A New Freshwater Cyanosiphovirus Harboring Integrase

Pelagic cyanobacteria are key players in the functioning of aquatic ecosystems, and their viruses (cyanophages) potentially affect the abundance and composition of cyanobacterial communities. Yet, there are few well-described freshwater cyanophages relative to their marine counterparts, and in gener...

Full description

Bibliographic Details
Main Authors: Kevin Xu Zhong, Curtis A. Suttle, Anne-Claire Baudoux, Evelyne Derelle, Jonathan Colombet, Anna Cho, Jessica Caleta, Christophe Six, Stéphan Jacquet
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-09-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2018.02204/full
id doaj-3a4e1705ecbd43a28c414d96632f44f7
record_format Article
spelling doaj-3a4e1705ecbd43a28c414d96632f44f72020-11-25T01:05:21ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-09-01910.3389/fmicb.2018.02204357303A New Freshwater Cyanosiphovirus Harboring IntegraseKevin Xu Zhong0Kevin Xu Zhong1Curtis A. Suttle2Curtis A. Suttle3Curtis A. Suttle4Anne-Claire Baudoux5Evelyne Derelle6Jonathan Colombet7Anna Cho8Jessica Caleta9Christophe Six10Stéphan Jacquet11INRA, UMR 042 CARRTEL, Thonon-les-Bains, FranceDepartment of Earth, Ocean, and Atmospheric Sciences, University of British Columbia, Vancouver, BC, CanadaDepartment of Earth, Ocean, and Atmospheric Sciences, University of British Columbia, Vancouver, BC, CanadaDepartment of Microbiology and Immunology, University of British Columbia, Vancouver, BC, CanadaDepartment of Botany, Institute for Oceans and Fisheries, University of British Columbia, Vancouver, BC, CanadaSorbonne Universités UPMC Paris 06, CNRS, UMR7144 Adaptation et Diversité en Milieu Marin, Station Biologique de Roscoff, Roscoff, FranceIntegrative Marine Biology Laboratory (BIOM), CNRS UMR7232, Sorbonne Universities, Banyuls-sur-Mer, FranceCNRS, Université Blaise Pascal, UMR 6023, Laboratory of Microorganismes, Aubière, FranceDepartment of Microbiology and Immunology, University of British Columbia, Vancouver, BC, CanadaDepartment of Microbiology and Immunology, University of British Columbia, Vancouver, BC, CanadaSorbonne Universités UPMC Paris 06, CNRS, UMR7144 Adaptation et Diversité en Milieu Marin, Station Biologique de Roscoff, Roscoff, FranceINRA, UMR 042 CARRTEL, Thonon-les-Bains, FrancePelagic cyanobacteria are key players in the functioning of aquatic ecosystems, and their viruses (cyanophages) potentially affect the abundance and composition of cyanobacterial communities. Yet, there are few well-described freshwater cyanophages relative to their marine counterparts, and in general, few cyanosiphoviruses (family Siphoviridae) have been characterized, limiting our understanding of the biology and the ecology of this prominent group of viruses. Here, we characterize S-LBS1, a freshwater siphovirus lytic to a phycoerythrin-rich Synechococcus isolate (Strain TCC793). S-LBS1 has a narrow host range, a burst size of ∼400 and a relatively long infecting step before cell lysis occurs. It has a dsDNA 34,641 bp genome with putative genes for structure, DNA packing, lysis, replication, host interactions, DNA repair and metabolism. S-LBS1 is similar in genome size, genome architecture, and gene content, to previously described marine siphoviruses also infecting PE-rich Synechococcus, e.g., S-CBS1 and S-CBS3. However, unlike other Synechococcus phages, S-LBS1 encodes an integrase, suggesting its ability to establish lysogenic relationships with its host. Sequence recruitment from viral metagenomic data showed that S-LBS1-like viruses are diversely present in a wide range of aquatic environments, emphasizing their potential importance in controlling and structuring Synechococcus populations. A comparative analysis with 16 available sequenced cyanosiphoviruses reveals the absence of core genes within the genomes, suggesting high degree of genetic variability in siphoviruses infecting cyanobacteria. It is likely that cyanosiphoviruses have evolved as distinct evolutionary lineages and that adaptive co-evolution occurred between these viruses and their hosts (i.e., Synechococcus, Prochlorococcus, Nodularia, and Acaryochloris), constituting an important driving force for such phage diversification.https://www.frontiersin.org/article/10.3389/fmicb.2018.02204/fullfreshwaterlakesSynechococcuscyanosiphovirusgenome sequencing
collection DOAJ
language English
format Article
sources DOAJ
author Kevin Xu Zhong
Kevin Xu Zhong
Curtis A. Suttle
Curtis A. Suttle
Curtis A. Suttle
Anne-Claire Baudoux
Evelyne Derelle
Jonathan Colombet
Anna Cho
Jessica Caleta
Christophe Six
Stéphan Jacquet
spellingShingle Kevin Xu Zhong
