Enterospora nucleophila

Last updated

Contents

Enterospora nucleophila
Enterospora nucleophila.tif
Transmission electron micrograph of an Enterospora nucleophila-infected rodlet cell harbouring spores within its nucleus (N). No stages are visible in the cytoplasm (C)
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Phylum: Microsporidia
Class: incertae sedis
Genus: Enterospora
Species:
E. nucleophila
Binomial name
Enterospora nucleophila
Palenzuela, Redondo, Cali, Takvorian, Alonso-Naveiro, Alvarez-Pellitero & Sitjà-Bobadilla, 2014

Enterospora nucleophila is a microsporidian infecting the gilt-head bream (Sparus aurata). It develops primarily within the nuclei of rodlet cells and enterocytes, at the intestinal epithelium. It can also be found in cytoplasmic position within other cell types, including phagocytes, at subepithelial layers. It is the causative agent of emaciative microsporidiosis of gilthead sea bream, a chronic condition manifested as a severe growth arrestment, normally accompanied by trickling mortality.

Taxonomy

E. nucleophila is a microsporidian, a group of intracellular parasites related to fungi. This species is rooted within the family Enterocytozoonidae. According to SSUrDNA-based phylogenetic inference, it clusters with Enterocytozoon hepatopenaei , Enterospora canceri and Enterocytozoon bieneusi in a well-supported clade. [1] The Enterocytozoonidae branches within the class Terresporidia in molecular-based classification of microsporidians [2] but taxonomical classification above the family level is currently not entirely settled in this phylum.

Life cycle

Only the development within gilthead sea bream is currently known. [1] Since some of the closest relatives of E. nucleophila infect crustaceans (e.g., Enterospora canceri or E. hepatopenaei), and some of them have heteroxenous cycles alternating between crustacean and fish hosts (e.g., Desmozoon lepeophtheri [3][ citation needed ]), a similar alternating cycle could occur for E. nucleophila.

Pathology and clinical signs

Infections by E. nucleophila are associated with stunted growth of gilthead sea bream stocks, which can be accompanied by low-level but sustained trickling mortality (0.1-0.3% daily, up to 1% at peaks per sea cage). [1] Affected fish normally appear lethargic and cachectic, with other nonspecific signs like discolouration and occasional scale loss. [1] Upon necropsy, gross pathological alterations include thinned and transparent wall in the intestines, which frequently accumulate clear or greenish fluid and white faeces in the terminal portion. The condition seems to appear in gilthead sea bream during their first winter in sea cages. As a result of the arrested growth of infected animals, these can average half the weight of the unaffected stock. [3]

Impact

The disease was first noticed in the early 2000s. However, the difficulties in the diagnosis of the parasite probably delayed acknowledgement of its presence and impact. Indeed, the parasite and its association with gilthead sea bream emaciative microsporidiosis were not described until recently, but retrospective studies identified it in samples taken in 1993. [1] The main clinical signs are only noticed in severe infections and can be largely masked by other infectious diseases of gilthead sea bream. Therefore, the approaches to understand the true impact of the disease can only be formed after the development of appropriate diagnostic methods to conduct specific epidemiological and risk-assessment studies. Besides the mortality, the main economic impact of the parasite is related to the segregation of sizes caused by the infection within affected sea cages, as it results in inefficient feeding, serious biomass and quality losses at the harvest.

Diagnosis

Presumptive diagnosis can be made based on clinical signs and histopathological examination of the intestinal epithelium. The most common observation in heavy infections is the presence of numerous hypertrophied cell nuclei and a remarkable hypercellularity. [1] When present, tiny microsporidian spores (1.67 x 1.05 µm) can be identified. Like in other microsporidioses, the detection of spores can be facilitated with calcofluor-white M2R or luna stains. [4] More reliable confirmatory diagnosis of E. nucleophila is possible with molecular-based methods, in situ hybridization [5] and RT-PCR tests. [6]

Treatments

There are currently no approved therapies for E. nucleophila. Microsporidian infections relevant for human and animal medicine are normally treated with Albendazole, Metronidazole or Fumagillin, but the use of these drugs in aquaculture settings is not regulated and their effectivity for treating gilthead sea bream microsporidiosis is unknown.

Research

As an emerging disease of gilthead sea bream, understanding E. nucleophila infection and exploring ways to mitigate its impact in aquaculture facilities has just started. The EU funded Horizon 2020 Project [7] has tackled several objectives related to this infection, like the development and validation of diagnostic methods and their use in epidemiological studies to evaluate the impact and risks factors associated to the disease. Ongoing research framed within the project has also focused on developing means for the transmission and maintenance of the infection in the laboratory, as well as its in vitro cultivation. More ambitious goals, such as the genome sequencing and the identification of therapeutic and diagnostic targets have also been attempted but are currently struggling with difficulties in reproducing the disease in the laboratory and generating appropriate material.

