Shewanella spp. are Gram-negative rods widely disseminated in aquatic niches that can also be found in human-associated environments. In recent years, reports of infections caused by these bacteria have increased significantly. Mobilome and resistome analysis of a few species showed that they are versatile; however, comprehensive comparative studies in the genus are lacking. Here, we analyzed the genetic traits of 144 genomes from Shewanella spp. isolates focusing on the mobilome, resistome, and virulome to establish their evolutionary relationship and detect unique features based on their genome content and habitat. Shewanella spp. showed a great diversity of mobile genetic elements (MGEs), most of them associated with monophyletic lineages of clinical isolates. Furthermore, 79/144 genomes encoded at least one antimicrobial resistant gene with their highest occurrence in clinical-related lineages. CRISPR-Cas systems, which confer immunity against MGEs, were found in 41 genomes being I-E and I-F the more frequent ones. Virulome analysis showed that all Shewanella spp. encoded different virulence genes (motility, quorum sensing, biofilm, adherence, etc.) that may confer adaptive advantages for survival against hosts. Our data revealed that key accessory genes are frequently found in two major clinical-related groups, which encompass the opportunistic pathogens Shewanella algae and Shewanella xiamenensis together with several other species. This work highlights the evolutionary nature of Shewanella spp. genomes, capable of acquiring different key genetic traits that contribute to their adaptation to different niches and facilitate the emergence of more resistant and virulent isolates that impact directly on human and animal health.

Shewanella spp. are Gram-negative bacteria that thrive in aquatic niches and also can cause infectious diseases as opportunistic pathogens. Chromosomal (CI) and mobile integrons (MI) were previously described in some Shewanella isolates. Here, we evaluated the occurrence of integrase genes, the integron systems and their genetic surroundings in the genus. We identified 22 integrase gene types, 17 of which were newly described, showing traits of multiple events of lateral genetic transfer (LGT). Phylogenetic analysis showed that most of them were strain-specific, except for Shewanella algae, where SonIntIA-like may have co-evolved within the host as typical CIs. It is noteworthy that co-existence of up to five different integrase genes within a strain, as well as their wide dissemination to Alteromonadales, Vibrionales, Chromatiales, Oceanospirillales and Enterobacterales was observed. In addition, identification of two novel MIs suggests that continuous LGT events may have occurred resembling the behavior of class 1 integrons. The constant emergence of determinants associated to antimicrobial resistance worldwide, concomitantly with novel MIs in strains capable to harbor several types of integrons, may be an alarming threat for the recruitment of novel antimicrobial resistance gene cassettes in the genus Shewanella, with its consequent contribution towards multidrug resistance in clinical isolates.

Shewanella spp. are gram-negative bacteria that thrive in aquatic niches and also cause infectious diseases as opportunistic pathogens. Chromosomal integrons (CI) and mobile integrons (MI) were previously described in some Shewanella isolates. Here, we evaluated the occurrence of integrase genes, the integron systems and their genetic surroundings in the genus. We identified 22 integrase gene types, 17 of which were newly described, in different Shewanella species, evidencing multiple gain and loss events. Phylogenetic analysis showed that most of them were strain-specific, except for Shewanella algae, which seem to have co-evolve within the host as typical CIs. Noteworthy, co-existence of up to 5 different integrase genes, as well as their wide dissemination to Alteromonadales, Vibronales, Chromatiales, Oceanospirillales and Enterobacterales was observed. Identification of novel MIs suggests that lateral genetic transfer may have occurred resembling the behavior of class 1 integrons. The constant emergence of determinants associated to antimicrobial resistance worldwide, concomitantly with novel MIs in strains capable to harbor several types of integrons may be an alarming threat for the recruitment of novel antimicrobial resistance gene cassettes in the genus Shewanella, and its evolution towards the multidrug resistance.