Kevin Xu Zhong
Curtis A. Suttle
Curtis A. Suttle
Curtis A. Suttle
Anne-Claire Baudoux
Evelyne Derelle
Jonathan Colombet
Anna Cho
Jessica Caleta
Christophe Six
Stéphan Jacquet
A New Freshwater Cyanosiphovirus Harboring Integrase
Frontiers in Microbiology
freshwater
lakes
Synechococcus
cyanosiphovirus
genome sequencing
author_facet Kevin Xu Zhong
Kevin Xu Zhong
Curtis A. Suttle
Curtis A. Suttle
Curtis A. Suttle
Anne-Claire Baudoux
Evelyne Derelle
Jonathan Colombet
Anna Cho
Jessica Caleta
Christophe Six
Stéphan Jacquet
author_sort Kevin Xu Zhong
title A New Freshwater Cyanosiphovirus Harboring Integrase
title_short A New Freshwater Cyanosiphovirus Harboring Integrase
title_full A New Freshwater Cyanosiphovirus Harboring Integrase
title_fullStr A New Freshwater Cyanosiphovirus Harboring Integrase
title_full_unstemmed A New Freshwater Cyanosiphovirus Harboring Integrase
title_sort new freshwater cyanosiphovirus harboring integrase
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2018-09-01
description Pelagic cyanobacteria are key players in the functioning of aquatic ecosystems, and their viruses (cyanophages) potentially affect the abundance and composition of cyanobacterial communities. Yet, there are few well-described freshwater cyanophages relative to their marine counterparts, and in general, few cyanosiphoviruses (family Siphoviridae) have been characterized, limiting our understanding of the biology and the ecology of this prominent group of viruses. Here, we characterize S-LBS1, a freshwater siphovirus lytic to a phycoerythrin-rich Synechococcus isolate (Strain TCC793). S-LBS1 has a narrow host range, a burst size of ∼400 and a relatively long infecting step before cell lysis occurs. It has a dsDNA 34,641 bp genome with putative genes for structure, DNA packing, lysis, replication, host interactions, DNA repair and metabolism. S-LBS1 is similar in genome size, genome architecture, and gene content, to previously described marine siphoviruses also infecting PE-rich Synechococcus, e.g., S-CBS1 and S-CBS3. However, unlike other Synechococcus phages, S-LBS1 encodes an integrase, suggesting its ability to establish lysogenic relationships with its host. Sequence recruitment from viral metagenomic data showed that S-LBS1-like viruses are diversely present in a wide range of aquatic environments, emphasizing their potential importance in controlling and structuring Synechococcus populations. A comparative analysis with 16 available sequenced cyanosiphoviruses reveals the absence of core genes within the genomes, suggesting high degree of genetic variability in siphoviruses infecting cyanobacteria. It is likely that cyanosiphoviruses have evolved as distinct evolutionary lineages and that adaptive co-evolution occurred between these viruses and their hosts (i.e., Synechococcus, Prochlorococcus, Nodularia, and Acaryochloris), constituting an important driving force for such phage diversification.
topic freshwater
lakes
Synechococcus
cyanosiphovirus
genome sequencing
url https://www.frontiersin.org/article/10.3389/fmicb.2018.02204/full
work_keys_str_mv AT kevinxuzhong anewfreshwatercyanosiphovirusharboringintegrase
AT kevinxuzhong anewfreshwatercyanosiphovirusharboringintegrase
AT curtisasuttle anewfreshwatercyanosiphovirusharboringintegrase
AT curtisasuttle anewfreshwatercyanosiphovirusharboringintegrase
AT curtisasuttle anewfreshwatercyanosiphovirusharboringintegrase
AT anneclairebaudoux anewfreshwatercyanosiphovirusharboringintegrase
AT evelynederelle anewfreshwatercyanosiphovirusharboringintegrase
AT jonathancolombet anewfreshwatercyanosiphovirusharboringintegrase
AT annacho anewfreshwatercyanosiphovirusharboringintegrase
AT jessicacaleta anewfreshwatercyanosiphovirusharboringintegrase
AT christophesix anewfreshwatercyanosiphovirusharboringintegrase
AT stephanjacquet anewfreshwatercyanosiphovirusharboringintegrase
AT kevinxuzhong newfreshwatercyanosiphovirusharboringintegrase
AT kevinxuzhong newfreshwatercyanosiphovirusharboringintegrase
AT curtisasuttle newfreshwatercyanosiphovirusharboringintegrase
AT curtisasuttle newfreshwatercyanosiphovirusharboringintegrase
AT curtisasuttle newfreshwatercyanosiphovirusharboringintegrase
AT anneclairebaudoux newfreshwatercyanosiphovirusharboringintegrase
AT evelynederelle newfreshwatercyanosiphovirusharboringintegrase
AT jonathancolombet newfreshwatercyanosiphovirusharboringintegrase
AT annacho newfreshwatercyanosiphovirusharboringintegrase
AT jessicacaleta newfreshwatercyanosiphovirusharboringintegrase
AT christophesix newfreshwatercyanosiphovirusharboringintegrase
AT stephanjacquet newfreshwatercyanosiphovirusharboringintegrase
_version_ 1725194883184984064