Publications by authors named "Shaozhi Zuo"

9 Publications

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Whole-genome association study searching for QTL for Aeromonas salmonicida resistance in rainbow trout.

Sci Rep 2021 Sep 8;11(1):17857. Epub 2021 Sep 8.

Laboratory of Aquatic Pathobiology, Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Frederiksberg C., Copenhagen, Denmark.

Aeromonas salmonicida subsp. salmonicida, the causative agent of furunculosis, has extensive negative effects on wild and farmed salmonids worldwide. Vaccination induces some protection under certain conditions but disease outbreaks occur even in vaccinated fish. Therefore, alternative disease control approaches are required to ensure the sustainable expansion of rainbow trout aquaculture. Selective breeding can be applied to enhance host resistance to pathogens. The present work used genome-wide association study (GWAS) to identify quantitative trait loci (QTL) associated with A. salmonicida resistance in rainbow trout. A total 798 rainbow trout exposed to A. salmonicida by bath challenge revealed 614 susceptible and 138 resistant fish. Genotyping was conducted using the 57 K single nucleotide polymorphism (SNP) array and the GWAS was performed for survival and time to death phenotypes. We identified a QTL on chromosome 16 and located positional candidate genes in the proximity of the most significant SNPs. In addition, samples from exposed fish were examined for expression of 24 immune-relevant genes indicating a systematic immune response to the infection. The present work demonstrated that resistance to A. salmonicida is moderately heritable with oligogenic architecture. These result will be useful for the future breeding programs for improving the natural resistance of rainbow trout against furunculosis.
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http://dx.doi.org/10.1038/s41598-021-97437-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8426485PMC
September 2021

(Apicomplexa) in in Europe with a potential for spread.

Int J Parasitol Parasites Wildl 2021 Aug 2;15:270-275. Epub 2021 Jul 2.

Laboratory of Aquatic Pathobiology, Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Denmark.

Four specimens of mallard () shot by local hunters (December 2020 to January 2021 along the eastern coastline of the island of Bornholm in the Baltic Sea) were diagnosed with a heavy load of sarcocysts in the musculature. Morphometric and molecular diagnosis based on rDNA (18 S, ITS1, 28 S) of parasites recovered from two of the birds revealed the causative pathogen to be . We further present novel sequences for the entire 5.8 S and ITS2 for this species. Elongate cysts (mean length 5.25 (SD 0.6) mm, width 1.37 (SD 0.2) mm) were recorded in all parts of the striated skeletal musculature of the birds. The main part (72%) of the 2585 cysts in one female mallard was located in the outer superficial pectoral musculature, with 11% in the inner pectoral musculature. Minor but significant parts were found in the dorsal, ventral abdominal, neck and head, legs, hand and arm (wing) musculature. No cysts were found in the smooth musculature. Each cyst contained a median of 3.2 mio bradyzoites indicating that more than 8 billion bradyzoites are available for infection of one or more predators/scavengers ingesting the bird. Bradyzoites (median length 13.5 μm (range 12.1-14.5) and median width 2.66 μm (range 2.1-3.3)) were highly resistant to proteinase treatment, which secures the passage through the stomach of the predator to its intestine where wall penetration takes place. One of the birds was ringed (tagged) in Sweden Island Øland in the Baltic Sea two years before being shot. This is documenting immigration of mallards from northern locations. The parasite species was originally described in North America in 1893 and was commonly reported in this region during the 20th century but not in Europe. Recent cases from Norway, Finland, Lithuania, Poland, UK and Hungary suggest that the species may be spreading geographically. Experienced duck hunters with a 40 years record of hunting on the island reported that this type of infection unprecedented. The final host is reported to be canines (fox, raccoon dog), skunk and mustelids, including ermines and American mink. Presence of these hosts in Europe may allow establishment of the life cycle and further colonization of the local duck populations which calls for implementation of a survey program in Europe.
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http://dx.doi.org/10.1016/j.ijppaw.2021.06.007DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8264532PMC
August 2021

A Major QTL for Resistance to in Rainbow Trout.

Front Genet 2020 29;11:607558. Epub 2020 Dec 29.

Laboratory of Aquatic Pathobiology, Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.

