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

Abstract 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...

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Main Authors: Kerstin Fischer, Vasyl V. Tkach, Kurt C. Curtis, Peter U. Fischer
Format: Article
Language:English
Published: BMC 2017-04-01
Series:Parasites & Vectors
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13071-017-2123-7
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spelling doaj-1ca40e09370a458c98cd1024ae3d1bb02020-11-24T21:07:50ZengBMCParasites & Vectors1756-33052017-04-0110111510.1186/s13071-017-2123-7Ultrastructure and localization of Neorickettsia in adult digenean trematodes provides novel insights into helminth-endobacteria interactionKerstin Fischer0Vasyl V. Tkach1Kurt C. Curtis2Peter U. Fischer3Infectious Diseases Division, Department of Medicine, Washington University School of MedicineDepartment of Biology, University of North DakotaInfectious Diseases Division, Department of Medicine, Washington University School of MedicineInfectious Diseases Division, Department of Medicine, Washington University School of MedicineAbstract 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. Methods We 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. Results Ultrastructural 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. Conclusions We 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.http://link.springer.com/article/10.1186/s13071-017-2123-7Digenan trematodesNeorickettsiaElectron microscopyImmunohistochemistryLocalization
collection DOAJ
language English
format Article
sources DOAJ
author Kerstin Fischer
Vasyl V. Tkach
Kurt C. Curtis
Peter U. Fischer
spellingShingle Kerstin Fischer
Vasyl V. Tkach
Kurt C. Curtis
Peter U. Fischer
Ultrastructure and localization of Neorickettsia in adult digenean trematodes provides novel insights into helminth-endobacteria interaction
Parasites & Vectors
Digenan trematodes
Neorickettsia
Electron microscopy
Immunohistochemistry
Localization
author_facet Kerstin Fischer
Vasyl V. Tkach
Kurt C. Curtis
Peter U. Fischer
author_sort Kerstin Fischer
title Ultrastructure and localization of Neorickettsia in adult digenean trematodes provides novel insights into helminth-endobacteria interaction
title_short Ultrastructure and localization of Neorickettsia in adult digenean trematodes provides novel insights into helminth-endobacteria interaction
title_full Ultrastructure and localization of Neorickettsia in adult digenean trematodes provides novel insights into helminth-endobacteria interaction
title_fullStr Ultrastructure and localization of Neorickettsia in adult digenean trematodes provides novel insights into helminth-endobacteria interaction
title_full_unstemmed Ultrastructure and localization of Neorickettsia in adult digenean trematodes provides novel insights into helminth-endobacteria interaction
title_sort ultrastructure and localization of neorickettsia in adult digenean trematodes provides novel insights into helminth-endobacteria interaction
publisher BMC
series Parasites & Vectors
issn 1756-3305
publishDate 2017-04-01
description Abstract 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. Methods We 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. Results Ultrastructural 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. Conclusions We 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.
topic Digenan trematodes
Neorickettsia
Electron microscopy
Immunohistochemistry
Localization
url http://link.springer.com/article/10.1186/s13071-017-2123-7
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