Whole genome sequencing reveals a novel Renibacterium salmoninarum lineage and suggests geographic endemism combined with anthropogenic spread in the North-East Atlantic area

Abstract

Renibacterium salmoninarum is the causative agent of bacterial kidney disease (BKD) and has been isolated from northern European salmonid farms since the 1960s. The bacterium has been detected only sporadically in Norway during the last decades, but the country experienced several geographically spread outbreaks since December 2022. The phylogenomic relationships of R. salmoninarum isolates associated with the epizootics ongoing on the West Coast and in Mid-Norway were explored using a whole genome sequencing approach. A broad overview of the phylogeography of this pathogen was gained through sequencing and analysis of a collection of isolates from Norway (n=67), Iceland (n=12), Denmark (n=12), and the Faroe Islands (n=1), along with a collection of 109 publicly available sequences. We identified two distinct contemporary clades of R. salmoninarum causing BKD in Norway in the period 2022-2024. Both clades belong to the expanding, aquaculture-associated Lineage 1. The epidemiological picture appears consistent with contemporary aquaculture operations, raising questions on the effectiveness or practice of current biosecurity practices towards R. salmoninarum. Our work also describes a hitherto undescribed lineage (Lineage 3), predominantly from Iceland, where BKD is considered endemic. The detection of endemic reservoirs of R. salmoninarum in European water systems underscores the potential for ongoing pathogen circulation independent of acute outbreaks. This finding emphasizes the importance of further investigation of the mechanisms of pathogen persistence, particularly within environments related to aquaculture, where chronic infection reservoirs could compromise disease management and biosecurity. IMPORTANCERenibacterium salmoninarum, the causative agent of bacterial kidney disease (BKD), is a chronic salmonid pathogen that often presents subclinically, complicating detection and control. Effective management of BKD is therefore crucial for sustainable aquaculture and wild fish conservation. Recognizing the need for comprehensive sampling, previous studies have underscored the importance of a global isolate collection to better understand the epidemiology of the pathogen. While the slow genetic evolution and highly conserved genome of the bacterium have reduced the resolution of conventional typing methods in the past, applying whole genome sequencing has enabled its molecular tracing at the outbreak level. Here, we present the largest phylogenomic analysis of R. salmoninarum to date, including sequences from Denmark, Iceland, and the Faroe Islands for the first time. This expanded dataset elucidates past and present movements of the pathogen in European waters, providing actionable insights to support development of targeted BKD management and biosecurity strategies.