Bridging clinical and environmental reservoirs: antimicrobial resistance in the emerging pathogen Shewanella algae

Abstract

The emergence of antimicrobial resistance in environmental bacteriathreatens therapeutic efficacy in clinical settings. Shewanella algae, historically regarded as a marine saprophyte, is increasingly recognized as an emerging opportunisticpathogen. In this study, we analyzed 86 S. algae isolates from Spain (19 clinical and 67environmental) and integrated them with 178 publicly available genomes to exploreantimicrobial susceptibility patterns and genomic diversity. Penicillins and fosfomycinconsistently showed poor activity, whereas piperacillin/tazobactam, third- and fourth-generation cephalosporins, aminoglycosides, ciprofloxacin, trimethoprim–sulfamethoxazole and several novel β-lactam–inhibitor combinations exhibited low MIC distributions.Recently introduced agents, including ceftazidime/avibactam, ceftolozane/tazobactam,and cefiderocol, also demonstrated strong in vitro activity. Carbapenems displayedan unusual intraclass pattern, with imipenem showing markedly higher MICs thanmeropenem and ertapenem. When interpreted using CLSI’s “Other Non-Enterobacterales” criteria, clinical and environmental isolates exhibited largely overlapping susceptibility profiles, highlighting the potential role of environmental strains as reservoirsof resistance-related traits. Genomic profiling revealed a conserved intrinsic resistome(OXA-type β-lactamases, qnrA variants, ugd, and efflux regulators) together withhorizontally acquired determinants. A 29 kb genomic island carrying multiple resistance genes was identified in a clinical isolate, with homologous structures detectedin Vibrio and Proteus, suggesting interspecies transfer. Furthermore, plasmids harboringclass 1 integrons (mobile integrons) were widespread, shared with Enterobacterales andVibrionaceae across clinical and environmental settings. Overall, these findings highlightS. algae as both a clinically relevant pathogen and a reservoir of mobile AMR determinants and underscore the urgent need for species-specific antimicrobial susceptibilityinterpretive criteria to improve clinical decision-making for this emerging pathogen.