Isolation and characterization of metallosphaera turreted icosahedral virus, a founding member of a new family of archaeal viruses

Cassia Wagner; Vijay Reddy; Francisco Asturias; Maryam Khoshouei; John E. Johnson; Pilar Manrique; Jacob Munson-McGee; Wolfgang Baumeister; C. Martin Lawrence; Mark J. Younge

doi:10.1128/JVI.00925-17

Isolation and characterization of metallosphaera turreted icosahedral virus, a founding member of a new family of archaeal viruses

Cassia Wagner, Vijay Reddy, Francisco Asturias, Maryam Khoshouei, John E. Johnson, Pilar Manrique, Jacob Munson-McGee, Wolfgang Baumeister, C. Martin Lawrence, Mark J. Younge

Research output: Contribution to journal › Article › peer-review

20 Scopus citations

Abstract

Our understanding of archaeal virus diversity and structure is just beginning to emerge. Here we describe a new archaeal virus, tentatively named Metallosphaera turreted icosahedral virus (MTIV), that was isolated from an acidic hot spring in Yellowstone National Park, USA. Two strains of the virus were identified and were found to replicate in an archaeal host species closely related to Metallosphaera yellowstonensis. Each strain encodes a 9.8- to 9.9-kb linear double-stranded DNA (dsDNA) genome with large inverted terminal repeats. Each genome encodes 21 open reading frames (ORFs). The ORFs display high homology between the strains, but they are quite distinct from other known viral genes. The 70-nmdiameter virion is built on a T=28 icosahedral lattice. Both single particle cryoelectron microscopy and cryotomography reconstructions reveal an unusual structure that has 42 turret-like projections: 12 pentameric turrets positioned on the icosahedral 5-fold axes and 30 turrets with apparent hexameric symmetry positioned on the icosahedral 2-fold axes. Both the virion structural properties and the genome content support MTIV as the founding member of a new family of archaeal viruses.

Original language	English (US)
Article number	e00925-17
Journal	Journal of virology
Volume	91
Issue number	20
DOIs	https://doi.org/10.1128/JVI.00925-17
State	Published - Oct 1 2017
Externally published	Yes

Bibliographical note

Funding Information:
This work was supported by NSF grant DEB-4W4596 to M.J. Y., and it was performed under Yellowstone National Park research permit YELL-2016-SCI-5090. Funding was also provided by National Science Foundation, grant MCB-1413534, to C.M.L. The M. J. Murdock Charitable Trust also funded instrumentation on which cryo-electron microscopy was performed. Special thanks to Susan Brumfield for assistance with electron microscopy.

Publisher Copyright:
© 2017 American Society for Microbiology.

Keywords

Archaea
Archaeal virus
Crenarchaeal
Cryo-electron microscopy
Environmental virology
Extremophiles
Viruses in extreme environments

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10.1128/JVI.00925-17

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Wagner, C., Reddy, V., Asturias, F., Khoshouei, M., Johnson, J. E., Manrique, P., Munson-McGee, J., Baumeister, W., Lawrence, C. M., & Younge, M. J. (2017). Isolation and characterization of metallosphaera turreted icosahedral virus, a founding member of a new family of archaeal viruses. Journal of virology, 91(20), Article e00925-17. https://doi.org/10.1128/JVI.00925-17

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title = "Isolation and characterization of metallosphaera turreted icosahedral virus, a founding member of a new family of archaeal viruses",

abstract = "Our understanding of archaeal virus diversity and structure is just beginning to emerge. Here we describe a new archaeal virus, tentatively named Metallosphaera turreted icosahedral virus (MTIV), that was isolated from an acidic hot spring in Yellowstone National Park, USA. Two strains of the virus were identified and were found to replicate in an archaeal host species closely related to Metallosphaera yellowstonensis. Each strain encodes a 9.8- to 9.9-kb linear double-stranded DNA (dsDNA) genome with large inverted terminal repeats. Each genome encodes 21 open reading frames (ORFs). The ORFs display high homology between the strains, but they are quite distinct from other known viral genes. The 70-nmdiameter virion is built on a T=28 icosahedral lattice. Both single particle cryoelectron microscopy and cryotomography reconstructions reveal an unusual structure that has 42 turret-like projections: 12 pentameric turrets positioned on the icosahedral 5-fold axes and 30 turrets with apparent hexameric symmetry positioned on the icosahedral 2-fold axes. Both the virion structural properties and the genome content support MTIV as the founding member of a new family of archaeal viruses.",

