Amoebic gill disease: a growing threat

The risk of disease outbreaks is predicted to increase due to climate change. For farmed fish an example is amoebic gill disease (AGD). While initially reported only in farmed salmonids in Washington State, USA, and Tasmania, Australia, it has now become an issue for Atlantic salmon farming worldwide and affects a range of other farmed marine fish species. Local high temperature anomalies and a lack of rainfall have been associated with the outbreaks of AGD. This worldwide presence is at least partly due to the cosmopolitan nature of the parasite and its low host-specificity. The disease can be treated using freshwater or hydrogen peroxide baths, but the treatments increase the cost of salmon production. Management of AGD contributes 20% to production costs of Atlantic salmon in Tasmania.

AGD, caused through infection of fish gills by the facultative parasite Neoparamoeba perurans, was first documented in sea-caged salmonids in 1985¹. Since its initial observation AGD has become a primary health concern globally for the marine salmonid industry, resulting in mortalities as great as 80% when left untreated². Clinical signs of AGD include respiratory distress, lethargy and inappetence, which are associated with grossly visible gill lesions³. Histologically, gill lesions are characterised by epithelial hyperplasia, interlamellar vesicles with associated amoebae and lamellar fusion⁴ (Figure 1).

Figure 1. Histological section showing two filaments from gills of infected Atlantic salmon, the top filament is affected and the bottom one is normal. Epithelial hyperplasia and lamellar fusion associated with presence of numerous amoebae can be seen in the top filament.

Because N. perurans was only recently identified⁵ and shown to cause AGD⁶, minimal information is available on its biology and ecology. Amoebae of the genus Neoparamoeba (Amoebozoa, Dactylopodida) are ubiquitous in the marine environment⁷, and N. perurans specifically have been detected throughout the water column on and near Atlantic salmon (Salmo salar L.) farms^8,9. All species from the genus Neoparamoeba harbour at least one intracellular endosymbiont known as a Perkinsela amoebae-like organism (PLO)¹⁰. The details of the symbiotic relationship between the PLOs and Neoparamoeba are unknown; however, the strict phylogenetic congruence of PLOs and their Neoparamoeba hosts suggests that PLOs are vertically transmitted from parent to daughter cells during mitotic division¹⁰. Species of Neoparamoeba all share the same general ultrastructural characteristics and cannot be differentiated morphologically¹¹.

Despite numerous studies investigating potential reservoirs of N. perurans, no significant reservoir outside farmed salmon has been identified⁹. Extensive surveys of the water column^8,12 and wild fish^13–15 have detected only minimal evidence of N. perurans. Studies of metazoan ectoparasites, for example copepods or isopods, on farmed salmon have detected low frequencies of N. perurans^16,17, but no evidence of a reservoir population. Additional studies using genus specific identification methods detected Neoparamoeba spp. in sediment samples¹⁸ and net biofouling¹⁹, but as yet no species specific testing has been conducted to detect N. perurans in these potential reservoirs.

Along with seemingly no reservoir, N. perurans is also an opportunistic parasite with no apparent host specificity. The pathogen has been detected not only in the commercially important Atlantic salmon²⁰, but also in a variety of farmed and non-farmed finfish species around the world⁹ (Figure 2). Presently AGD is a major issue for aquaculture in Tasmania, Ireland, Scotland, Norway and the United States with varying levels of impact from 10% to 82% mortality in some cases⁹. Additional outbreaks have been reported in Chile, France, Spain, South Africa, and most recently Canada and the Faroe Islands^9,21.

Figure 2. Map showing reported confirmed (PCR and/or ISH) cases of amoebic gill disease (AGD) in farmed Atlantic salmon.

Beyond salmon, N. perurans has been found on the gills of an additional 14 finfish species including ayu in Japan²², sea bass in the Mediterranean²³, and olive flounder in Korea²⁴. There is no traceable pattern from one of these outbreaks to another making it unlikely that it is a specific sub-population that causes the disease or that amoebae are transferred from one outbreak site to another. What is known of its lifecycle suggests an asexual clonal evolutionary pattern. It has been postulated by statistical analysis that the sheer number of individuals in any given microbial species is so large that dispersal would rarely be restricted by contrived geographical barriers²⁵, especially in marine environments⁷.

The cosmopolitan nature of N. perurans and lack of host specificity make discerning trends and risk factors for AGD challenging. A recent meta-analysis which considered all reports of AGD to date suggests locally high temperature anomalies, rather than absolute temperature, are related to disease outbreak⁹. Salinity also plays an important role in AGD. N. perurans is a marine amoeba with minimal tolerance for low salinity. Freshwater bathing for 2–4 hours is the most commonly utilised commercial treatment for AGD²⁶, and though many reports do not include information on rainfall, the few which have report lower than average rainfall preceding outbreaks^3,27–29. Given the predicted increase in ocean temperatures and altered rainfall patterns associated with climate change, there is concern that AGD associated costs will continue to increase for the salmonid industry moving forward³⁰.

Although research into AGD has come a long way in the past 30 years there are still many knowledge gaps in key areas from basic biology to industry research. For instance, little is known about the parasite N. perurans. The mechanisms behind the successful transfer of the PLO from mother to daughter cell, and benefits of the symbiosis, are not yet known. In addition there is little information on how the amoebae cause disease and whether there is potential for vaccines or drug targets. On a more practical side, extensive and thorough testing of sediment, biofouling and other potential reservoirs would also be beneficial for predicting outbreaks and controlling this globally increasing threat.