Illumination of anguillid herpesvirus 1 transmission in European eels reveals the importance of host developmental stage and agonistic social interactions

ABSTRACT The European eel has a complex life cycle involving various developmental stages and migrations through marine and freshwater environments. It is critically endangered and therefore a flagship species for conservation efforts. The European eel is also an important fish species in aquaculture. One of the major pathogens contributing to the decline of the European eel is thought to be anguillid herpesvirus 1 (AngHV-1). In this study, we used in vivo bioluminescent imaging to study the ability of AngHV-1 to infect the various developmental stages of the European eel, and to investigate virus transmission between eels. Our results highlight that eels become sensitive to AngHV-1 infection only when they become yellow eels (a freshwater stage prior to maturity), with the gills and the periodontal mucosa acting as the first sites of replication after inoculation by immersion in virus-containing water. Also, multifocal cutaneous bioluminescent signals appeared in grouped eels, but not in isolated eels. These observations suggested that the virus might be transmitted through biting between fish. In support of this hypothesis, experiments based on single artificial bites occurring between infected eels and naïve eels led to the infection of all exposed subjects. The biological relevance of AngHV-1 transmission by biting was further supported by observation of the instability of virion infectivity in water and fish mucus. Our study thus challenges the current paradigm that fish viruses are transmitted mainly via water acting as an abiotic vector. It demonstrates that, as in air, so in water, social interactions matter. IMPORTANCE Fish viruses have devastating effects on wildlife and severe economic impact on aquaculture. The current paradigm is that they are transmitted via water acting as an abiotic vector. Here, we used in vivo bioluminescent imaging to study the ability of anguillid herpesvirus 1 (AngHV-1) to infect different developmental stages of European eel and to investigate virus transmission between eels. The major findings were that (i) eels become sensitive to AngHV-1 infection only when they become yellow eels, with the gills and the periodontal mucosa acting as the first sites of replication after inoculation by immersion in virus-containing water; (ii) AngHV-1 is efficiently transmitted between fish through biting, thereby avoiding virion instability in water and mucus. Our study thus challenges the current paradigm that fish viruses are transmitted mainly via water acting as an abiotic and protective vector. It demonstrates that, as in air, so in water, social interactions matter.