Dataset Information

A novel betaproteobacterial agent of gill epitheliocystis in seawater farmed Atlantic salmon (Salmo salar).

ABSTRACT: Epitheliocystis, a disease characterised by cytoplasmic bacterial inclusions (cysts) in the gill and less commonly skin epithelial cells, has been reported in many marine and freshwater fish species and may be associated with mortality. Previously, molecular and ultrastructural analyses have exclusively associated members of the Chlamydiae with such inclusions. Here we investigated a population of farmed Atlantic salmon from the west coast of Norway displaying gill epitheliocystis. Although 'Candidatus Piscichlamydia salmonis', previously reported to be present in such cysts, was detected by PCR in most of the gill samples analysed, this bacterium was found to be a rare member of the gill microbiota, and not associated with the observed cysts as demonstrated by fluorescence in situ hybridization assays. The application of a broad range 16 S rRNA targeted PCR assay instead identified a novel betaproteobacterium as an abundant member of the gill microbiota. Fluorescence in situ hybridization demonstrated that this bacterium, tentatively classified as 'Candidatus Branchiomonas cysticola', was the cyst-forming agent in these samples. While histology and ultrastructure of 'Ca. B. cysticola' cysts revealed forms similar to the reticulate and intermediate bodies described in earlier reports from salmon in seawater, no elementary bodies typical of the chlamydial developmental cycle were observed. In conclusion, this study identified a novel agent of epitheliocystis in sea-farmed Atlantic salmon and demonstrated that these cysts can be caused by bacteria phylogenetically distinct from the Chlamydiae.

SUBMITTER: Toenshoff ER

PROVIDER: S-EPMC3299688 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

A novel betaproteobacterial agent of gill epitheliocystis in seawater farmed Atlantic salmon (Salmo salar).

Toenshoff Elena R ER Kvellestad Agnar A Mitchell Susan O SO Steinum Terje T Falk Knut K Colquhoun Duncan J DJ Horn Matthias M

PloS one 20120312 3

Epitheliocystis, a disease characterised by cytoplasmic bacterial inclusions (cysts) in the gill and less commonly skin epithelial cells, has been reported in many marine and freshwater fish species and may be associated with mortality. Previously, molecular and ultrastructural analyses have exclusively associated members of the Chlamydiae with such inclusions. Here we investigated a population of farmed Atlantic salmon from the west coast of Norway displaying gill epitheliocystis. Although 'Can ...[more]

PMID: 22427865

Similar Datasets

Project description:To characterize intracellular gram-negative bacteria associated with epitheliocystis in farmed Atlantic salmon (Salmo salar), gills with proliferative lesions were collected for histopathology, conventional transmission and immunoelectron microscopy, in situ hybridization, and DNA extraction during epitheliocystis outbreaks in Ireland and Norway in 1999 and 2000, respectively, and compared by ultrastructure and immunoreactivity to nonproliferative gills from Ireland archived in 1995. Genomic DNA from proliferative gills was used to amplify 16S ribosomal DNA (rDNA) for molecular phylogenetic analyses. Epitheliocystis inclusions from proliferative gills possessed variably elongate reticulate bodies, examples of binary fission, and vacuolated and nonvacuolated intermediate bodies, whereas inclusions in nonproliferative gills had typical chlamydial developmental stages plus distinctive head-and-tail cells. Immunogold processing using anti-chlamydial lipopolysaccharide antibody labeled reticulate bodies from proliferative and nonproliferative gills. 16S rDNA amplified directly from Irish (1999) and Norwegian (2000) gill samples demonstrated 99% nucleotide identity, and riboprobes transcribed from cloned near-full-length 16S rDNA amplicons from Norwegian gills hybridized with inclusions in proliferative lesions from Irish (1999) and Norwegian (2000) sections. A 1,487-bp consensus 16S rRNA gene sequence representing the chlamydia-like bacterium (CLB) from proliferative gills had the highest percent nucleotide identity with endosymbionts of Acanthamoeba spp. (order Chlamydiales). Molecular phylogenetic relationships inferred from 16S rRNA gene sequences using distance and parsimony indicated that the CLB from proliferative gills branched with members of the order Chlamydiales. "Candidatus Piscichlamydia salmonis" is proposed for the CLB associated with epitheliocystis from proliferative gills of Atlantic salmon, which exhibits developmental stages different from those identified in nonproliferative gills.

