Beyond the limits of the unassigned protist microbiome: inferring large-scale spatio-temporal patterns of Syndiniales marine parasites

Abstract Marine protists are major components of the oceanic microbiome that remain largely unrepresented in culture collections and genomic reference databases. The exploration of this uncharted protist diversity in oceanic communities relies essentially on studying genetic markers from the environ...

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Main Authors: Iris Rizos, Pavla Debeljak, Thomas Finet, Dylan Klein, Sakina-Dorothée Ayata, Fabrice Not, Lucie Bittner
Format: Article
Language:English
Published: Oxford University Press 2023-02-01
Series:ISME Communications
Online Access:https://doi.org/10.1038/s43705-022-00203-7
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author Iris Rizos
Pavla Debeljak
Thomas Finet
Dylan Klein
Sakina-Dorothée Ayata
Fabrice Not
Lucie Bittner
author_facet Iris Rizos
Pavla Debeljak
Thomas Finet
Dylan Klein
Sakina-Dorothée Ayata
Fabrice Not
Lucie Bittner
author_sort Iris Rizos
collection DOAJ
description Abstract Marine protists are major components of the oceanic microbiome that remain largely unrepresented in culture collections and genomic reference databases. The exploration of this uncharted protist diversity in oceanic communities relies essentially on studying genetic markers from the environment as taxonomic barcodes. Here we report that across 6 large scale spatio-temporal planktonic surveys, half of the genetic barcodes remain taxonomically unassigned at the genus level, preventing a fine ecological understanding for numerous protist lineages. Among them, parasitic Syndiniales (Dinoflagellata) appear as the least described protist group. We have developed a computational workflow, integrating diverse 18S rDNA gene metabarcoding datasets, in order to infer large-scale ecological patterns at 100% similarity of the genetic marker, overcoming the limitation of taxonomic assignment. From a spatial perspective, we identified 2171 unassigned clusters, i.e., Syndiniales sequences with 100% similarity, exclusively shared between the Tropical/Subtropical Ocean and the Mediterranean Sea among all Syndiniales orders and 25 ubiquitous clusters shared within all the studied marine regions. From a temporal perspective, over 3 time-series, we highlighted 39 unassigned clusters that follow rhythmic patterns of recurrence and are the best indicators of parasite community’s variation. These clusters withhold potential as ecosystem change indicators, mirroring their associated host community responses. Our results underline the importance of Syndiniales in structuring planktonic communities through space and time, raising questions regarding host-parasite association specificity and the trophic mode of persistent Syndiniales, while providing an innovative framework for prioritizing unassigned protist taxa for further description.
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spelling doaj.art-18f2e70073d3483c9592b6c563a83aa72024-04-02T05:43:36ZengOxford University PressISME Communications2730-61512023-02-013111110.1038/s43705-022-00203-7Beyond the limits of the unassigned protist microbiome: inferring large-scale spatio-temporal patterns of Syndiniales marine parasitesIris Rizos0Pavla Debeljak1Thomas Finet2Dylan Klein3Sakina-Dorothée Ayata4Fabrice Not5Lucie Bittner6Institut de Systématique, Evolution, Biodiversité (ISYEB), Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des AntillesInstitut de Systématique, Evolution, Biodiversité (ISYEB), Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des AntillesInstitut de Systématique, Evolution, Biodiversité (ISYEB), Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des AntillesInstitut de Systématique, Evolution, Biodiversité (ISYEB), Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des AntillesSorbonne Université, Laboratoire d’Océanographie et du Climat: Expérimentation et Analyses Numériques (LOCEAN, SU/CNRS/IRD/MNHN)Sorbonne Université, CNRS, AD2M-UMR7144 Station Biologique de RoscoffInstitut de Systématique, Evolution, Biodiversité (ISYEB), Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des AntillesAbstract Marine protists are major components of the oceanic microbiome that remain largely unrepresented in culture collections and genomic reference databases. The exploration of this uncharted protist diversity in oceanic communities relies essentially on studying genetic markers from the environment as taxonomic barcodes. Here we report that across 6 large scale spatio-temporal planktonic surveys, half of the genetic barcodes remain taxonomically unassigned at the genus level, preventing a fine ecological understanding for numerous protist lineages. Among them, parasitic Syndiniales (Dinoflagellata) appear as the least described protist group. We have developed a computational workflow, integrating diverse 18S rDNA gene metabarcoding datasets, in order to infer large-scale ecological patterns at 100% similarity of the genetic marker, overcoming the limitation of taxonomic assignment. From a spatial perspective, we identified 2171 unassigned clusters, i.e., Syndiniales sequences with 100% similarity, exclusively shared between the Tropical/Subtropical Ocean and the Mediterranean Sea among all Syndiniales orders and 25 ubiquitous clusters shared within all the studied marine regions. From a temporal perspective, over 3 time-series, we highlighted 39 unassigned clusters that follow rhythmic patterns of recurrence and are the best indicators of parasite community’s variation. These clusters withhold potential as ecosystem change indicators, mirroring their associated host community responses. Our results underline the importance of Syndiniales in structuring planktonic communities through space and time, raising questions regarding host-parasite association specificity and the trophic mode of persistent Syndiniales, while providing an innovative framework for prioritizing unassigned protist taxa for further description.https://doi.org/10.1038/s43705-022-00203-7
spellingShingle Iris Rizos
Pavla Debeljak
Thomas Finet
Dylan Klein
Sakina-Dorothée Ayata
Fabrice Not
Lucie Bittner
Beyond the limits of the unassigned protist microbiome: inferring large-scale spatio-temporal patterns of Syndiniales marine parasites
ISME Communications
title Beyond the limits of the unassigned protist microbiome: inferring large-scale spatio-temporal patterns of Syndiniales marine parasites
title_full Beyond the limits of the unassigned protist microbiome: inferring large-scale spatio-temporal patterns of Syndiniales marine parasites
title_fullStr Beyond the limits of the unassigned protist microbiome: inferring large-scale spatio-temporal patterns of Syndiniales marine parasites
title_full_unstemmed Beyond the limits of the unassigned protist microbiome: inferring large-scale spatio-temporal patterns of Syndiniales marine parasites
title_short Beyond the limits of the unassigned protist microbiome: inferring large-scale spatio-temporal patterns of Syndiniales marine parasites
title_sort beyond the limits of the unassigned protist microbiome inferring large scale spatio temporal patterns of syndiniales marine parasites
url https://doi.org/10.1038/s43705-022-00203-7
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