High Throughput Sequencing and Network Analysis Disentangle the Microbial Communities of Ticks and Hosts Within and Between Ecosystems

We aimed to develop a framework, based on graph theory, to capture the ecological meaning behind pure pair comparisons of microbiome-derived data. As a proof of concept, we applied the framework to analyze the co-occurrence of bacteria in either Ixodes ricinus ticks or the spleen of one of their mai...

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Main Authors: Agustín Estrada-Peña, Alejandro Cabezas-Cruz, Thomas Pollet, Muriel Vayssier-Taussat, Jean-François Cosson
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-07-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fcimb.2018.00236/full
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spelling doaj-eb365c989dc24b06ad91f5ed676a0c1e2020-11-24T21:50:32ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882018-07-01810.3389/fcimb.2018.00236363616High Throughput Sequencing and Network Analysis Disentangle the Microbial Communities of Ticks and Hosts Within and Between EcosystemsAgustín Estrada-Peña0Alejandro Cabezas-Cruz1Thomas Pollet2Muriel Vayssier-Taussat3Jean-François Cosson4Faculty of Veterinary Medicine, University of Zaragoza, Zaragoza, SpainUMR BIPAR, INRA, ANSES, Ecole Nationale Vétérinaire d'Alfort, Université Paris-Est, Maisons-Alfort, FranceUMR BIPAR, INRA, ANSES, Ecole Nationale Vétérinaire d'Alfort, Université Paris-Est, Maisons-Alfort, FranceUMR BIPAR, INRA, ANSES, Ecole Nationale Vétérinaire d'Alfort, Université Paris-Est, Maisons-Alfort, FranceUMR BIPAR, INRA, ANSES, Ecole Nationale Vétérinaire d'Alfort, Université Paris-Est, Maisons-Alfort, FranceWe aimed to develop a framework, based on graph theory, to capture the ecological meaning behind pure pair comparisons of microbiome-derived data. As a proof of concept, we applied the framework to analyze the co-occurrence of bacteria in either Ixodes ricinus ticks or the spleen of one of their main hosts, the vole Myodes glareolus. As a secondary lymphoid organ, the spleen acts as a filter of blood and represents well the exposure to microorganisms circulating in the blood; including those acquired and transmitted by ticks during feeding. The microbiome of 301 and 269 individual tick and vole samples, respectively, were analyzed using next generation sequencing (NGS) of 16S rRNA. To assess the effect of habitat on ecological communities of bacteria associated to ticks and voles, two different biotopes were included in the study, forest, and ecotone. An innovative approach of NGS data analysis combining network analysis and phylogenies of co-occuring of bacteria was used to study associations between bacteria in individual samples. Of the 126 bacterial genera found in ticks and voles, 62% were shared by both species. Communities of co-occurring bacteria were always more phylogenetically diverse in ticks than in voles. Interestingly, ~80% of bacterial phylogenetic diversity was found in ~20% of ticks. This pattern was not observed in vole-associated bacteria. Results revealed that the microbiome of I. ricinus is only slightly related to that of M. glareolus and that the biotope plays the most important role in shaping the bacterial communities of either ticks or voles. The analysis of the phylogenetic signal of the network indexes across the 16S rRNA-derived tree of bacteria suggests that the microbiome of both ticks and voles has high phylogenetic diversity and that closest bacterial genera do not co-occur. This study shows that network analysis is a promising tool to unravel complex microbial communities associated to arthropod vectors and vertebrate hosts.https://www.frontiersin.org/article/10.3389/fcimb.2018.00236/fullmicrobiometicksvolesnetwork analysisIxodes ricinusnext generation sequencing (NGS)
collection DOAJ
language English
format Article
sources DOAJ
author Agustín Estrada-Peña
Alejandro Cabezas-Cruz
Thomas Pollet
Muriel Vayssier-Taussat
Jean-François Cosson
spellingShingle Agustín Estrada-Peña
Alejandro Cabezas-Cruz
Thomas Pollet
Muriel Vayssier-Taussat
Jean-François Cosson
High Throughput Sequencing and Network Analysis Disentangle the Microbial Communities of Ticks and Hosts Within and Between Ecosystems
Frontiers in Cellular and Infection Microbiology
microbiome
ticks
voles
network analysis
Ixodes ricinus
next generation sequencing (NGS)
author_facet Agustín Estrada-Peña
Alejandro Cabezas-Cruz
Thomas Pollet
Muriel Vayssier-Taussat
Jean-François Cosson
author_sort Agustín Estrada-Peña
title High Throughput Sequencing and Network Analysis Disentangle the Microbial Communities of Ticks and Hosts Within and Between Ecosystems
title_short High Throughput Sequencing and Network Analysis Disentangle the Microbial Communities of Ticks and Hosts Within and Between Ecosystems
title_full High Throughput Sequencing and Network Analysis Disentangle the Microbial Communities of Ticks and Hosts Within and Between Ecosystems
title_fullStr High Throughput Sequencing and Network Analysis Disentangle the Microbial Communities of Ticks and Hosts Within and Between Ecosystems
title_full_unstemmed High Throughput Sequencing and Network Analysis Disentangle the Microbial Communities of Ticks and Hosts Within and Between Ecosystems
title_sort high throughput sequencing and network analysis disentangle the microbial communities of ticks and hosts within and between ecosystems
publisher Frontiers Media S.A.
series Frontiers in Cellular and Infection Microbiology
issn 2235-2988
publishDate 2018-07-01
description We aimed to develop a framework, based on graph theory, to capture the ecological meaning behind pure pair comparisons of microbiome-derived data. As a proof of concept, we applied the framework to analyze the co-occurrence of bacteria in either Ixodes ricinus ticks or the spleen of one of their main hosts, the vole Myodes glareolus. As a secondary lymphoid organ, the spleen acts as a filter of blood and represents well the exposure to microorganisms circulating in the blood; including those acquired and transmitted by ticks during feeding. The microbiome of 301 and 269 individual tick and vole samples, respectively, were analyzed using next generation sequencing (NGS) of 16S rRNA. To assess the effect of habitat on ecological communities of bacteria associated to ticks and voles, two different biotopes were included in the study, forest, and ecotone. An innovative approach of NGS data analysis combining network analysis and phylogenies of co-occuring of bacteria was used to study associations between bacteria in individual samples. Of the 126 bacterial genera found in ticks and voles, 62% were shared by both species. Communities of co-occurring bacteria were always more phylogenetically diverse in ticks than in voles. Interestingly, ~80% of bacterial phylogenetic diversity was found in ~20% of ticks. This pattern was not observed in vole-associated bacteria. Results revealed that the microbiome of I. ricinus is only slightly related to that of M. glareolus and that the biotope plays the most important role in shaping the bacterial communities of either ticks or voles. The analysis of the phylogenetic signal of the network indexes across the 16S rRNA-derived tree of bacteria suggests that the microbiome of both ticks and voles has high phylogenetic diversity and that closest bacterial genera do not co-occur. This study shows that network analysis is a promising tool to unravel complex microbial communities associated to arthropod vectors and vertebrate hosts.
topic microbiome
ticks
voles
network analysis
Ixodes ricinus
next generation sequencing (NGS)
url https://www.frontiersin.org/article/10.3389/fcimb.2018.00236/full
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