI-7 ICEs have been found in both S. enterica and S. bongori and in other bacterial species, and they appear to be evolutionarily related, suggesting that both inter-and intraspecies ICE transfer occurs and further enhances ICE diversity (115).…”

Genomic Dissection of Travel-Associated Extended-Spectrum-Beta-Lactamase-Producing Salmonella enterica Serovar Typhi Isolates Originating from the Philippines: a One-Off Occurrence or a Threat to Effective Treatment of Typhoid Fever?

“…The 144-kb deletion consists of various distinct regions, including the conjugal DNA transfer region, the type IVB pilus system, the DNA conjugational transfer region, and a partial sopE bacteriophage region (see Table S1D in the supplemental material). Deletions of different sizes of SPI-7 have previously been described (13)(14)(15)(16)(17) and related to plasmid-or chromosome-borne integrative and conjugative elements (ICEs) (17,18). ICEs, the conjugative system, allow the exchange of new genetic material by, e.g., horizontal gene transfer (18).…”

A New Member of the Growing Family of Contact-Dependent Growth Inhibition Systems in Xenorhabdus doucetiae

“…The cdi locus is shown in blue. The conserved genes of the ICE, as defined in a previous study [40], are highlighted in green. Notable cargo genes (e.g.…”