Host-Dependent Differences in Replication Strategy of the Sulfolobus Spindle-Shaped Virus Strain SSV9 (a.k.a., SSVK1): Infection Profiles in Hosts of the Family Sulfolobaceae

The Sulfolobus Spindle-shaped Virus (SSV) system has become a model for studying thermophilic virus biology, including archaeal host-virus interactions and biogeography. Several factors make the SSV system amenable to studying archaeal genetic mechanisms (e.g., CRISPRs) as well as virus-host interac...

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Main Authors: Ruben Michael Ceballos, Coyne Gareth Drummond, Carson Len Stacy, Elizabeth Padilla-Crespo, Kenneth Mark Stedman
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-07-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2020.01218/full
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author Ruben Michael Ceballos
Ruben Michael Ceballos
Ruben Michael Ceballos
Coyne Gareth Drummond
Carson Len Stacy
Elizabeth Padilla-Crespo
Kenneth Mark Stedman
author_facet Ruben Michael Ceballos
Ruben Michael Ceballos
Ruben Michael Ceballos
Coyne Gareth Drummond
Carson Len Stacy
Elizabeth Padilla-Crespo
Kenneth Mark Stedman
author_sort Ruben Michael Ceballos
collection DOAJ
description The Sulfolobus Spindle-shaped Virus (SSV) system has become a model for studying thermophilic virus biology, including archaeal host-virus interactions and biogeography. Several factors make the SSV system amenable to studying archaeal genetic mechanisms (e.g., CRISPRs) as well as virus-host interactions in high temperature acidic environments. Previously, we reported that SSVs exhibited differential infectivity on allopatric vs. sympatric hosts. We also noticed a wide host range for virus strain SSV9 (a.k.a., SSVK1). For decades, SSVs have been described as “non-lytic” double-stranded DNA viruses that infect species of the genus Sulfolobus and release virions via budding rather than host lysis. In this study, we show that SSVs infect hosts representing more than one genus of the family Sulfolobaceae in spot-on-lawn “halo” assays and in liquid culture infection assays. Growth curve analyses support the hypothesis that SSV9 virion release causes cell lysis. While SSV9 appears to lyse allopatric hosts, on a single sympatric host, SSV9 exhibits canonical non-lytic viral release historically reported SSVs. Therefore, the nature of SSV9 lytic-like behavior may be driven by allopatric evolution. The SSV9-infected host growth profile does not appear to be driven by multiplicity of infection (MOI). Greater stability of SSV9 vs. other SSVs (i.e., SSV1) in high temperature, low pH environments may contribute to higher transmission rates. However, neither higher transmission rate nor relative virulence in SSV9 infection seems to alter replication profile in susceptible hosts. Although it is known that CRISPR-Cas systems offer protection against viral infection in prokaryotes, CRISPRS are not reported to be a determinant of virus replication strategy. The mechanisms underlying SSV9 lytic-like behavior remain unknown and are the subject of ongoing investigations. These results suggest that genetic elements, potentially resulting from allopatric evolution, mediate distinct virus-host growth profiles of specific SSV-host strain pairings.