Project description:Understanding the relationship between resident microbiota and disease in cultured fish represents an important and emerging area of study. Marine gill disorders in particular are considered an important challenge to Atlantic salmon (Salmo salar) aquaculture, however relatively little is known regarding the role resident gill microbiota might play in providing protection from or potentiating different gill diseases. Here, 16S rRNA sequencing was used to examine the gill microbiome alongside fish health screening in farmed Atlantic salmon. Results were used to explore the relationship between microbial communities and gill disease. Microbial community restructuring was observed throughout the sampling period and linked to varied drivers of change, including environmental conditions and severity of gill pathology. Taxa with significantly greater relative abundance on healthier gills included isolates within genus Shewanella, and taxa within family Procabacteriaceae. In contrast, altered abundance of Candidatus Branchiomonas and Rubritalea spp. were associated with damaged gills. Interestingly, more general changes in community richness and diversity were not associated with altered gill health, and thus not apparently deleterious to fish. Gross and histological gill scoring demonstrated seasonal shifts in gill pathology, with increased severity of gill damage in autumn. Specific infectious causes that contributed to observed pathology within the population included the gill disorder amoebic gill disease (AGD), however due to the uncontrolled nature of this study and likely mixed contribution of various causes of gill disease to observed pathology results do not strongly support an association between the microbial community and specific infectious or non-infectious drivers of gill pathology. Results suggest that the microbial community of farmed Atlantic salmon gills undergo continual restructuring in the marine environment, with mixed influences upon this change including environmental, host, and pathogenic factors. A significant association of specific taxa with different gill health states suggests these taxa might make meaningful indicators of gill health. Further research with more frequent sampling and deliberate manipulation of gills would provide important advancement of knowledge in this area. Overall, although much is still to be learnt regarding what constitutes a healthy or maladapted gill microbial community, the results of this study provide clear advancement of the field, providing new insight into the microbial community structure of gills during an annual production cycle of marine-stage farmed Atlantic salmon.

Project description:The gill of teleost fish is a multifunctional organ involved in many physiological processes such as gas exchange, osmotic and ionic regulation, acid-base balance and excretion of nitrogenous waste. Due to its extensive interface with the environment, the gill plays a key role as a primary mucosal defense tissue against pathogens, as manifested by the presence of the gill-associated lymphoid tissue (GIALT). In recent years, the prevalence of multifactorial gill pathologies has increased significantly, causing substantial losses in Atlantic salmon aquaculture. The transition from healthy to unhealthy gill phenotypes and the progression of multifactorial gill pathologies, such as proliferative gill disease (PGD), proliferative gill inflammation (PGI) and complex gill disorder (CGD), are commonly characterized by epithelial hyperplasia, lamellar fusion and inflammation. Routine monitoring for PGD relies on visual inspection and non-invasive scoring of the gill tissue (gross morphology), coupled with histopathological examination of gill sections. To explore the underlying molecular events that are associated with the progression of PGD, we sampled Atlantic salmon from three different marine production sites in Scotland and examined the gill tissue at three different levels of organization: gross morphology with the use of PGD scores (macroscopic examination), whole transcriptome (gene expression by RNA-seq) and histopathology (microscopic examination). Our results strongly suggested that the changes in PGD scores of the gill tissue were not associated with the changes in gene expression or histopathology. In contrast, integration of the gill RNA-seq data with the gill histopathology enabled us to identify common gene expression patterns associated with multifactorial gill disease, independently from the origin of samples. We demonstrated that the gene expression patterns associated with multifactorial gill disease were dominated by two processes: a range of immune responses driven by pro-inflammatory cytokines and the events associated with tissue damage and repair, driven by caspases and angiogenin.

Dataset Information

A novel betaproteobacterial agent of gill epitheliocystis in seawater farmed Atlantic salmon (Salmo salar).

Publications

A novel betaproteobacterial agent of gill epitheliocystis in seawater farmed Atlantic salmon (Salmo salar).

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets