Abstract
Salmonella genomic island 1 (SGI1) is a resistance-conferring chromosomal genomic island that contains an antibiotic resistance gene cluster. The international spread of SGI1-containing strains drew attention to the role of genomic islands in the dissemination of antibiotic resistance genes in Salmonella and other Gram-negative bacteria. In this study, five SGI1 variants conferring multidrug and heavy metal resistance were identified and characterized in Proteus mirabilis strains: SGI1-PmCAU, SGI1-PmABB, SGI1-PmJN16, SGI1-PmJN40, and SGI1-PmJN48. The genetic structures of SGI1-PmCAU and SGI1-PmABB were identical to previously reported SGI1s, while structural analysis showed that SGI1-PmJN16, SGI1-PmJN40, and SGI1-PmJN48 are new SGI1 variants. SGI1-PmJN16 is derived from SGI1-Z with the MDR region containing a new gene cassette array dfrA12-orfF-aadA2-qacEΔ1-sul1-chrA-orf1. SGI1-PmJN40 has an unprecedented structure that contains two right direct repeat sequences separated by a transcriptional regulator-rich DNA fragment, and is predicted to form two different extrachromosomal mobilizable DNA circles for dissemination. SGI1-PmJN48 lacks a common ORF S044, and its right junction region exhibits a unique genetic organization due to the reverse integration of a P. mirabilis chromosomal gene cluster and the insertion of part of a P. mirabilis plasmid, making it the largest known SGI1 to date (189.1 kb). Further mobility functional analysis suggested that these SGIs can be excised from the chromosome for transfer between bacteria, which promotes the horizontal transfer of antibiotic and heavy metal resistance genes. The identification and characterization of the new SGI1 variants in this work suggested the diversity of SGI1 structures and their significant roles in the evolution of bacteria.
Highlights
Salmonella genomic island 1 (SGI1) is a genomic island containing an antibiotic resistance gene cluster initially identified in Salmonella enterica serovar Typhimurium phage type DT104 strain (Boyd et al, 2001)
The right junction regions of these two SGI1s were further analyzed by PCR with primer pairs 104-RJ/hipA-R1 and 104-RJ/MPR1 that respectively, target the two genes downstream of hipB on the chromosome of P. mirabilis HI4320 (Siebor and Neuwirth, 2013)
Five SGI1s were identified and characterized in multidrug resistant P. mirabilis strains, and different antibiotic and heavy metal resistant gene clusters were identified in their multidrug resistance (MDR) regions, suggesting their roles in the conferment and dissemination of resistance
Summary
Salmonella genomic island 1 (SGI1) is a genomic island containing an antibiotic resistance gene cluster initially identified in Salmonella enterica serovar Typhimurium phage type DT104 strain (Boyd et al, 2001). Three SGI1-related elements, SGI2, Proteus genomic island (PGI1/PGI2) and Acinetobacter genomic island 1 (AGI1), were reported in S. enterica, P. mirabilis and Acinetobacter baumannii, respectively (Levings et al, 2008; Siebor and Neuwirth, 2014; Hamidian et al, 2015; Lei et al, 2018) All these four genomic islands integrate into the 3 -end of chromosomal trmE gene and carry diverse antibiotic resistance genes in their MDR regions (Hall, 2010; Hamidian et al, 2015; Lei et al, 2018). The emergence of these strains carrying SGI1/PGI1 with ESBL gene and/or carbapenemase gene is of great concern to public health, as β-lactams and carbapenems remain the most widely used antibiotics for the treatment of bacterial infection
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