keywords = "Archaea, Archaeal virus, Crenarchaeal, Cryo-electron microscopy, Environmental virology, Extremophiles, Viruses in extreme environments",

author = "Cassia Wagner and Vijay Reddy and Francisco Asturias and Maryam Khoshouei and Johnson, {John E.} and Pilar Manrique and Jacob Munson-McGee and Wolfgang Baumeister and Lawrence, {C. Martin} and Younge, {Mark J.}",

note = "Funding Information: This work was supported by NSF grant DEB-4W4596 to M.J. Y., and it was performed under Yellowstone National Park research permit YELL-2016-SCI-5090. Funding was also provided by National Science Foundation, grant MCB-1413534, to C.M.L. The M. J. Murdock Charitable Trust also funded instrumentation on which cryo-electron microscopy was performed. Special thanks to Susan Brumfield for assistance with electron microscopy. Publisher Copyright: {\textcopyright} 2017 American Society for Microbiology.",

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AU - Wagner, Cassia

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AU - Asturias, Francisco

AU - Khoshouei, Maryam

AU - Johnson, John E.

AU - Manrique, Pilar

AU - Munson-McGee, Jacob

AU - Baumeister, Wolfgang

AU - Lawrence, C. Martin

AU - Younge, Mark J.

N1 - Funding Information: This work was supported by NSF grant DEB-4W4596 to M.J. Y., and it was performed under Yellowstone National Park research permit YELL-2016-SCI-5090. Funding was also provided by National Science Foundation, grant MCB-1413534, to C.M.L. The M. J. Murdock Charitable Trust also funded instrumentation on which cryo-electron microscopy was performed. Special thanks to Susan Brumfield for assistance with electron microscopy. Publisher Copyright: © 2017 American Society for Microbiology.

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N2 - Our understanding of archaeal virus diversity and structure is just beginning to emerge. Here we describe a new archaeal virus, tentatively named Metallosphaera turreted icosahedral virus (MTIV), that was isolated from an acidic hot spring in Yellowstone National Park, USA. Two strains of the virus were identified and were found to replicate in an archaeal host species closely related to Metallosphaera yellowstonensis. Each strain encodes a 9.8- to 9.9-kb linear double-stranded DNA (dsDNA) genome with large inverted terminal repeats. Each genome encodes 21 open reading frames (ORFs). The ORFs display high homology between the strains, but they are quite distinct from other known viral genes. The 70-nmdiameter virion is built on a T=28 icosahedral lattice. Both single particle cryoelectron microscopy and cryotomography reconstructions reveal an unusual structure that has 42 turret-like projections: 12 pentameric turrets positioned on the icosahedral 5-fold axes and 30 turrets with apparent hexameric symmetry positioned on the icosahedral 2-fold axes. Both the virion structural properties and the genome content support MTIV as the founding member of a new family of archaeal viruses.

AB - Our understanding of archaeal virus diversity and structure is just beginning to emerge. Here we describe a new archaeal virus, tentatively named Metallosphaera turreted icosahedral virus (MTIV), that was isolated from an acidic hot spring in Yellowstone National Park, USA. Two strains of the virus were identified and were found to replicate in an archaeal host species closely related to Metallosphaera yellowstonensis. Each strain encodes a 9.8- to 9.9-kb linear double-stranded DNA (dsDNA) genome with large inverted terminal repeats. Each genome encodes 21 open reading frames (ORFs). The ORFs display high homology between the strains, but they are quite distinct from other known viral genes. The 70-nmdiameter virion is built on a T=28 icosahedral lattice. Both single particle cryoelectron microscopy and cryotomography reconstructions reveal an unusual structure that has 42 turret-like projections: 12 pentameric turrets positioned on the icosahedral 5-fold axes and 30 turrets with apparent hexameric symmetry positioned on the icosahedral 2-fold axes. Both the virion structural properties and the genome content support MTIV as the founding member of a new family of archaeal viruses.

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KW - Archaeal virus

KW - Crenarchaeal

KW - Cryo-electron microscopy

KW - Environmental virology

KW - Extremophiles

KW - Viruses in extreme environments

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SN - 0022-538X

VL - 91

JO - Journal of virology

JF - Journal of virology

IS - 20

M1 - e00925-17

ER -

Isolation and characterization of metallosphaera turreted icosahedral virus, a founding member of a new family of archaeal viruses

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