Pinniped- and Cetacean-Derived ETosis Contributes to Combating Emerging Apicomplexan Parasites (Toxoplasma gondii, Neospora caninum) Circulating in Marine Environments

Leukocytes play a major role in combating infections either by phagocytosis, release of antimicrobial granules, or extracellular trap (ET) formation. ET formation is preceded by a certain leukocyte cell death form, known as ETosis, an evolutionarily conserved mechanism of the innate immune system also observed in marine mammals. Besides several biomolecules and microbial stimuli, marine mammal ETosis is also trigged by various terrestrial protozoa and metazoa, considered nowadays as neozoan parasites, which are circulating in oceans worldwide and causing critical emerging marine diseases. Recent studies demonstrated that pinniped- and cetacean-derived polymorphonuclear neutrophils (PMNs) and monocytes are able to form different phenotypes of ET structures composed of nuclear DNA, histones, and cytoplasmic peptides/proteases against terrestrial apicomplexan parasites, e.g., Toxoplasma gondii and Neospora caninum. Detailed molecular analyses and functional studies proved that marine mammal PMNs and monocytes cast ETs in a similar way as terrestrial mammals, entrapping and immobilizing T. gondii and N. caninum tachyzoites. Pinniped- and cetacean leukocytes induce vital and suicidal ETosis, with highly reliant actions of nicotinamide adenine dinucleotide phosphate oxidase (NOX), generation of reactive oxygen species (ROS), and combined mechanisms of myeloperoxidase (MPO), neutrophil elastase (NE), and DNA citrullination via peptidylarginine deiminase IV (PAD4).This scoping review intends to summarize the knowledge on emerging protozoans in the marine environment and secondly to review limited data about ETosis mechanisms in marine mammalian species.

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Environmental pollutants and marine mammal health: The potential impact of hydrocarbons and halogenated hydrocarbons on immune system dysfunction

J. Cetacean Res. Manage. ◽

10.47536/jcrm.v18i1.254 ◽

2020 ◽

pp. 223-248

Author(s):

David Busbee ◽

Ian Tizard ◽

Jeffrey Sroit ◽

Davide Ferrirc ◽

Ellen Orr-reeves

Keyword(s):

Immune System ◽

Food Chain ◽

Marine Mammal ◽

Marine Mammals ◽

Large Scale ◽

Environmental Pollutants ◽

Halogenated Hydrocarbons ◽

Mechanisms Of Toxicity ◽

Terrestrial Mammals ◽

Immune System Dysfunction

This paper provides a detailed review of the immunotoxicological effects of environmental pollutants on the health of marine mammals, particularly in relation to their impact on the immune system and mechanisms of toxicity. Environmental pollutants are increasingly implicated (both directly and indirectly) with the onset of infectious disease and related mortality incidents in marine mammals,. The release of chemicals into the marine environment and the subsequent bioaccumulation up the food chain may pose a serious threat to marine mammals inhabiting contaminated areas; this has been documented in various studies of pollutant concentrations in tissue samples and large scale mass mortalities. Data correlating pollutant residues with altered reproductive/developmental states, and immune system dysfunction in particular, are reported for terrestrial mammals and suggest a similar association in marine mammals. Immunology is emphasised as a tool for assessing marine mammal health using quantitative and qualitative techniques to establish the effects of chemical pollutants. This has become increasingly important in relation to the subsequent dangers that may be posed to humans through any indirect exposure via the food chain.

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Exposure of free-living jaguars to Toxoplasma gondii, Neospora caninum and Sarcocystis neurona in the Brazilian Pantanal

Revista Brasileira de Parasitologia Veterinária ◽

10.1590/s1984-29612014077 ◽

2014 ◽

Vol 23 (4) ◽

pp. 547-553 ◽

Cited By ~ 5

Author(s):

Selma Samiko Miyazaki Onuma ◽

Andréia Lima Tomé Melo ◽

Daniel Luis Zanella Kantek ◽

Peter Gransden Crawshaw-Junior ◽

Ronaldo Gonçalves Morato ◽

...

Keyword(s):

Toxoplasma Gondii ◽

Neospora Caninum ◽

Antibody Test ◽

Free Living ◽

Sarcocystis Neurona ◽

Mato Grosso ◽

Apicomplexan Parasites ◽

Wide Range ◽

Coccidian Parasites ◽

Brazilian Pantanal

Toxoplasma gondii, Neospora caninum and Sarcocystis neurona are related apicomplexan parasites that cause reproductive and neurological disorders in a wide range of domestic and wild animals. In the present study, the immunofluorescence antibody test (IFAT) was used to investigate the presence of antibodies against T. gondii, N. caninum and S. neurona in the sera of 11 free-living jaguars (Panthera onca) in two protected areas in the Pantanal region of Mato Grosso state, Brazil. Ten jaguars (90.9%) showed seropositivity for T. gondii, eight (72.7%) for S. neurona, and seven (63.6%) for N. caninum antigens. Our findings reveal exposure of jaguars to these related coccidian parasites and circulation of these pathogens in this wild ecosystem. To the best of our knowledge, this is the first serological detection of N. caninum and S. neurona in free-living jaguars.