Genetic selection of disease resistant fish is a major strategy to improve health, welfare and sustainability in aquaculture. Mapping of single nucleotide polymorphisms (SNP) in the fish genome may be a fruitful tool to define relevant quantitative trait loci (QTL) and we here show its use for characterization of resistant rainbow trout (). Fingerlings were exposed to the pathogen serotype O1 in a solution of 1.5 × 10 cfu/ml and observed for 14 days. Disease signs appeared 3 days post exposure (dpe) whereafter mortality progressed exponentially until 6 dpe reaching a total mortality of 55% within 11 days. DNA was sampled from all fish - including survivors - and analyzed on a 57 k Affymetrix SNP platform whereby it was shown that disease resistance was associated with a major QTL on chromosome 21 (Omy 21). Gene expression analyses showed that diseased fish activated genes associated with innate and adaptive immune responses. The possible genes associated with resistance are discussed.
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http://dx.doi.org/10.3389/fgene.2020.607558DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7802751PMC
December 2020

Immune gene expression and genome-wide association analysis in rainbow trout with different resistance to Yersinia ruckeri infection.

Fish Shellfish Immunol 2020 Nov 11;106:441-450. Epub 2020 Aug 11.

Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Frederiksberg C., Denmark.

Selective breeding programmes involving marker assisted selection of innately pathogen resistant strains of rainbow trout rely on reliable controlled infection studies, extensive DNA typing of individual fish and recording of expression of relevant genes. We exposed juvenile rainbow trout (6 h bath to 2.6 × 10 CFU mL) to the fish pathogen Yersinia ruckeri serotype O1, biotype 2, eliciting Enteric Red Mouth Disease ERM, and followed the disease progression over 21 days. Cumulative mortality reached 42% at 12 days post challenge (dpc) after which no disease signs were recorded. All fish were sampled for DNA-typing (50 k SNP chip, Affymetrix®) throughout the course of infection when they showed clinical signs of disease (susceptible fish) or at day 21 when fish showed no clinical signs of disease (survivors - resistant fish). Genome-wide association analyses of 1027 trout applying single nucleotide polymorphisms (SNPs) as markers revealed an association between traits (susceptible/resistant) and certain regions of the trout genome. It was indicated that multiple genes are involved in rainbow trout resistance towards ERM whereby it is considered a polygenic trait. A corresponding trout group was kept as non-exposed controls and a comparative expression analysis of central innate and adaptive immune genes in gills, spleen and liver was performed for three fish groups: 1) moribund trout exhibiting clinical signs 7 dpc (CS), 2) exposed fish without clinical signs at the same sampling point (NCS) and 3) surviving fish at 21 dpc (survivors). Immune genes encoding inflammatory cytokines (IL-1β, IL-2A, IL-6A, IL-8, IL-10A, IL-12, IL-17A/F2A, IL-17C1, IL-17C2, IL-22, IFNγ, TNFα), acute phase reactants (SAA, C3, cathelicidins, lysozyme) were expressed differently in CS and NCS fish. Correlation (negative or positive) between expression of genes and bacterial load suggested involvement of immune genes in protection. Down-regulation of adaptive immune genes including IgDm, IgDs, IgT and TCR-β was seen primarily in CS and NCS fish whereas survivors showed up-regulation of effector molecule genes such as cathelicidins, complement and lysozyme suggesting their role in clearing the infection. In conclusion, SNP analyses indicated that ERM resistance in rainbow trout is a multi-locus trait. The gene expression in surviving fish suggested that several immune genes are associated with the trait conferring resistance.
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http://dx.doi.org/10.1016/j.fsi.2020.07.023DOI Listing
November 2020

Contracaecum osculatum (sensu lato) infection of Gadus morhua in the Baltic Sea: inter- and intraspecific interactions.

Int J Parasitol 2020 09 15;50(10-11):891-898. Epub 2020 Jul 15.

Department of Veterinary and Animal Science, Faculty of Health and Medical Sciences, University of Copenhagen, Frederiksberg C., Denmark. Electronic address:

