Specialized attachment structure of the fish pathogenic oomycete Saprolegnia parasitica

Abstract

The secondary cysts of the fish pathogen oomycete Saprolegnia parasitica possess bundles of long hooked hairs that are characteristic to this economically important pathogenic species. Few studies have been carried out on elucidating their specific role in the S. parasitica life cycle and the role they may have in the infection process. We show here their function by employing several strategies that focus on descriptive, developmental and predictive approaches. The strength of attachment of the secondary cysts of this pathogen was compared to other closely related species where bundles of long hooked hairs are absent. We found that the attachment of the S. parasitica cysts was around three times stronger than that of other species. The time sequence and influence of selected factors on morphology and the number of the bundles of long hooked hairs conducted by scanning electron microscopy study revealed that these are dynamic structures. They are deployed early after encystment, i.e., within 30 sec of zoospore encystment, and the length, but not the number, of the bundles steadily increased over the encystment period. We also observed that the number and length of the bundles was influenced by the type of substrate and encystment treatment applied, suggesting that these structures can adapt to different substrates (glass or fish scales) and can be modulated by different signals (i.e., protein media, 50 mM CaCl2 concentrations, carbon particles). Immunolocalization studies evidenced the presence of an adhesive extracellular matrix. The bioinformatic analyses of the S. parasitica secreted proteins showed that there is a high expression of genes encoding domains of putative proteins related to the attachment process and cell adhesion (fibronectin and thrombospondin) coinciding with the deployment stage of the bundles of long hooked hairs formation. This suggests that the bundles are structures that might contribute to the adhesion of the cysts to the host because they are composed of these adhesive proteins and/or by increasing the surface of attachment of this extracellular matrix.

Saprolegnia molecular phylogeny among farmed teleosts in Nova Scotia, Canada

“…The isolates pathogenic to fish appear to spend energy for asexual propagation, a successful tactic employed by S. parasitica to disseminate quickly through the water column to colonize new hosts (Lida et al, ; Sarowar et al, ). In addition, the pathogenic isolates of Clade I produce specialized “boat hooks” at the end of hair‐like threads ornamented on secondary cysts which may aid buoyancy in water column and increase the chance of attachment to swimming hosts (Rezinciuc et al, ). The pathogenicity of S. parasitica among fish is further enhanced by deception of host immune system to establish infection and, appressoria formation that are bulged thick‐walled hyphal tips at the point of entry on the host (Belmonte et al, ; Trusch et al, ; Willoughby & Hasenjäger, ).…”

“…(Lida et al, 2016;Sarowar et al, 2014). In addition, the pathogenic isolates of Clade I produce specialized "boat hooks" at the end of hair-like threads ornamented on secondary cysts which may aid buoyancy in water column and increase the chance of attachment to swimming hosts (Rezinciuc et al, 2018). The pathogenicity of F I G U R E 3 The summary of the phylogenetic tree of a Bayesian inference and maximum likelihood analyses based on 18S region of the nrDNA.…”

“…Among the several species of Saprolegnia, S. parasitica poses the greatest threat to fish and is now considered a specialized pathogen, and not a saprotroph (Hussein & Hatai, 2002;Sandoval-Sierra, Latif-Eugenin, et al, 2014;Sarowar et al, 2019). It produces special "boat hooks" on its secondary cysts to aid attachment to hosts (Rezinciuc, Sandoval-Sierra, Ruiz-León, van West, & Diéguez-Uribeondo, 2018), and the mycelia form "appressoria" to gain access through teleost skin/eggs to establish infection (Willoughby & Hasenjäger, 1987), and can suppress the host immune response by translocating specific proteins into host cells (Belmonte et al, 2014;Trusch et al, 2018;Wawra et al, 2012;van West et al, 2010). Within the genus Saprolegnia, other species (S. diclina, S. australis, S. delica and S. ferax) can also cause saprolegniosis in fish and eggs (Thoen, Evensen, & Skaar, 2011).…”

Genetic diversity and phenotypic characterization of Iodobacter limnosediminis associated with skin lesions in freshwater fish

“…was most frequently isolated from salmonid fish with saprolegniosis along with Aeromonas sp. (Carbajal-Gonzalez et al, 2011 et al, 2007;Rezinciuc et al, 2018). When attached, Saprolegnia sp.…”

Isolation, molecular identification, and pathological lesions of Saprolegnia spp. isolated from common carp, Cyprinus carpio in floating cages in Mosul, Iraq

“…S. parasitica is a fish pathogen with secondary cysts characterized by clusters of long-haired hook bundles. These hooks, along with adhesive extracellular matrix and proteins (fibronectin and thrombospondin), increase the strength of cyst attachment to hosts [ 14 ], and leading to damage the host epidermis cells and consequently causes tissue damage and dehydration as a result of the release of toxic materials and body fluids [ 9 ].…”