Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics

Abstract The persistent inertia in the ability to culture environmentally abundant microbes from aquatic ecosystems represents an obstacle in disentangling the complex web of ecological interactions spun by a diverse assortment of participants (pro- and eukaryotes and their viruses). In aquatic micr...

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Main Authors: Vinicius S. Kavagutti, Adrian-Ştefan Andrei, Maliheh Mehrshad, Michaela M. Salcher, Rohit Ghai
Format: Article
Language:English
Published: BMC 2019-10-01
Series:Microbiome
Online Access:http://link.springer.com/article/10.1186/s40168-019-0752-0
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author Vinicius S. Kavagutti
Adrian-Ştefan Andrei
Maliheh Mehrshad
Michaela M. Salcher
Rohit Ghai
author_facet Vinicius S. Kavagutti
Adrian-Ştefan Andrei
Maliheh Mehrshad
Michaela M. Salcher
Rohit Ghai
author_sort Vinicius S. Kavagutti
collection DOAJ
description Abstract The persistent inertia in the ability to culture environmentally abundant microbes from aquatic ecosystems represents an obstacle in disentangling the complex web of ecological interactions spun by a diverse assortment of participants (pro- and eukaryotes and their viruses). In aquatic microbial communities, the numerically most abundant actors, the viruses, remain the most elusive, and especially in freshwaters their identities and ecology remain unknown. Here, using ultra-deep metagenomic sequencing from pelagic freshwater habitats, we recovered complete genomes of > 2000 phages, including small “miniphages” and large “megaphages” infecting iconic freshwater prokaryotic lineages. For instance, abundant freshwater Actinobacteria support infection by a very broad size range of phages (13–200 Kb). We describe many phages encoding genes that likely afford protection to their host from reactive oxygen species (ROS) in the aquatic environment and in the oxidative burst in protist phagolysosomes (phage-mediated ROS defense). Spatiotemporal abundance analyses of phage genomes revealed evanescence as the primary dynamic in upper water layers, where they displayed short-lived existences. In contrast, persistence was characteristic for the deeper layers where many identical phage genomes were recovered repeatedly. Phage and host abundances corresponded closely, with distinct populations displaying preferential distributions in different seasons and depths, closely mimicking overall stratification and mixis.
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spelling doaj.art-ecb40dd656304d6cbcf3a94c8250304f2022-12-21T18:59:11ZengBMCMicrobiome2049-26182019-10-017111510.1186/s40168-019-0752-0Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomicsVinicius S. Kavagutti0Adrian-Ştefan Andrei1Maliheh Mehrshad2Michaela M. Salcher3Rohit Ghai4Department of Aquatic Microbial Ecology, Institute of Hydrobiology, Biology Centre of the Academy of Sciences of the Czech RepublicDepartment of Aquatic Microbial Ecology, Institute of Hydrobiology, Biology Centre of the Academy of Sciences of the Czech RepublicDepartment of Aquatic Microbial Ecology, Institute of Hydrobiology, Biology Centre of the Academy of Sciences of the Czech RepublicDepartment of Aquatic Microbial Ecology, Institute of Hydrobiology, Biology Centre of the Academy of Sciences of the Czech RepublicDepartment of Aquatic Microbial Ecology, Institute of Hydrobiology, Biology Centre of the Academy of Sciences of the Czech RepublicAbstract The persistent inertia in the ability to culture environmentally abundant microbes from aquatic ecosystems represents an obstacle in disentangling the complex web of ecological interactions spun by a diverse assortment of participants (pro- and eukaryotes and their viruses). In aquatic microbial communities, the numerically most abundant actors, the viruses, remain the most elusive, and especially in freshwaters their identities and ecology remain unknown. Here, using ultra-deep metagenomic sequencing from pelagic freshwater habitats, we recovered complete genomes of > 2000 phages, including small “miniphages” and large “megaphages” infecting iconic freshwater prokaryotic lineages. For instance, abundant freshwater Actinobacteria support infection by a very broad size range of phages (13–200 Kb). We describe many phages encoding genes that likely afford protection to their host from reactive oxygen species (ROS) in the aquatic environment and in the oxidative burst in protist phagolysosomes (phage-mediated ROS defense). Spatiotemporal abundance analyses of phage genomes revealed evanescence as the primary dynamic in upper water layers, where they displayed short-lived existences. In contrast, persistence was characteristic for the deeper layers where many identical phage genomes were recovered repeatedly. Phage and host abundances corresponded closely, with distinct populations displaying preferential distributions in different seasons and depths, closely mimicking overall stratification and mixis.http://link.springer.com/article/10.1186/s40168-019-0752-0
spellingShingle Vinicius S. Kavagutti
Adrian-Ştefan Andrei
Maliheh Mehrshad
Michaela M. Salcher
Rohit Ghai
Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics
Microbiome
title Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics
title_full Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics
title_fullStr Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics
title_full_unstemmed Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics
title_short Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics
title_sort phage centric ecological interactions in aquatic ecosystems revealed through ultra deep metagenomics
url http://link.springer.com/article/10.1186/s40168-019-0752-0
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AT malihehmehrshad phagecentricecologicalinteractionsinaquaticecosystemsrevealedthroughultradeepmetagenomics
AT michaelamsalcher phagecentricecologicalinteractionsinaquaticecosystemsrevealedthroughultradeepmetagenomics
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