Single Cell Genomics Reveals Viruses Consumed by Marine Protists

The predominant model of the role of viruses in the marine trophic web is that of the “viral shunt,” where viral infection funnels a substantial fraction of the microbial primary and secondary production back to the pool of dissolved organic matter. Here, we analyzed the composition of non-eukaryoti...

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Main Authors: Julia M. Brown, Jessica M. Labonté, Joseph Brown, Nicholas R. Record, Nicole J. Poulton, Michael E. Sieracki, Ramiro Logares, Ramunas Stepanauskas
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-09-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2020.524828/full
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author Julia M. Brown
Jessica M. Labonté
Joseph Brown
Nicholas R. Record
Nicole J. Poulton
Michael E. Sieracki
Ramiro Logares
Ramunas Stepanauskas
author_facet Julia M. Brown
Jessica M. Labonté
Joseph Brown
Nicholas R. Record
Nicole J. Poulton
Michael E. Sieracki
Ramiro Logares
Ramunas Stepanauskas
author_sort Julia M. Brown
collection DOAJ
description The predominant model of the role of viruses in the marine trophic web is that of the “viral shunt,” where viral infection funnels a substantial fraction of the microbial primary and secondary production back to the pool of dissolved organic matter. Here, we analyzed the composition of non-eukaryotic DNA associated with individual cells of small, planktonic protists in the Gulf of Maine (GoM) and the Mediterranean Sea. We found viral DNA associated with a substantial fraction cells from the GoM (51%) and the Mediterranean Sea (35%). While Mediterranean SAGs contained a larger proportion of cells containing bacterial sequences (49%), a smaller fraction of cells contained bacterial sequences in the GoM (19%). In GoM cells, nearly identical bacteriophage and ssDNA virus sequences where found across diverse lineages of protists, suggesting many of these viruses are non-infective. The fraction of cells containing viral DNA varied among protistan lineages and reached 100% in Picozoa and Choanozoa. These two groups also contained significantly higher numbers of viral sequences than other identified taxa. We consider mechanisms that may explain the presence of viral DNA in protistan cells and conclude that protistan predation on free viral particles contributed to the observed patterns. These findings confirm prior experiments with protistan isolates and indicate that the viral shunt is complemented by a viral link in the marine microbial food web. This link may constitute a sink of viral particles in the ocean and has implications for the flow of carbon through the microbial food web.
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spelling doaj.art-2dfa6aa616b148c6b063a46ca583f78c2022-12-21T23:55:12ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-09-011110.3389/fmicb.2020.524828524828Single Cell Genomics Reveals Viruses Consumed by Marine ProtistsJulia M. Brown0Jessica M. Labonté1Joseph Brown2Nicholas R. Record3Nicole J. Poulton4Michael E. Sieracki5Ramiro Logares6Ramunas Stepanauskas7Bigelow Laboratory for Ocean Sciences, East Boothbay, ME, United StatesDepartment of Marine Biology, Texas A&M University at Galveston, Galveston, TX, United StatesDepartment of Human Genetics, University of Utah, Salt Lake City, UT, United StatesBigelow Laboratory for Ocean Sciences, East Boothbay, ME, United StatesBigelow Laboratory for Ocean Sciences, East Boothbay, ME, United StatesDivision of Ocean Sciences, National Science Foundation, Alexandria, VA, United StatesInstitute of Marine Sciences (ICM), CSIC, Barcelona, SpainBigelow Laboratory for Ocean Sciences, East Boothbay, ME, United StatesThe predominant model of the role of viruses in the marine trophic web is that of the “viral shunt,” where viral infection funnels a substantial fraction of the microbial primary and secondary production back to the pool of dissolved organic matter. Here, we analyzed the composition of non-eukaryotic DNA associated with individual cells of small, planktonic protists in the Gulf of Maine (GoM) and the Mediterranean Sea. We found viral DNA associated with a substantial fraction cells from the GoM (51%) and the Mediterranean Sea (35%). While Mediterranean SAGs contained a larger proportion of cells containing bacterial sequences (49%), a smaller fraction of cells contained bacterial sequences in the GoM (19%). In GoM cells, nearly identical bacteriophage and ssDNA virus sequences where found across diverse lineages of protists, suggesting many of these viruses are non-infective. The fraction of cells containing viral DNA varied among protistan lineages and reached 100% in Picozoa and Choanozoa. These two groups also contained significantly higher numbers of viral sequences than other identified taxa. We consider mechanisms that may explain the presence of viral DNA in protistan cells and conclude that protistan predation on free viral particles contributed to the observed patterns. These findings confirm prior experiments with protistan isolates and indicate that the viral shunt is complemented by a viral link in the marine microbial food web. This link may constitute a sink of viral particles in the ocean and has implications for the flow of carbon through the microbial food web.https://www.frontiersin.org/article/10.3389/fmicb.2020.524828/fullnanoeukaryotemarine eukaryotevirusphagemicrobial ecologymarine food web
spellingShingle Julia M. Brown
Jessica M. Labonté
Joseph Brown
Nicholas R. Record
Nicole J. Poulton
Michael E. Sieracki
Ramiro Logares
Ramunas Stepanauskas
Single Cell Genomics Reveals Viruses Consumed by Marine Protists
Frontiers in Microbiology
nanoeukaryote
marine eukaryote
virus
phage
microbial ecology
marine food web
title Single Cell Genomics Reveals Viruses Consumed by Marine Protists
title_full Single Cell Genomics Reveals Viruses Consumed by Marine Protists
title_fullStr Single Cell Genomics Reveals Viruses Consumed by Marine Protists
title_full_unstemmed Single Cell Genomics Reveals Viruses Consumed by Marine Protists
title_short Single Cell Genomics Reveals Viruses Consumed by Marine Protists
title_sort single cell genomics reveals viruses consumed by marine protists
topic nanoeukaryote
marine eukaryote
virus
phage
microbial ecology
marine food web
url https://www.frontiersin.org/article/10.3389/fmicb.2020.524828/full
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