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Spectral-tuning mechanisms of marine mammal rhodopsins and correlations with foraging depth

Visual Neuroscience ◽

10.1017/s095252380017511x ◽

2000 ◽

Vol 17 (5) ◽

pp. 781-788 ◽

Cited By ~ 49

Author(s):

JEFFRY I. FASICK ◽

PHYLLIS R. ROBINSON

Keyword(s):

Amino Acid ◽

Marine Mammal ◽

Molecular Basis ◽

Marine Mammals ◽

Visual Pigments ◽

Amino Acid Substitutions ◽

Spectral Tuning ◽

Long Wavelength ◽

Terrestrial Mammals ◽

Deep Diving

It has been observed that deep-foraging marine mammals have visual pigments that are blue shifted in terms of their wavelength of maximal absorbance (λmax) when compared to analogous pigments from terrestrial mammals. The mechanisms underlying the spectral tuning of two of these blue-shifted pigments have recently been elucidated and depend on three amino acid substitutions (83Asn, 292Ser, and 299Ser) in dolphin rhodopsin, but only one amino acid substitution (308Ser) in the dolphin long-wavelength-sensitive pigment. The objective of this study was to investigate the molecular basis for changes in the spectral sensitivity of rod visual pigments from seven distantly related marine mammals. The results show a relationship between blue-shifted rhodopsins (λmax ≤ 490 nm), deep-diving foraging behavior, and the substitutions 83Asn and 292Ser. Species that forage primarily near the surface in coastal habitats have a rhodopsin with a λmax similar to that of terrestrial mammals (500 nm) and possess the substitutions 83Asp and 292Ala, identical to rhodopsins from terrestrial mammals.

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Species-specific differences in Toxoplasma gondii, Neospora caninum and Besnoitia besnoiti seroprevalence in Namibian wildlife

Parasites & Vectors ◽

10.1186/s13071-019-3871-3 ◽

2020 ◽

Vol 13 (1) ◽

Cited By ~ 4

Author(s):

Anne Seltmann ◽

Gereon Schares ◽

Ortwin H. K. Aschenborn ◽

Sonja K. Heinrich ◽

Susanne Thalwitzer ◽

...

Keyword(s):

Toxoplasma Gondii ◽

Neospora Caninum ◽

Animal Health ◽

Natural Habitat ◽

Parasitic Infections ◽

Besnoitia Besnoiti ◽

Acinonyx Jubatus ◽

Apicomplexan Parasites ◽

Wildlife Species ◽

African Lions

Abstract Background Knowledge about parasitic infections is crucial information for animal health, particularly of free-ranging species that might come into contact with livestock and humans. Methods We investigated the seroprevalence of three tissue-cyst-forming apicomplexan parasites (Toxoplasma gondii, Neospora caninum and Besnoitia besnoiti) in 506 individuals of 12 wildlife species in Namibia using in-house enzyme linked immunosorbent assays (indirect ELISAs applying purified antigens) for screening and immunoblots as confirmatory tests. We included six species of the suborder Feliformia, four species of the suborder Caniformia and two species of the suborder Ruminantia. For the two species for which we had most samples and life-history information, i.e. cheetahs (Acinonyx jubatus, n = 250) and leopards (Panthera pardus, n = 58), we investigated T. gondii seroprevalence in relation to age class, sex, sociality (solitary, mother-offspring group, independent sibling group, coalition group) and site (natural habitat vs farmland). Results All but one carnivore species (bat-eared fox Otocyon megalotis, n = 4) were seropositive to T. gondii, with a seroprevalence ranging from 52.4% (131/250) in cheetahs to 93.2% (55/59) in African lions (Panthera leo). We also detected antibodies to T. gondii in 10.0% (2/20) of blue wildebeest (Connochaetes taurinus). Adult cheetahs and leopards were more likely to be seropositive to T. gondii than subadult conspecifics, whereas seroprevalence did not vary with sex, sociality and site. Furthermore, we measured antibodies to N. caninum in 15.4% (2/13) of brown hyenas (Hyaena brunnea) and 2.6% (1/39) of black-backed jackals (Canis mesomelas). Antibodies to B. besnoiti were detected in 3.4% (2/59) of African lions and 20.0% (4/20) of blue wildebeest. Conclusions Our results demonstrate that Namibian wildlife species were exposed to apicomplexan parasites at different prevalences, depending on parasite and host species. In addition to serological work, molecular work is also needed to better understand the sylvatic cycle and the clear role of wildlife in the epidemiology of these parasites in southern Africa.

