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Microbiota and gut ultrastructure of Anisakis pegreffii isolated from stranded cetaceans in the Adriatic Sea

BACKGROUND: Inferring the microbiota diversity of helminths enables depiction of evolutionarily established ecological and pathological traits that characterize a particular parasite-host interaction. In turn, these traits could provide valuable information for the development of parasitosis control...

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Autores principales: Mladineo, Ivona, Hrabar, Jerko, Vrbatović, Anamarija, Duvnjak, Sanja, Gomerčić, Tomislav, Đuras, Martina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6668197/
https://www.ncbi.nlm.nih.gov/pubmed/31362767
http://dx.doi.org/10.1186/s13071-019-3636-z
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author Mladineo, Ivona
Hrabar, Jerko
Vrbatović, Anamarija
Duvnjak, Sanja
Gomerčić, Tomislav
Đuras, Martina
author_facet Mladineo, Ivona
Hrabar, Jerko
Vrbatović, Anamarija
Duvnjak, Sanja
Gomerčić, Tomislav
Đuras, Martina
author_sort Mladineo, Ivona
collection PubMed
description BACKGROUND: Inferring the microbiota diversity of helminths enables depiction of evolutionarily established ecological and pathological traits that characterize a particular parasite-host interaction. In turn, these traits could provide valuable information for the development of parasitosis control and mitigation strategy. The parasite Anisakis pegreffii (Nematoda: Anisakidae) realizes the final stage of its life-cycle within gastric chambers of aquatic mammals, causing mild-to-moderate granulomatous gastritis with eosinophilic infiltrate, to severe ulcerative gastritis with mixed inflammatory infiltrate, often associated with bacterial colonies. However, its interaction with the host microbiota remains unknown, and might reveal important aspects of parasite colonization and propagation within the final host. METHODS: MySeq Illumina sequencing was performed for the 16S rRNA gene from microbiota isolated from larvae, and uterus and gut of adult A. pegreffii parasitizing stranded striped dolphins (Stenella coeruleoalba). To assess the potential presence of Brucella ceti within isolated microbiota, Brucella-targeted real-time PCR was undertaken. In addition, TEM of the gastrointestinal tract of the infective third-stage (L3) and transitioning fourth-stage larvae (L4) was performed to characterize the morphological differences and the level of larval feeding activity. RESULTS: In total, 230 distinct operational taxonomic units (OTUs) were identified across all samples (n = 20). The number of shared taxa was lower than the number of taxa found specifically in each parasite stage or organ. The dominant taxon was Mycoplasmataceae (genus Mycoplasma) in the gut and uterus of adult A. pegreffii, whereas Fusobacteriaceae (genus Cetobacterium) was the most abundant in 40% of larvae, alongside Mycoplasmataceae. No B. ceti DNA was detected in any of the microbiota isolates. TEM revealed differences in gut ultrastructure between L3 and L4, reflecting a feeble, most likely passive, level of feeding activity in L3. CONCLUSIONS: Microbiota from L3 was more related to that of the gut rather than the uterus of adult A. pegreffii. Taxa of the larval microbiota showed qualitative and quantitative perturbations, likely reflecting the propagation through different environments during its life-cycle. This suggests an ontogenetic shift in the alpha and beta diversity of microbial communities from uterus-derived towards cetacean-derived microbiota. Although TEM did not reveal active L3 feeding, microbiota of the latter showed similarity to that of an actively feeding adult nematode. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13071-019-3636-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-66681972019-08-06 Microbiota and gut ultrastructure of Anisakis pegreffii isolated from stranded cetaceans in the Adriatic Sea Mladineo, Ivona Hrabar, Jerko Vrbatović, Anamarija Duvnjak, Sanja Gomerčić, Tomislav Đuras, Martina Parasit Vectors Research BACKGROUND: Inferring the microbiota diversity of helminths enables depiction of evolutionarily established ecological and pathological traits that characterize a particular parasite-host interaction. In turn, these traits could provide valuable information for the development of parasitosis control and mitigation strategy. The parasite Anisakis pegreffii (Nematoda: Anisakidae) realizes the final stage of its life-cycle within gastric chambers of aquatic mammals, causing mild-to-moderate granulomatous gastritis with eosinophilic infiltrate, to severe ulcerative gastritis with mixed inflammatory infiltrate, often associated with bacterial colonies. However, its interaction with the host microbiota remains unknown, and might reveal important aspects of parasite colonization and propagation within the final host. METHODS: MySeq Illumina sequencing was performed for the 16S rRNA gene from microbiota isolated from larvae, and uterus and gut of adult A. pegreffii parasitizing stranded striped dolphins (Stenella coeruleoalba). To assess the potential presence of Brucella ceti within isolated microbiota, Brucella-targeted real-time PCR was undertaken. In addition, TEM of the gastrointestinal tract of the infective third-stage (L3) and transitioning fourth-stage larvae (L4) was performed to characterize the morphological differences and the level of larval feeding activity. RESULTS: In total, 230 distinct operational taxonomic units (OTUs) were identified across all samples (n = 20). The number of shared taxa was lower than the number of taxa found specifically in each parasite stage or organ. The dominant taxon was Mycoplasmataceae (genus Mycoplasma) in the gut and uterus of adult A. pegreffii, whereas Fusobacteriaceae (genus Cetobacterium) was the most abundant in 40% of larvae, alongside Mycoplasmataceae. No B. ceti DNA was detected in any of the microbiota isolates. TEM revealed differences in gut ultrastructure between L3 and L4, reflecting a feeble, most likely passive, level of feeding activity in L3. CONCLUSIONS: Microbiota from L3 was more related to that of the gut rather than the uterus of adult A. pegreffii. Taxa of the larval microbiota showed qualitative and quantitative perturbations, likely reflecting the propagation through different environments during its life-cycle. This suggests an ontogenetic shift in the alpha and beta diversity of microbial communities from uterus-derived towards cetacean-derived microbiota. Although TEM did not reveal active L3 feeding, microbiota of the latter showed similarity to that of an actively feeding adult nematode. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13071-019-3636-z) contains supplementary material, which is available to authorized users. BioMed Central 2019-07-30 /pmc/articles/PMC6668197/ /pubmed/31362767 http://dx.doi.org/10.1186/s13071-019-3636-z Text en © The Author(s) 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Mladineo, Ivona
Hrabar, Jerko
Vrbatović, Anamarija
Duvnjak, Sanja
Gomerčić, Tomislav
Đuras, Martina
Microbiota and gut ultrastructure of Anisakis pegreffii isolated from stranded cetaceans in the Adriatic Sea
title Microbiota and gut ultrastructure of Anisakis pegreffii isolated from stranded cetaceans in the Adriatic Sea
title_full Microbiota and gut ultrastructure of Anisakis pegreffii isolated from stranded cetaceans in the Adriatic Sea
title_fullStr Microbiota and gut ultrastructure of Anisakis pegreffii isolated from stranded cetaceans in the Adriatic Sea
title_full_unstemmed Microbiota and gut ultrastructure of Anisakis pegreffii isolated from stranded cetaceans in the Adriatic Sea
title_short Microbiota and gut ultrastructure of Anisakis pegreffii isolated from stranded cetaceans in the Adriatic Sea
title_sort microbiota and gut ultrastructure of anisakis pegreffii isolated from stranded cetaceans in the adriatic sea
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6668197/
https://www.ncbi.nlm.nih.gov/pubmed/31362767
http://dx.doi.org/10.1186/s13071-019-3636-z
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