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spelling doaj.art-e418eea1150d4676be6cd158eccae0be2022-12-21T21:51:54ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-07-011110.3389/fmicb.2020.01218537440Host-Dependent Differences in Replication Strategy of the Sulfolobus Spindle-Shaped Virus Strain SSV9 (a.k.a., SSVK1): Infection Profiles in Hosts of the Family SulfolobaceaeRuben Michael Ceballos0Ruben Michael Ceballos1Ruben Michael Ceballos2Coyne Gareth Drummond3Carson Len Stacy4Elizabeth Padilla-Crespo5Kenneth Mark Stedman6Department of Biological Sciences, The University of Arkansas, Fayetteville, AR, United StatesArkansas Center for Space and Planetary Sciences, Fayetteville, AR, United StatesCell and Molecular Biology Program, The University of Arkansas, Fayetteville, AR, United StatesDepartmento de Ciencias y Tecnología, Universidad Interamericana de Puerto Rico, Aguadilla, PR, United StatesCell and Molecular Biology Program, The University of Arkansas, Fayetteville, AR, United StatesDepartmento de Ciencias y Tecnología, Universidad Interamericana de Puerto Rico, Aguadilla, PR, United StatesDepartment of Biology, Center for Life in Extreme Environments, Portland State University, Portland, OR, United StatesThe Sulfolobus Spindle-shaped Virus (SSV) system has become a model for studying thermophilic virus biology, including archaeal host-virus interactions and biogeography. Several factors make the SSV system amenable to studying archaeal genetic mechanisms (e.g., CRISPRs) as well as virus-host interactions in high temperature acidic environments. Previously, we reported that SSVs exhibited differential infectivity on allopatric vs. sympatric hosts. We also noticed a wide host range for virus strain SSV9 (a.k.a., SSVK1). For decades, SSVs have been described as “non-lytic” double-stranded DNA viruses that infect species of the genus Sulfolobus and release virions via budding rather than host lysis. In this study, we show that SSVs infect hosts representing more than one genus of the family Sulfolobaceae in spot-on-lawn “halo” assays and in liquid culture infection assays. Growth curve analyses support the hypothesis that SSV9 virion release causes cell lysis. While SSV9 appears to lyse allopatric hosts, on a single sympatric host, SSV9 exhibits canonical non-lytic viral release historically reported SSVs. Therefore, the nature of SSV9 lytic-like behavior may be driven by allopatric evolution. The SSV9-infected host growth profile does not appear to be driven by multiplicity of infection (MOI). Greater stability of SSV9 vs. other SSVs (i.e., SSV1) in high temperature, low pH environments may contribute to higher transmission rates. However, neither higher transmission rate nor relative virulence in SSV9 infection seems to alter replication profile in susceptible hosts. Although it is known that CRISPR-Cas systems offer protection against viral infection in prokaryotes, CRISPRS are not reported to be a determinant of virus replication strategy. The mechanisms underlying SSV9 lytic-like behavior remain unknown and are the subject of ongoing investigations. These results suggest that genetic elements, potentially resulting from allopatric evolution, mediate distinct virus-host growth profiles of specific SSV-host strain pairings.https://www.frontiersin.org/article/10.3389/fmicb.2020.01218/fullSulfolobus spindle-shaped viruslytic replicationallopatric evolutionsympatric coevolutionnon-lytic releaseSulfolobus
spellingShingle Ruben Michael Ceballos
Ruben Michael Ceballos
Ruben Michael Ceballos
Coyne Gareth Drummond
Carson Len Stacy
Elizabeth Padilla-Crespo
Kenneth Mark Stedman
Host-Dependent Differences in Replication Strategy of the Sulfolobus Spindle-Shaped Virus Strain SSV9 (a.k.a., SSVK1): Infection Profiles in Hosts of the Family Sulfolobaceae
Frontiers in Microbiology
Sulfolobus spindle-shaped virus
lytic replication
allopatric evolution
sympatric coevolution
non-lytic release
Sulfolobus
title Host-Dependent Differences in Replication Strategy of the Sulfolobus Spindle-Shaped Virus Strain SSV9 (a.k.a., SSVK1): Infection Profiles in Hosts of the Family Sulfolobaceae
title_full Host-Dependent Differences in Replication Strategy of the Sulfolobus Spindle-Shaped Virus Strain SSV9 (a.k.a., SSVK1): Infection Profiles in Hosts of the Family Sulfolobaceae
title_fullStr Host-Dependent Differences in Replication Strategy of the Sulfolobus Spindle-Shaped Virus Strain SSV9 (a.k.a., SSVK1): Infection Profiles in Hosts of the Family Sulfolobaceae
title_full_unstemmed Host-Dependent Differences in Replication Strategy of the Sulfolobus Spindle-Shaped Virus Strain SSV9 (a.k.a., SSVK1): Infection Profiles in Hosts of the Family Sulfolobaceae
title_short Host-Dependent Differences in Replication Strategy of the Sulfolobus Spindle-Shaped Virus Strain SSV9 (a.k.a., SSVK1): Infection Profiles in Hosts of the Family Sulfolobaceae
title_sort host dependent differences in replication strategy of the sulfolobus spindle shaped virus strain ssv9 a k a ssvk1 infection profiles in hosts of the family sulfolobaceae
topic Sulfolobus spindle-shaped virus
lytic replication
allopatric evolution
sympatric coevolution
non-lytic release
Sulfolobus
url https://www.frontiersin.org/article/10.3389/fmicb.2020.01218/full
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