Multidrug Resistance Salmonella Genomic Island 1 in a Morganella morganii subsp. morganii Human Clinical Isolate from France

Abstract

Salmonella genomic island 1 (SGI1) is a multidrug resistance integrative mobilizable element that harbors a great diversity of antimicrobial resistance gene clusters described in numerous Salmonella enterica serovars and also in Proteus mirabilis. A serious threat to public health was revealed in the recent description in P. mirabilis of a SGI1-derivative multidrug resistance island named PGI1 (Proteus genomic island 1) carrying extended-spectrum-β-lactamase (ESBL) and metallo-β-lactamase resistance genes, bla_VEB-6 and bla_NDM-1, respectively. Here, we report the first description of Salmonella genomic island 1 (SGI1) in a multidrug-resistant clinical Morganella morganii subsp. morganii strain isolated from a patient in France in 2013. Complete-genome sequencing of the strain revealed SGI1 variant SGI1-L carrying resistance genes dfrA15, floR, tetA(G), bla_PSE-1 (now referred to as bla_CARB-2), and sul1, conferring resistance to trimethoprim, phenicols, tetracyclines, amoxicillin, and sulfonamides, respectively. The SGI1-L variant was integrated into the usual chromosome-specific integration site at the 3' end of the trmE gene. Beyond Salmonella enterica and Proteus mirabilis, the SGI1 integrative mobilizable element may thus also disseminate its multidrug resistance phenotype in another genus belonging to the Proteae tribe of the family Enterobacteriaceae. IMPORTANCE Since its initial identification in epidemic multidrug-resistant Salmonella enterica serovar Typhimurium DT104 strains, several SGI1 variants, SGI1 lineages, and SGI1-related elements (SGI2, PGI1, and AGI1) have been described in many bacterial genera (Salmonella, Proteus, Morganella, Vibrio, Shewanella, etc.). They constitute a family of multidrug resistance site-specific integrative elements acquired by horizontal gene transfer, SGI1 being the best-characterized element. The horizontal transfer of SGI1/PGI1 elements into other genera is of public health concern, notably with regard to the spread of critically important resistance genes such as ESBL and carbapenemase genes. The identification of SGI1 in Morganella morganii raises the issue of (i) the potential for SGI1 to emerge in other human pathogens and (ii) its bacterial host range. Further surveillance and research are needed to understand the epidemiology, the spread, and the importance of the members of this SGI1 family of integrative elements in contributing to antibiotic resistance development.

Keywords: Salmonella genomic island 1; integrative mobilizable element; integrons; multidrug resistance.

FIG 1

Schematic view of SGI1-L and its specific features encountered in Morganella morganii strain LIM90. The gray arrow corresponds to chromosomal gene trmE into which SGI1 is integrated into the last 18 bp. DR-L and DR-R are the 18-bp left and right direct repeats, respectively, bracketing SGI1. The insertion points of complex class 1 integron InSGI1-L between the res gene and ORF S044 of the SGI1 backbone and the 5-bp target site duplication are indicated. IRi and IRt are 25-bp imperfect inverted repeats defining the left and right end of the complex class 1 integron. Black arrows correspond to SGI1 antibiotic resistance genes. IS elements are indicated by boxes containing black hatched arrows representing the transposase genes. Base pair coordinates are from the complete SGI1-L sequence of M. morganii strain LIM90 (ENA accession no. LT630458).