The subpopulation of Atlantic cod, Gadus morhua, in the eastern part of the Baltic Sea has experienced a significant increase in infections with anisakid nematode larvae of the species Contracaecum osculatum sensu lato (s.l.) since the year 2000. The life cycle of the parasite includes seals and especially the grey seal, Halichoerus grypus, as final hosts, carrying the adult nematodes in the stomach, crustaceans (copepods, amphipods) as first intermediate hosts and various fish species (clupeids, sandeel) including cod as second intermediate/paratenic hosts. Cod with a body length below 28 cm are generally non-infected but experience increasing infection levels when they switch to a piscine diet (infected intermediate/paratenic hosts). We present an overall frequency distribution analysis of worms in 166 cod (body length 30-49 cm) collected in the spawning area over the last 5 years. It shows a fit to the negative binomial distribution, a prevalence of infection of 89.8%, a mean intensity of 29.3 parasites per fish (range 1-377) and a variance/mean ratio of 59.2 (≫1), indicating overdispersion. We present measurements of the adult Contracaecum osculatum (s.l.) specimens in the seal stomach and show that the parasites reach a maximum length of 6.6 cm (females) and 5.8 cm (males). L3s in sprat have a total length from 1to 11 mm whereas the larvae in cod liver are 3-27 mm. A decreasing mean worm length associated with high worm densities in cod (number of nematodes per liver) was recorded. Possible explanations might include timing of feeding on infected intermediate/paratenic hosts, intraspecific competition (crowding) between larvae in cod and host responses (indicated by a significant antibody production in cod against C. osculatum (s.l.) antigens). A significant negative correlation between infection intensity and muscle mass of cod was found, suggesting parasite-induced down-regulation of growth factors in cod.
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http://dx.doi.org/10.1016/j.ijpara.2020.06.003DOI Listing
September 2020

Anisakid nematode larvae in the liver of Atlantic cod Gadus morhua L. from West Greenland.

Parasitol Res 2020 Oct 13;119(10):3233-3241. Epub 2020 Jul 13.

Department of Veterinary and Animal Science, Faculty of Health and Medical Sciences, University of Copenhagen, Stigbøjlen 7, DK-1870, Frederiksberg C, Denmark.

Anisakid nematode larvae occur frequently in the liver of Atlantic cod, but merely few infection data from cod in waters around Greenland exist. The present study reports the occurrence of third-stage anisakid larvae in the livers of 200 Atlantic cod caught on fishing grounds along the West coast of Greenland (fjord systems of Maniitsoq) in May, June, August and September 2017. Classical and molecular helminthological techniques were used to identify the nematodes. A total of 200 cod livers were examined, and 194 were infected with third-stage nematode larvae (overall prevalence of infection 97%) with a mean intensity of 10.3 (range between 1 and 44 parasites per fish). Prevalences recorded were 96% for Anisakis simplex (s.l.), 55% for Pseudoterranova decipiens (s.l.) and 8% for Contracaecum osculatum (s.l.). Sequencing the mtDNA cox2 from 8 out of 23 these latter larvae conferred these to C. osculatum sp. B. A clear seasonal variation was observed, with a rise in A. simplex (s.l.) and P. decipiens (s.l.) occurrence in June and August and a decline in September. The study may serve as a baseline for future investigations using the three anisakids as biological indicators in Greenland waters.
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http://dx.doi.org/10.1007/s00436-020-06807-zDOI Listing
October 2020

Endoparasitic helminths in Baltic salmon Salmo salar: ecological implications.

Dis Aquat Organ 2019 Sep;135(3):193-199

Department of Veterinary and Animal Science, Faculty of Health and Medical Sciences, University of Copenhagen, Frederiksberg C 1870, Denmark.

Parasites in fish are ecological indicators, as they reflect the host's migration routes, feeding behavior and immune status. We performed a parasitological investigation of sea-running Baltic salmon to study the use of parasites as indicators for this fish stock. The host-a strain of Atlantic salmon Salmo salar-has been isolated for several millennia in the semi-enclosed brackish Baltic Sea, with limited migration to and from the North Sea. Twenty-four salmon (total body weight: 4.2-14.2 kg; total body length: 80-105 cm) were caught by spoon bait in the southern Baltic Sea during feeding migrations, necropsied shortly afterwards and internal organs subjected to parasitological investigation focusing on endoparasitic helminths. The pyloric region was heavily parasitized by the cestode Eubothrium crassum (100% prevalence; intensity: 97-273 parasites per infected fish), reflecting a diet of smaller pelagic fishes. The stomach contained the hemiurid digeneans Brachyphallus crenatus (95.8% prevalence; intensity: 8-151) and Hemiurus luehei (58.3% prevalence; intensity: 2-13), indicating a diet of clupeids. Schistocephalus solidus (25% prevalence; intensity: 1-2), liberated from ingested sticklebacks, the acanthocephalan Echinorhynchus truttae (54% prevalence; intensity: 1-13) and the adult nematode Hysterothylacium aduncum (29% prevalence; intensity: 1-13) were found in the intestine. The liver was parasitized by third-stage nematode larvae of Contracaecum osculatum (45.8% prevalence; intensity: 1-4), but these were growth-stunted and encapsulated. The parasite fauna differs markedly from salmon in North Atlantic waters, and the lack of purely marine parasite species indicates that the Baltic salmon has remained in the Baltic Sea during its life history.
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http://dx.doi.org/10.3354/dao03391DOI Listing
September 2019

Transcriptomic analysis of Baltic cod (Gadus morhua) liver infected with Contracaecum osculatum third stage larvae indicates parasitic effects on growth and immune response.