Related Research Articles

Nosema apis is a microsporidian, a small, unicellular parasite recently reclassified as a fungus that mainly affects honey bees. It causes nosemosis, also called nosema, which is the most common and widespread of adult honey bee diseases. The dormant stage of N. apis is a long-lived spore which is resistant to temperature extremes and dehydration, and cannot be killed by freezing the contaminated comb. Nosemosis is a listed disease with the Office International des Epizooties (OIE).

<span class="mw-page-title-main">Microsporidia</span> Phylum of fungi

Microsporidia are a group of spore-forming unicellular parasites. These spores contain an extrusion apparatus that has a coiled polar tube ending in an anchoring disc at the apical part of the spore. They were once considered protozoans or protists, but are now known to be fungi, or a sister group to fungi. These fungal microbes are obligate eukaryotic parasites that use a unique mechanism to infect host cells. They have recently been discovered in a 2017 Cornell study to infect Coleoptera on a large scale. So far, about 1500 of the probably more than one million species are named. Microsporidia are restricted to animal hosts, and all major groups of animals host microsporidia. Most infect insects, but they are also responsible for common diseases of crustaceans and fish. The named species of microsporidia usually infect one host species or a group of closely related taxa. Approximately 10 percent of the species are parasites of vertebrates —several species, most of which are opportunistic, can infect humans, in whom they can cause microsporidiosis.

Microsporidiosis is an opportunistic intestinal infection that causes diarrhea and wasting in immunocompromised individuals. It results from different species of microsporidia, a group of microbial (unicellular) fungi.

<span class="mw-page-title-main">Xenoma</span> Growth caused by various species of protists and fungi

A xenoma is a growth caused by various protists and fungi, most notably microsporidia. It can occur on numerous organisms; however is predominantly found on fish.

Enterocytozoon bieneusi is a species of the order Chytridiopsida which infects the intestinal epithelial cells. It is an obligate intracellular parasite.

<span class="mw-page-title-main">Gilt-head bream</span> Mediterranean fish

The gilt-head bream, also known as the gilthead, gilt-head seabream or silver seabream, is a species of marine ray-finned fish belonging to the family Sparidae, the seabreams or porgies. This fish is found in the Eastern Atlantic and the Mediterranean. It is a highly esteemed food fish and an important species in aquaculture.

Glugea is a genus of microsporidian parasites, predominantly infecting fish. Infections of Glugea cause xenoma formation.

Encephalitozoon intestinalis is a parasite. It can cause microsporidiosis.

Paramoeba is a genus of common parasites, including species that can cause infection in fish, crabs, sea urchins and others.

<span class="mw-page-title-main">Fish diseases and parasites</span> Disease that affects fish

Like humans and other animals, fish suffer from diseases and parasites. Fish defences against disease are specific and non-specific. Non-specific defences include skin and scales, as well as the mucus layer secreted by the epidermis that traps microorganisms and inhibits their growth. If pathogens breach these defences, fish can develop inflammatory responses that increase the flow of blood to infected areas and deliver white blood cells that attempt to destroy the pathogens.

<span class="mw-page-title-main">Warthin–Starry stain</span>

The Warthin–Starry stain (WS) is a silver nitrate-based staining method used in histology. It was first introduced in 1920 by American pathologists Aldred Scott Warthin (1866–1931) and Allen Chronister Starry (1890–1973), for the detection of spirochetes. It has been considered a standard stain for the detection of spirochetes, and is also used to stain Helicobacter pylori, Lawsonia intracellularis, Microsporidia, and particulates. It is also important for confirmation of Bartonella henselae, a causative organism in cat-scratch disease.

Ceratomyxa is a genus of myxozoan.

<i>Encephalitozoon cuniculi</i> Microsporidial pathogen

Encephalitozoon cuniculi is a microsporidial parasite of mammals with world-wide distribution. An important cause of neurologic and renal disease in rabbits, E. cuniculi can also cause disease in immunocompromised people.

Nosema bombi is a microsporidian, a small, unicellular parasite recently reclassified as a fungus that mainly affects bumble bees. It was reclassified as Vairimorpha bombi in 2020. The parasite infects numerous Bombus spp. at variable rates, and has been found to have a range of deleterious effects on its hosts.

<i>Sparicotyle chrysophrii</i> Species of worms

Sparicotyle chrysophrii is a species of monogenean, parasitic on the gills of the marine fish. It belongs to the family Microcotylidae. Its type-host is the gilt-head seabream.

