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Adult schistosomes have an epithelial bacterial population distinct from the surrounding mammalian host blood

BACKGROUND: Schistosomiasis is a neglected tropical parasitic and chronic disease affecting hundreds of millions of people. Adult schistosomes reside in the blood stream of the definitive mammalian host. These helminth parasites possess two epithelial surfaces, the tegument and the gastrodermis, bot...

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Autores principales: Gobert, Geoffrey N., McManus, Donald P., McMullan, Geoff, Creevey, Christopher J., Carson, Jack, Jones, Malcolm K., Nawaratna, Sujeevi S. K., Weerakoon, Kosala G., You, Hong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8794206/
https://www.ncbi.nlm.nih.gov/pubmed/35085360
http://dx.doi.org/10.1371/journal.pone.0263188
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author Gobert, Geoffrey N.
McManus, Donald P.
McMullan, Geoff
Creevey, Christopher J.
Carson, Jack
Jones, Malcolm K.
Nawaratna, Sujeevi S. K.
Weerakoon, Kosala G.
You, Hong
author_facet Gobert, Geoffrey N.
McManus, Donald P.
McMullan, Geoff
Creevey, Christopher J.
Carson, Jack
Jones, Malcolm K.
Nawaratna, Sujeevi S. K.
Weerakoon, Kosala G.
You, Hong
author_sort Gobert, Geoffrey N.
collection PubMed
description BACKGROUND: Schistosomiasis is a neglected tropical parasitic and chronic disease affecting hundreds of millions of people. Adult schistosomes reside in the blood stream of the definitive mammalian host. These helminth parasites possess two epithelial surfaces, the tegument and the gastrodermis, both of which interact with the host during immune evasion and in nutrient uptake. METHODS: Female ARC Swiss mice (4–6 weeks old) were infected percutaneously with Schistosoma japonicum cercariae freshly shed from Oncomelania hupensis quadrasi snails (Philippines strain). Fluorescent in situ hybridisation (FISH) was performed by using fresh adult S. japonicum perfused from those infected mice. Adult S. japonicum worms were processed to isolate the tegument from the carcass containing the gastrodermis; blood and bile were collected individually from infected and uninfected mice. Total DNA extracted from all those samples were used for microbiome profiling. RESULTS: FISH and microbiome profiling showed the presence of bacterial populations on two epithelial surfaces of adult worms, suggesting they were distinct not only from the host blood but also from each other. Whereas microbial diversity was reduced overall in the parasite epithelial tissues when compared with that of host blood, specific bacterial taxa, including Anoxybacillus and Escherichia, were elevated on the tegument. Minimal differences were evident in the microbiome of host blood during an active infection, compared with that of control uninfected blood. However, sampling of bile from infected animals identified some differences compared with controls, including elevated levels of Limnohabitans, Clostridium and Curvibacter. CONCLUSIONS: Using FISH and microbial profiling, we were able to demonstrate, for the first time, that bacteria are presented on the epithelial surfaces of adult schistosomes. These schistosome surface-associated bacteria, which are distinct from the host blood microenvironment, should be considered as a new and important component of the host-schistosome interaction. The importance of individual bacterial species in relation to schistosome parasitism needs further elucidation.
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spelling pubmed-87942062022-01-28 Adult schistosomes have an epithelial bacterial population distinct from the surrounding mammalian host blood Gobert, Geoffrey N. McManus, Donald P. McMullan, Geoff Creevey, Christopher J. Carson, Jack Jones, Malcolm K. Nawaratna, Sujeevi S. K. Weerakoon, Kosala G. You, Hong PLoS One Research Article BACKGROUND: Schistosomiasis is a neglected tropical parasitic and chronic disease affecting hundreds of millions of people. Adult schistosomes reside in the blood stream of the definitive mammalian host. These helminth parasites possess two epithelial surfaces, the tegument and the gastrodermis, both of which interact with the host during immune evasion and in nutrient uptake. METHODS: Female ARC Swiss mice (4–6 weeks old) were infected percutaneously with Schistosoma japonicum cercariae freshly shed from Oncomelania hupensis quadrasi snails (Philippines strain). Fluorescent in situ hybridisation (FISH) was performed by using fresh adult S. japonicum perfused from those infected mice. Adult S. japonicum worms were processed to isolate the tegument from the carcass containing the gastrodermis; blood and bile were collected individually from infected and uninfected mice. Total DNA extracted from all those samples were used for microbiome profiling. RESULTS: FISH and microbiome profiling showed the presence of bacterial populations on two epithelial surfaces of adult worms, suggesting they were distinct not only from the host blood but also from each other. Whereas microbial diversity was reduced overall in the parasite epithelial tissues when compared with that of host blood, specific bacterial taxa, including Anoxybacillus and Escherichia, were elevated on the tegument. Minimal differences were evident in the microbiome of host blood during an active infection, compared with that of control uninfected blood. However, sampling of bile from infected animals identified some differences compared with controls, including elevated levels of Limnohabitans, Clostridium and Curvibacter. CONCLUSIONS: Using FISH and microbial profiling, we were able to demonstrate, for the first time, that bacteria are presented on the epithelial surfaces of adult schistosomes. These schistosome surface-associated bacteria, which are distinct from the host blood microenvironment, should be considered as a new and important component of the host-schistosome interaction. The importance of individual bacterial species in relation to schistosome parasitism needs further elucidation. Public Library of Science 2022-01-27 /pmc/articles/PMC8794206/ /pubmed/35085360 http://dx.doi.org/10.1371/journal.pone.0263188 Text en © 2022 Gobert et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Gobert, Geoffrey N.
McManus, Donald P.
McMullan, Geoff
Creevey, Christopher J.
Carson, Jack
Jones, Malcolm K.
Nawaratna, Sujeevi S. K.
Weerakoon, Kosala G.
You, Hong
Adult schistosomes have an epithelial bacterial population distinct from the surrounding mammalian host blood
title Adult schistosomes have an epithelial bacterial population distinct from the surrounding mammalian host blood
title_full Adult schistosomes have an epithelial bacterial population distinct from the surrounding mammalian host blood
title_fullStr Adult schistosomes have an epithelial bacterial population distinct from the surrounding mammalian host blood
title_full_unstemmed Adult schistosomes have an epithelial bacterial population distinct from the surrounding mammalian host blood
title_short Adult schistosomes have an epithelial bacterial population distinct from the surrounding mammalian host blood
title_sort adult schistosomes have an epithelial bacterial population distinct from the surrounding mammalian host blood
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8794206/
https://www.ncbi.nlm.nih.gov/pubmed/35085360
http://dx.doi.org/10.1371/journal.pone.0263188
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