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Functional Studies with Primary Cells Provide a System for Genome-to-Phenome Investigations in Marine Mammals

Integrative and Comparative Biology ◽

10.1093/icb/icaa065 ◽

2020 ◽

Vol 60 (2) ◽

pp. 348-360 ◽

Cited By ~ 1

Author(s):

Emily K Lam ◽

Kaitlin N Allen ◽

Julia María Torres-Velarde ◽

José Pablo Vázquez-Medina

Keyword(s):

Marine Mammals ◽

Supply And Demand ◽

Mammalian Species ◽

Physiological Adaptation ◽

Primary Cells ◽

Functional Studies ◽

Terrestrial Mammals ◽

Physiological Adaptations ◽

Cellular Modeling

Synopsis Marine mammals exhibit some of the most dramatic physiological adaptations in their clade and offer unparalleled insights into the mechanisms driving convergent evolution on relatively short time scales. Some of these adaptations, such as extreme tolerance to hypoxia and prolonged food deprivation, are uncommon among most terrestrial mammals and challenge established metabolic principles of supply and demand balance. Non-targeted omics studies are starting to uncover the genetic foundations of such adaptations, but tools for testing functional significance in these animals are currently lacking. Cellular modeling with primary cells represents a powerful approach for elucidating the molecular etiology of physiological adaptation, a critical step in accelerating genome-to-phenome studies in organisms in which transgenesis is impossible (e.g., large-bodied, long-lived, fully aquatic, federally protected species). Gene perturbation studies in primary cells can directly evaluate whether specific mutations, gene loss, or duplication confer functional advantages such as hypoxia or stress tolerance in marine mammals. Here, we summarize how genetic and pharmacological manipulation approaches in primary cells have advanced mechanistic investigations in other non-traditional mammalian species, and highlight the need for such investigations in marine mammals. We also provide key considerations for isolating, culturing, and conducting experiments with marine mammal cells under conditions that mimic in vivo states. We propose that primary cell culture is a critical tool for conducting functional mechanistic studies (e.g., gene knockdown, over-expression, or editing) that can provide the missing link between genome- and organismal-level understanding of physiological adaptations in marine mammals.

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Metabolic rates of seals and whales

Canadian Journal of Zoology ◽

10.1139/z86-047 ◽

1986 ◽

Vol 64 (2) ◽

pp. 279-284 ◽

Cited By ~ 112

Author(s):

D. M. Lavigne ◽

S. Innes ◽

G. A. J. Worthy ◽

K. M. Kovacs ◽

O. J. Schmitz ◽

...

Keyword(s):

Metabolic Rate ◽

Food Consumption ◽

Marine Mammal ◽

Critical Review ◽

Comparative Studies ◽

Marine Mammals ◽

Metabolic Rates ◽

Sea Lions ◽

Terrestrial Mammals ◽

Fur Seals

A critical review of metabolic rate determinations for pinnipeds (seals, sea lions, fur seals, and walrus) and cetaceans (whales, dolphins, and porpoises) does not support the widely accepted generalization that they have higher metabolic rates than terrestrial mammals of similar size. This finding necessitates a rethinking of the thermoregulatory adaptations of these marine mammals for an aquatic existence and has important implications in comparative studies of mammals, which frequently omit marine forms because they are perceived to be "different" from other mammals. It also suggests that numerous studies have overestimated food consumption by marine mammal populations.

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The structure of a major surface antigen SAG19 from Eimeria tenella unifies the Eimeria SAG family

Communications Biology ◽

10.1038/s42003-021-01904-w ◽

2021 ◽

Vol 4 (1) ◽

Author(s):

Nur Zazarina Ramly ◽

Samuel R. Dix ◽

Sergey N. Ruzheinikov ◽

Svetlana E. Sedelnikova ◽

Patrick J. Baker ◽

...

Keyword(s):

Toxoplasma Gondii ◽

Neospora Caninum ◽

Sequence Similarity ◽

Surface Antigens ◽

Eimeria Tenella ◽

Besnoitia Besnoiti ◽

Sequence Comparisons ◽

Host Interactions ◽

Apicomplexan Parasites ◽

Major Surface

AbstractIn infections by apicomplexan parasites including Plasmodium, Toxoplasma gondii, and Eimeria, host interactions are mediated by proteins including families of membrane-anchored cysteine-rich surface antigens (SAGs) and SAG-related sequences (SRS). Eimeria tenella causes caecal coccidiosis in chickens and has a SAG family with over 80 members making up 1% of the proteome. We have solved the structure of a representative E. tenella SAG, EtSAG19, revealing that, despite a low level of sequence similarity, the entire Eimeria SAG family is unified by its three-layer αβα fold which is related to that of the CAP superfamily. Furthermore, sequence comparisons show that the Eimeria SAG fold is conserved in surface antigens of the human coccidial parasite Cyclospora cayetanensis but this fold is unrelated to that of the SAGs/SRS proteins expressed in other apicomplexans including Plasmodium species and the cyst-forming coccidia Toxoplasma gondii, Neospora caninum and Besnoitia besnoiti. However, despite having very different structures, Consurf analysis showed that Eimeria SAG and Toxoplasma SRS families each exhibit marked hotspots of sequence hypervariability that map to their surfaces distal to the membrane anchor. This suggests that the primary and convergent purpose of the different structures is to provide a platform onto which sequence variability can be imposed.

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