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

Abstract

The emergence of antimicrobial resistance in environmental bacteria threatens therapeutic efficacy in clinical settings. Shewanella algae, historically regarded as a marine saprophyte, is increasingly recognized as an emerging opportunistic pathogen. In this study, we analyzed 86 S. algae isolates from Spain (19 clinical and 67 environmental) and integrated them with 178 publicly available genomes to explore antimicrobial susceptibility patterns and genomic diversity. Penicillins and fosfomycin consistently 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 displayed an unusual intraclass pattern, with imipenem showing markedly higher MICs than meropenem 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 reservoirs of resistance-related traits. Genomic profiling revealed a conserved intrinsic resistome (OXA-type β-lactamases, qnrA variants, ugd, and efflux regulators) together with horizontally acquired determinants. A 29 kb genomic island carrying multiple resistance genes was identified in a clinical isolate, with homologous structures detected in Vibrio and Proteus, suggesting interspecies transfer. Furthermore, plasmids harboring class 1 integrons (mobile integrons) were widespread, shared with Enterobacterales and Vibrionaceae across clinical and environmental settings. Overall, these findings highlight S. algae as both a clinically relevant pathogen and a reservoir of mobile AMR determinants and underscore the urgent need for species-specific antimicrobial susceptibility interpretive criteria to improve clinical decision-making for this emerging pathogen.