Fish Shellfish Immunol 2019 Oct 13;93:965-976. Epub 2019 Aug 13.

Department of Veterinary and Animal Science, Faculty of Health and Medical Sciences, University of Copenhagen, Frederiksberg C, Denmark.

High infection levels due to third-stage larvae of the anisakid nematode Contracaecum osculatum have been documented in cod from the eastern part of the Baltic sea during the latest decades. The nematode larvae mainly infect the liver of Baltic cod and prevalence of infection has reached 100% with a mean intensity up to 80 parasites per host in certain areas and size classes. Low condition factors of the cod have been observed concomitant with the rise in parasite abundance suggesting a parasitic effect on growth parameters. To investigate any association between parasite infection and physiological status of the host we performed a comparative transcriptomic analysis of liver obtained from C. osculatum infected and non-infected cod. A total of 47,025 predicted gene models showed expression in cod liver and sequences corresponding to 2084 (4.43%) unigenes were differentially expressed in infected liver when compared to non-infected liver. Of the differentially expressed unigenes (DEGs) 1240 unigenes were up-regulated while 844 unigenes were down-regulated. The Gene Ontology (GO) enrichment analysis showed that 1304 DEGs were represented in cellular process and single-organism process, cell and cell part, binding and catalytic activity. As determined by the Kyoto Encyclopedia of Gene and Genomes (KEGG) Pathways analysis, 454 DEGs were involved in 138 pathways. Ninety-seven genes were related to metabolic pathways including carbohydrate, lipid, and amino acid metabolism. Thirteen regulated genes were playing a role in immune response such as Toll-like receptor signaling, NOD-like receptor signaling, RIG-I-like receptor signalling and thirty-six genes were associated with growth processes. This indicates that the nematode infection in Baltic cod may affect on molecular mechanisms involving metabolism, immune function and growth.
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http://dx.doi.org/10.1016/j.fsi.2019.08.034DOI Listing
October 2019

Host size-dependent anisakid infection in Baltic cod Gadus morhua associated with differential food preferences.

Dis Aquat Organ 2016 Jun;120(1):69-75

Laboratory of Aquatic Pathobiology, Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen, 1870 Frederiksberg C, Denmark.

A significant increase in the infection level of Baltic cod Gadus morhua with the anisakid nematode larvae Contracaecum osculatum and Pseudoterranova decipiens has been recorded during recent years due to the expanding local population of grey seals Halichoerus grypus, which act as final hosts for these parasites. Here, we report from an investigation of 368 cod (total length [TL] 6-49 cm; caught in ICES Subdivision 25) that the infection level of juvenile cod (TL 6-30 cm) with larvae of C. osculatum and P. decipiens is absent or very low, whereas it increases drastically in larger cod (TL 31-48 cm). A third nematode Hysterothylacium aduncum was rarely found. The study indicates that the prey animals for large cod act as transport hosts for the parasite larvae. Analyses of stomach contents of cod caught in the same area (2007-2014) showed that small benthic organisms (including polychaetes Harmothoë sarsi) are preferred food items by small cod, the isopod Saduria entomon is taken by all size classes, and sprat Sprattus sprattus are common prey items for cod larger than 30 cm. Parasitological investigations (microscopic and molecular analyses) of H. sarsi (100 specimens) and S. entomon (40 specimens) did not reveal infection in these invertebrates, but 11.6% of sprat (265 specimens examined) was shown to be infected with 1-8 C. osculatum third stage larvae per fish. Analyses of sprat stomach contents confirmed that copepods and cladocerans are the main food items of sprat. These observations suggest that the C. osculatum life cycle in the Baltic Sea includes grey seals as final hosts, sprat as the first transport host and cod as second transport host. It may be speculated that sprat obtain infection by feeding on copepods and/or cladocerans, which could serve as the first intermediate hosts. One cannot exclude the possibility that the size-dependent C. osculatum infection of cod may contribute (indirectly or directly) to the differential mortality of larger cod (>38 cm) compared to smaller cod (<30 cm) recently recorded in the Baltic cod population.
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http://dx.doi.org/10.3354/dao03002DOI Listing
June 2016
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