<i>Enteromyxum leei</i> Species of marine parasite

Enteromyxum leei is a species of myxozoan, histozoic parasite that infects the intestinal tract and sometimes associated organs, like gall bladder and liver, of several teleostean fish species. Myxozoans are microscopic metazoans, with an obligate parasitic life-style. The parasite stages of this species live in the paracelullar space between fish enterocytes. It is the causative agent of enteromyxosis, or emaciative disease, also known as "razor blade syndrome" in sparid fish. E. leei has a wide host and geographical range within marine fish, and even freshwater fish have been infected experimentally. E. leei initially emerged in the Mediterranean in the late 1980s and it is believed to have been unintentionally introduced into the Red Sea. Its pathogenicity and economic impact depend on the host species. In the gilt-head seabream, it is manifested as a chronic disease that provokes anorexia, delayed growth with weight loss, cachexia, reduced marketability and increased mortality. In other species, it has no clinical signs. In sharpsnout seabream, infection results in very high mortality rates, which have pushed fish farmers to abandon the culture of this fish species.

Enteromyxum scophthalmi is a species of parasitic myxozoan, a pathogen of fish. It is an intestinal parasite of the turbot and can cause outbreaks of disease in farmed fish. It causes a cachectic syndrome characterised by loss of weight, muscle atrophy, weakness and fatigue.

<i>Ceratothoa oestroides</i> A parasitic marine isopod

Ceratothoa oestroides is a crustacean isopod, obligate ectoparasite of marine fish that dwells in the buccal cavity. It is the causative agent of various pathologies including tissue damage at the parasitisation site (tongue), growth defects, decrease in mean host weight and size and increases mortalities in farmed and wild fish populations. It has been recorded in six different fish families: Sparidae, Carangidae, Clupeidae, Maenidae, Scorpenidae, and Mugilidae.

Enterospora is a genus of protists belonging to the family Enterocytozoonidae.

Carlos José Correia de Azevedo is a Portuguese biologist specialising in microparasites of aquatic organisms, particularly Apicomplexa, Haplosporidia, Microsporidia, and Myxozoa.

References

  1. 1 2 3 4 5 6 Palenzuela, O., Redondo, M. J., Cali, A., Takvorian, P. M., Alonso-Naveiro, M., Alvarez-Pellitero, P., & Sitja-Bobadilla, A. (2014). A new intranuclear microsporidium, Enterospora nucleophila n. sp., causing an emaciative syndrome in a piscine host (Sparus aurata), prompts the redescription of the family Enterocytozoonidae. Int. J. Parasitol. 44:189-203.http://doi.org/10.1016/j.ijpara.2013.10.005
  2. Vossbrinck, C.R., & Debrunner-Vossbrinck, B.A. (2005). Molecular phylogeny of the Microsporidia: ecological, ultrastructural and taxonomic considerations. Folia Parasitol. 52:131-142.
  3. Amparo Picard-Sánchez, M. Carla Piazzon, Nahla Hossameldin Ahmed, Raquel Del Pozo, Ariadna Sitjà-Bobadilla, Oswaldo Palenzuela. 2020. Pathology and cellular immune response of gilthead sea bream (Sparus aurata) infected by Enterospora nucleophila (Microsporidia). Vet. Pathol.
  4. Kent, M.; Harper, C.; Wolf, J. (2012). "Documented and Potential Research Impacts of Subclinical Diseases in Zebrafish". ILAR Journal . 53 (2). Oxford University Press (OUP): 126–134. doi:10.1093/ilar.53.2.126. eISSN   1930-6180. ISSN   1084-2020. PMC   3703941 . PMID   23382344. S2CID   20772717. NIHMSID: NIHMS488220. Institute for Laboratory Animal Research.
    This review cites this research.
    Peterson, T.; Spitsbergen, J.; Feist, S.; Kent, M. (2011). "Luna stain, an improved selective stain for detection of microsporidian spores in histologic sections". Diseases of Aquatic Organisms (DAO). 95 (2). Inter-Research Science Center: 175–180. doi:10.3354/dao02346. ISSN   0177-5103. PMC   4097144 . PMID   21848126. S2CID   8753938. NIHMSID: NIHMS588204.
  5. Ahmed N.H., Caffara, M., Sitjà-Bobadilla, A., Fioravanti, M.L., Mazzone, A., Aboulezz, A. S., Metwally, A.M., Omar M.A., Palenzuela, O. (2019). Detection of the intranuclear microsporidian Enterospora nucleophila in gilthead sea bream by In situ Hybridization. J. Fish Dis. 42: 809-815. https://doi.org/10.1111/jfd.12993
  6. Hossam Eldin N, Abu El Ezz A, Del Pozo R, Metwally A, Omar M, Sitjà-Bobadilla A, Palenzuela O (2017) Validation of diagnostic methods for the detection of Enterospora nucleophila (Microsporidia) in the intestine of gilthead sea bream. Proceedings of the 18th Int. Conference on Diseases of Fish & Shellfish, p.410. (192-P).
  7. "ParaFishControl Project".