"Salmon Poisoning" Disease. IV. Transmission of the Disease to Dogs by Nanophyetus salmincola Eggs

Nyberg, Peter A.; Knapp, Stuart E.; Millemann, Raymond E.

doi:10.2307/3276754

Cited by 12 publications

(13 citation statements)

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“…To study N. helminthoeca transmission by trematode eggs, dogs were injected either with fluke eggs homogenized in a glass tissue grinder or with intact eggs. Only homogenized eggs were infectious to dogs, suggesting that infectious Neorickettsiae were localized within the interior of the unembryonated N. salmincola eggs but not outside the egg shells [28]. In agreement with this observation we never observed in the present study endobacteria on the surface of the egg shell, and only relatively small numbers within the egg.…”

Section: Discussionsupporting

confidence: 91%

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Ultrastructure and localization of Neorickettsia in adult digenean trematodes provides novel insights into helminth-endobacteria interaction

et al. 2017

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Background Neorickettsia are a group of intracellular α proteobacteria transmitted by digeneans (Platyhelminthes, Trematoda). These endobacteria can also infect vertebrate hosts of the helminths and cause serious diseases in animals and humans. Neorickettsia have been isolated from infected animals and maintained in cell cultures, and their morphology in mammalian cells has been described. However, limited information is available on the morphology and localization of Neorickettsia in the trematode host.MethodsWe used a Neorickettsia-infected strain of the model trematode Plagiorchis elegans to infect Syrian Golden hamsters to produce adult worms. Ultrastructure of Neorickettsia was assessed by transmission electron microscopy of high pressure freezing/freeze substitution fixed specimens. A Neorickettsia surface protein from P. elegans (PeNsp-3) was cloned and antibodies against the recombinant protein were used to localize Neorickettsia by immunohistochemistry.ResultsUltrastructural analysis revealed moderate numbers of pleomorphic endobacteria with a median size of 600 × 400 nm and characteristic double membranes in various tissue types. Endobacteria showed tubular membrane invaginations and secretion of polymorphic vesicles. Endobacteria were unevenly localized as single cells, or less frequently as small morula-like clusters in the ovary, Mehlis’ gland, vitelline follicles, uterus, intrauterine eggs, testis, cirrus-sac, tegument, intestine and the oral and ventral sucker. Examination of hamster small intestine infected with P. elegans showed many endobacteria at the host-parasite interface such as the oral and ventral sucker, the tegument and the excretory pore.ConclusionsWe conclude that adult P. elegans trematodes carry Neorickettsia endobacteria in varying numbers in many tissue types that support vertical transmission, trematode to trematode transmission via seminal fluid, and possibly horizontal transmission from trematodes to vertebrate hosts. These means appear to be novel mechanisms of pathogen transmission by endoparasitic worms.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-017-2123-7) contains supplementary material, which is available to authorized users.

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Section: Discussionsupporting

confidence: 91%

“…It has been reported that N. risticii was horizontally transmitted to bats by its trematode host Acantharium oregonense or that N. helminthoeca was transmitted to dogs by adult Nanophyetus salmincola trematodes [11, 28]. In both reports trematode eggs were considered as source of infection.…”

Section: Discussionmentioning

confidence: 99%

Ultrastructure and localization of Neorickettsia in adult digenean trematodes provides novel insights into helminth-endobacteria interaction

et al. 2017

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“…Prior to our research, it had been presumed that Neorickettsia is transmitted transovarially to successive generations of digeneans (9). However, it remained unknown how the eggs became infected with neorickettsiae.…”

Section: Discussionmentioning

confidence: 99%

“…However, there has been no study to directly and systematically identify the location of the bacteria within a digenean host. Nyberg et al (9) successfully transmitted Neorickettsia helminthoeca, the causative agent of salmon dog poisoning disease, by injecting dogs with fluke eggs homogenized in a glass tissue grinder but not with intact eggs, indicating that infectious neorickettsiae are contained within the interior of Nanophyetus salmincola eggs but not on the exterior surfaces of the egg shells. This led the authors to conclude that N. helminthoeca is transmitted transovarially to successive generations of digeneans.…”

mentioning

confidence: 99%

Germs within Worms: Localization of Neorickettsia sp. within Life Cycle Stages of the Digenean Plagiorchis elegans

