Microbial and pathological findings in farmed Atlantic salmon Salmo salar with proliferative gill inflammation

Abstract

Proliferative gill inflammation (PGI) is an important cause of loss in seawater-farmed Atlantic salmon in Norway. Several microbes have been associated with PGI, including the commonly but not exclusively observed inclusions (epitheliocysts) within the gill lamellae related to infection with 'Candidatus Piscichlamydia salmonis'. Atlantic salmon transferred in the spring of 2004 to 12 seawater farms situated in mid-and southwest Norway were sampled throughout that year. Outbreaks of PGI, as evaluated by clinical examination, histology, and mortality data, were diagnosed in 6 of 7 farms in southwest Norway but not in the 5 farms studied in mid-Norway. Generally, mortality started 3 to 5 mo after seawater transfer and outbreaks lasted at least 1 to 3 mo. 'Ca. P. salmonis' was detected by real-time PCR only in fish from PGI-affected farms and our results indicate an association between 'Ca. P. salmonis' load and PGI severity. Likewise, although widely distributed in all 12 farms studied, epitheliocyst prevalence and number per fish as observed by histology appears associated with PGI prevalence and severity. However, the occurrence of epitheliocysts showed no association with molecular detection of 'Ca. P. salmonis', suggesting that at least 1 other organism is responsible for many of the observed inclusions. A microsporidian, Desmozoon lepeophtherii, was identified at high prevalence regardless of fish and farm PGI status, but at higher loads in fish with PGI. Our results support a multifactorial etiology for PGI in which 'Ca. P. salmonis', an unidentified epitheliocyst agent, and the microsporidian are contributing causes. No evidence for the involvement of Atlantic salmon paramyxovirus in PGI development was identified in the present study. High water temperatures and ectoparasites probably exacerbated mortality. KEY WORDS: Proliferative gill inflammation · Epitheliocysts · 'Candidatus Piscichlamydia salmonis' · Desmozoon lepeophtherii · 'Candidatus Clavochlamydia salmonicola' · Atlantic salmon paramyxovirusResale or republication not permitted without written consent of the publisher Dis Aquat Org 91: 201-211, 2010 to months (Kvellestad et al. 2004, Skjelstad et al. 2007. Mortality varies and losses of 15 to 20% or higher have been reported (Flesjå et al. 2004, Kvellestad et al. 2004. Estimation of economic losses is difficult, but one of the largest farming companies in Norway considered PGI to be the disease responsible for most losses in terms of both numbers of fish and biomass in 2007(Skjelstad et al. 2007). Gill disorders were also the most important cause of losses in Ireland in 2005(Rodger 2007. Previous studies have indicated a multifactorial etiology behind PGI, following identification of various microorganisms occurring alone or in combination with others, including Atlantic salmon paramyxovirus (ASPV) (Kvellestad et al. 2003(Kvellestad et al. , 2005, salmon gill poxvirus , various ectoparasites (Kvellestad et al. 2005), as well as lamellar bacterial inclusions (epitheliocystis) (Nylund ...

A novel agent (Endozoicomonas elysicola) responsible for epitheliocystis in cobia Rachycentrum canadum larvae

“…More recently, Toenshoff et al (2012) have shown that a newly identified Betaproteobacteria, tentatively called 'Candidatus Branchiomonas cysticola', caused epitheliocystis in Atlantic salmon Salmo salar, and they proposed that bacteria from different evolutionary branches may cause epitheliocystis. A similar multifactorial hypothesis for epitheliocystis was also proposed by Steinum et al (2010), who identified a microsporidian, Desmozoon lepeophtherii, present at high loads in Atlantic salmon with proliferative gill inflammation (PGI), suggesting that 'Candidatus Piscichlamydia salmonis' and the microsporidian could be contributing causes of epitheliocystis.…”

“…More recently, Toenshoff et al (2012) have shown that a newly identified Betaproteobacteria, tentatively called 'Candidatus Branchiomonas cysticola', caused epitheliocystis in Atlantic salmon Salmo salar, and they proposed that bacteria from different evolutionary branches may cause epitheliocystis. A similar multifactorial hypothesis for epitheliocystis was also proposed by Steinum et al (2010), who identified a microsporidian, Desmozoon lepeophtherii, present at high loads in Atlantic salmon with proliferative gill inflammation (PGI), suggesting that 'Candidatus Piscichlamydia salmonis' and the microsporidian could be contributing causes of epitheliocystis.In the present study, sequencing of 16S rRNA genes from the lesions of moribund larvae, and BLAST analysis against the RDB and NCBI databases, showed a 99% similarity with Endozoicomonas elysicola strain MKT110 GenBank accession number NR_041264. This organism was first isolated from the sea slug Elysia ornata collected in Japan in 2007 (Kurahashi & Yokota 2007 (Yi et al 2003).…”

Paranucleospora theridion (Microsporidia) infection dynamics in farmed Atlantic salmon Salmo salar put to sea in spring and autumn

“…It is interesting that gill inflammation with phagocytosis of the autoinfective spores may be important for the spread of the parasite from the gills to the kidney and other tissues. Paranucleospora theridion infections have been found to be closely associated with PGI (Steinum et al 2010, S. Nylund et al 2011.…”

“…Heavy P. theridion densities in Paranucleospora theridion (Microsporidia) infection dynamics in farmed Atlantic salmon Salmo salar put to sea in spring and autumn salmon are often associated with other diseases and diagnoses, and the parasite has been suspected of predisposing the host to other infectious agents and of being responsible for some of the pathology attributed to some viral diseases (S. Nylund et al 2011). An association has been shown between P. theridion infection levels and the unspecific diagnosis 'proliferative gill inflammation' (PGI) in salmon (Steinum et al 2010, S. Nylund et al 2011). …”

Evaluation of Non-destructive Molecular Diagnostics for the Detection of Neoparamoeba perurans

“…This method is particularly suitable on Atlantic salmon farms that are constantly affected by the disease, allowing operators to become familiar with the gross presentation of lesions. However, the gross gill score can be difficult to interpret when non-AGD pathologies, such as proliferative gill disease or gill necrosis are present (Steinum et al, 2010;Mitchell and Rodger, 2011). It is also reported that the gross gill scoring method is less applicable for other fish species affected by AGD, such as lumpfish (Cyclopterus lumpus) which are used as cleaner fish in Atlantic salmon cages (Haugland et al, in press).…”