Comparative genome analysis of the genus Shewanella unravels the association of key genetic traits with known and potential pathogenic lineages

Gabriela N Cerbino; German M Traglia; Teolincacihuatl Ayala Nuñez; Gisela Parmeciano Di Noto; María Soledad Ramírez; Daniela Centrón; Andrés Iriarte; Cecilia Quiroga

doi:10.3389/fmicb.2023.1124225

Comparative genome analysis of the genus Shewanella unravels the association of key genetic traits with known and potential pathogenic lineages

Front Microbiol. 2023 Feb 28:14:1124225. doi: 10.3389/fmicb.2023.1124225. eCollection 2023.

Authors

Gabriela N Cerbino¹, German M Traglia², Teolincacihuatl Ayala Nuñez¹, Gisela Parmeciano Di Noto¹, María Soledad Ramírez³, Daniela Centrón¹, Andrés Iriarte², Cecilia Quiroga¹

Affiliations

¹ Universidad de Buenos Aires, Consejo Nacional de Investigaciones Científicas y Tecnológicas, Instituto de Investigaciones en Microbiología y Parasitología Médica (IMPAM), Facultad de Medicina, Buenos Aires, Argentina.
² Laboratorio de Biología Computacional, Departamento de Desarrollo Biotecnológico, Instituto de Higiene, Facultad de Medicina, Universidad de la República, Montevideo, Uruguay.
³ Center for Applied Biotechnology Studies, Department of Biological Science, California State University, Fullerton, Fullerton, CA, United States.

Abstract

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.

Keywords: Shewanella; accessory genome; horizontal gene transfer; mobilome; resistome; virulome.

Grants and funding

GC was a member of the CPA from the National Scientific and Technical Research Council (CONICET). TA was the recipient of a scholarship from CONICET. CQ and DC were members of the CIC from CONICET. AI was a member of the SNI, Uruguay. This work was supported by grant ANPCyT 2018-03222 from the Ministry of Science, Technology and Innovation of Argentina.