Greiman

Rikihisa

Cain

et al. 2016

Appl Environ Microbiol

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Neorickettsia spp. are bacterial endosymbionts of parasitic flukes (Digenea) that also have the potential to infect and cause disease (e.g., Sennetsu fever) in the vertebrate hosts of the fluke. One of the largest gaps in our knowledge of Neorickettsia biology is the very limited information available regarding the localization of the bacterial endosymbiont within its digenean host. In this study, we used indirect immunofluorescence microscopy to visualize Neorickettsia sp. within several life cycle stages of the digenean Plagiorchis elegans. Individual sporocysts, cercariae, metacercariae, and adults of P. elegans naturally infected with Neorickettsia sp. were obtained from our laboratory-maintained life cycle, embedded, sectioned, and prepared for indirect immunofluorescence microscopy using anti-Neorickettsia risticii horse serum as the primary antibody. Neorickettsia sp. was found within the tegument of sporocysts, throughout cercarial embryos (germ balls) and fully formed cercariae (within the sporocysts), throughout metacercariae, and within the tegument, parenchyma, vitellaria, uteri, testes, cirrus sacs, and eggs of adults. Interestingly, Neorickettsia sp. was not found within the ovarian tissue. This suggests that vertical transmission of Neorickettsia within adult digeneans occurs via the incorporation of infected vitelline cells into the egg rather than direct infection of the ooplasm of the oocyte, as has been described for other bacterial endosymbionts of invertebrates (e.g., Rickettsia and Wolbachia). Bacteria in the genus Neorickettsia (order Rickettsiales, family Anaplasmataceae) are intracellular endosymbionts of digeneans. Digeneans are a diverse group of metazoan endoparasitic flatworms, with Ͼ18,000 nominal species (1). Digeneans have complex life cycles involving several stages that require two to four hosts for completion. Adult digeneans produce eggs containing a miracidium stage that penetrates the body of the first intermediate host (always a mollusk). The miracidium develops into a mother sporocyst, which produces daughter sporocysts, or rediae, by asexual reproduction, depending on the group of digeneans. Daughter sporocysts/rediae produce numerous free-living cercariae, which usually (with some exceptions) need to penetrate a second intermediate (usually an arthropod or a vertebrate) host to become metacercariae. When an infected intermediate host is eaten by a suitable definitive host, the metacercariae develop into hermaphroditic adult digeneans, which then reproduce sexually.Neorickettsiae are maintained throughout the digenean life cycle by vertical transmission. In some cases, neorickettsiae may be transmitted horizontally by digeneans to their vertebrate definitive hosts, where the bacteria can infect leukocytes and cause debilitating disease in horses, dogs, black bears, and humans (2).The localization of Neorickettsia in the vertebrate definitive host tissue is well known. A number of studies (3-8) have used techniques, such as in situ hybridization, immunofluorescence microsc...

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“…are unique environmental, Gram-negative, obligate intracellular bacteria maintained in nature through vertical transmission in trematodes (16,17,39,42). Neorickettsia spp.…”

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confidence: 99%

Proteomic Analysis of Neorickettsia sennetsu Surface-Exposed Proteins and Porin Activity of the Major Surface Protein P51

2010

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Neorickettsia sennetsu is an obligate intracellular bacterium of monocytes and macrophages and is the etiologic agent of human Sennetsu neorickettsiosis. Neorickettsia proteins expressed in mammalian host cells, including the surface proteins of Neorickettsia spp., have not been defined. In this paper, we isolated surface-exposed proteins from N. sennetsu by biotin surface labeling followed by streptavidin-affinity chromatography. Forty-two of the total of 936 (4.5%) N. sennetsu open reading frames (ORFs) were detected by liquid chromatography-tandem mass spectrometry (LC/MS/MS), including six hypothetical proteins. Among the major proteins identified were the two major ␤-barrel proteins: the 51-kDa antigen (P51) and Neorickettsia surface protein 3 (Nsp3). Immunofluorescence labeling not only confirmed surface exposure of these proteins but also showed rosary-like circumferential labeling with anti-P51 for the majority of bacteria and polar to diffuse punctate labeling with anti-Nsp3 for a minority of bacteria. We found that the isolated outer membrane of N. sennetsu had porin activity, as measured by a proteoliposome swelling assay. This activity allowed the diffusion of L-glutamine, the monosaccharides arabinose and glucose, and the tetrasaccharide stachyose, which could be inhibited with anti-P51 antibody. We purified native P51 and Nsp3 under nondenaturing conditions. When reconstituted into proteoliposomes, purified P51, but not Nsp3, exhibited prominent porin activity. This the first proteomic study of a Neorickettsia sp. showing new sets of proteins evolved as major surface proteins for Neorickettsia and the first identification of a porin for the genus Neorickettsia.

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"Salmon Poisoning" Disease. IV. Transmission of the Disease to Dogs by Nanophyetus salmincola Eggs

Cited by 12 publications

References 5 publications

Ultrastructure and localization of Neorickettsia in adult digenean trematodes provides novel insights into helminth-endobacteria interaction

Ultrastructure and localization of Neorickettsia in adult digenean trematodes provides novel insights into helminth-endobacteria interaction

Germs within Worms: Localization of Neorickettsia sp. within Life Cycle Stages of the Digenean Plagiorchis elegans

Proteomic Analysis of Neorickettsia sennetsu Surface-Exposed Proteins and Porin Activity of the Major Surface Protein P51

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