Convergence of virulence and resistance in international clones of WHO critical priority enterobacterales isolated from Marine Bivalves

Abstract

The global spread of critical-priority antimicrobial-resistant Enterobacterales by food is a public health problem. Wild-caught seafood are broadly consumed worldwide, but exposure to land-based pollution can favor their contamination by clinically relevant antimicrobial-resistant bacteria. As part of the Grand Challenges Explorations: New Approaches to Characterize the Global Burden of Antimicrobial Resistance Program, we performed genomic surveillance and cell culture-based virulence investigation of WHO critical priority Enterobacterales isolated from marine bivalves collected in the Atlantic Coast of South America. Broad-spectrum cephalosporin-resistant Klebsiella pneumoniae and Escherichia coli isolates were recovered from eight distinct geographical locations. These strains harbored blaCTX-M-type or blaCMY-type genes. Most of the surveyed genomes confirmed the convergence of wide virulome and resistome (i.e., antimicrobials, heavy metals, biocides, and pesticides resistance). We identified strains belonging to the international high-risk clones K. pneumoniae ST307 and E. coli ST131 carrying important virulence genes, whereas in vitro experiments confirmed the high virulence potential of these strains. Thermolabile and thermostable toxins were identified in some strains, and all of them were biofilm producers. These data point to an alarming presence of resistance and virulence genes in marine environments, which may favor horizontal gene transfer and the spread of these traits to other bacterial species.

Co‐localization of clinically relevant antibiotic‐ and heavy metal resistance genes on plasmids in Klebsiella pneumoniae from marine bivalves

“…pneumoniae isolated from marine bivalves in Brazil, consistent with our results for K. pneumoniae (Bueris et al, 2022;Citterio et al, 2020).…”

Emergence and Dissemination of Extraintestinal Pathogenic High-Risk International Clones of Escherichia coli

“…Furthermore, in countries such as Canada, the USA, Korea, Kuwait, Lebanon, France, Switzerland, Portugal, Spain, Germany, Bangladesh, China, and Japan, many lineages (e.g., ST131) circulate with quite similar resistance patterns [8] (Table 2). Globally, the predominant ExPEC clone is ST131, which is clustered into clades and subclades [15,37,39,[45][46][47]. It possesses a wide variety of beta-lactamases, with the most frequent including ESBLs (bla CTX-M-14,15,27 ), AmpCs (bla FOX−5 , bla DHA-1 ), MBLs, and carbapenemases (bla NDM-1,5; bla VIM-1 , bla KPC-2,-3,-18; bla OXA-48,-181,-232 ).…”

“…The vast majority of strains in this clone are resistant to several antibiotic groups, namely beta-lactams, aminoglycosides, tetracycline, fluoroquinolones, sulfonamides, chloramphenicol and nitrofurantoin [43,44]. Moreover, in the last 15 years, this clone became the predominant high-risk international clone among ExPEC clinical isolates, as 133 of 169 collected studies have reported its presence from various clinical samples between 1995 and 2018 [15,37,39,[45][46][47].…”

“…Based on the 'One Health' approach, zoonotic risk, as a novel aspect of MDR CC131 global distribution, has been also suggested. As a common feature, many rapid outbreaks of high-risk international MDR bacteria have originated from the human-animal interface [47]. Due to the similar and overlapping molecular regions between avian pathogenic E. coli and ExPEC, it has previously been hypothesised that avian E. coli may act like a reservoir of virulence and resistance markers.…”

“…Furthermore, production of thermostable toxin has also been reported among these strains, so a great deal of attention should be paid to seafood as a source of diseases induced by high-risk toxin producer MDR bacterial clones. The whole-genome sequence of this ST131 strain was deposited in GenBank under the accession number NCVZ00000000.1 [47] (Table 1). Furthermore, houseflies have been hypothesised to be vectors of many MDR bacteria, including Pseudomonas aeruginosa, Acinetobacter baumannii, Citrobacter freundii, Enterobacter cloacae, Klebsiella oxytoca and ExPEC clones, such as CC131, in a tertiary hospital in Rwanda, Africa.…”