Literature DB >> 27053548

Life Cycle Characterization of Sulfolobus Monocaudavirus 1, an Extremophilic Spindle-Shaped Virus with Extracellular Tail Development.

Kristine B Uldahl1, Signe B Jensen1, Yuvaraj Bhoobalan-Chitty1, Laura Martínez-Álvarez1, Pavlos Papathanasiou1, Xu Peng2.   

Abstract

UNLABELLED: We provide here, for the first time, insights into the initial infection stages of a large spindle-shaped archaeal virus and explore the following life cycle events. Our observations suggest that Sulfolobus monocaudavirus 1 (SMV1) exhibits a high adsorption rate and that virions adsorb to the host cells via three distinct attachment modes: nosecone association, body association, and body/tail association. In the body/tail association mode, the entire virion, including the tail(s), aligns to the host cell surface and the main body is greatly flattened, suggesting a possible fusion entry mechanism. Upon infection, the intracellular replication cycle lasts about 8 h, at which point the virions are released as spindle-shaped tailless particles. Replication of the virus retarded host growth but did not cause lysis of the host cells. Once released from the host and at temperatures resembling that of its natural habitat, SMV1 starts developing one or two tails. This exceptional property of undergoing a major morphological development outside, and independently of, the host cell has been reported only once before for the related Acidianus two-tailed virus. Here, we show that SMV1 can develop tails of more than 900 nm in length, more than quadrupling the total virion length. IMPORTANCE: Very little is known about the initial life cycle stages of viruses infecting hosts of the third domain of life, Archaea This work describes the first example of an archaeal virus employing three distinct association modes. The virus under study, Sulfolobus monocaudavirus 1, is a representative of the large spindle-shaped viruses that are frequently found in acidic hot springs. The results described here will add valuable knowledge about Archaea, the least studied domain in the virology field.
Copyright © 2016, American Society for Microbiology. All Rights Reserved.

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Year:  2016        PMID: 27053548      PMCID: PMC4886783          DOI: 10.1128/JVI.00075-16

Source DB:  PubMed          Journal:  J Virol        ISSN: 0022-538X            Impact factor:   5.103


  30 in total

1.  Global network of specific virus-host interactions in hypersaline environments.

Authors:  Nina S Atanasova; Elina Roine; Aharon Oren; Dennis H Bamford; Hanna M Oksanen
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2.  Structural and genomic properties of the hyperthermophilic archaeal virus ATV with an extracellular stage of the reproductive cycle.

Authors:  David Prangishvili; Gisle Vestergaard; Monika Häring; Ricardo Aramayo; Tamara Basta; Reinhard Rachel; Roger A Garrett
Journal:  J Mol Biol       Date:  2006-04-27       Impact factor: 5.469

3.  Comparative Metagenomics of Eight Geographically Remote Terrestrial Hot Springs.

Authors:  Peter Menzel; Sóley Ruth Gudbergsdóttir; Anne Gunn Rike; Lianbing Lin; Qi Zhang; Patrizia Contursi; Marco Moracci; Jakob K Kristjansson; Benjamin Bolduc; Sergey Gavrilov; Nikolai Ravin; Andrey Mardanov; Elizaveta Bonch-Osmolovskaya; Mark Young; Anders Krogh; Xu Peng
Journal:  Microb Ecol       Date:  2015-02-25       Impact factor: 4.552

4.  Sulfolobus tengchongensis spindle-shaped virus STSV1: virus-host interactions and genomic features.

Authors:  Xiaoyu Xiang; Lanming Chen; Xiaoxing Huang; Yuanmin Luo; Qunxin She; Li Huang
Journal:  J Virol       Date:  2005-07       Impact factor: 5.103

5.  Novel insights into gene regulation of the rudivirus SIRV2 infecting Sulfolobus cells.

Authors:  Ebru Okutan; Ling Deng; Saideh Mirlashari; Kristine Uldahl; Mayada Halim; Chao Liu; Roger A Garrett; Qunxin She; Xu Peng
Journal:  RNA Biol       Date:  2013-04-12       Impact factor: 4.652

6.  A unique virus release mechanism in the Archaea.

Authors:  Ariane Bize; Erik A Karlsson; Karin Ekefjärd; Tessa E F Quax; Mery Pina; Marie-Christine Prevost; Patrick Forterre; Olivier Tenaillon; Rolf Bernander; David Prangishvili
Journal:  Proc Natl Acad Sci U S A       Date:  2009-06-19       Impact factor: 11.205

Review 7.  Archaeal viruses and bacteriophages: comparisons and contrasts.

Authors:  Maija K Pietilä; Tatiana A Demina; Nina S Atanasova; Hanna M Oksanen; Dennis H Bamford
Journal:  Trends Microbiol       Date:  2014-03-16       Impact factor: 17.079

8.  Characterization of the Sulfolobus host-SSV2 virus interaction.

Authors:  Patrizia Contursi; Susanne Jensen; Tiziana Aucelli; Mosé Rossi; Simonetta Bartolucci; Qunxin She
Journal:  Extremophiles       Date:  2006-08-03       Impact factor: 3.035

9.  A genetic study of SSV1, the prototypical fusellovirus.

Authors:  Eric Iverson; Kenneth Stedman
Journal:  Front Microbiol       Date:  2012-06-05       Impact factor: 5.640

10.  Virus-induced dormancy in the archaeon Sulfolobus islandicus.

Authors:  Maria A Bautista; Changyi Zhang; Rachel J Whitaker
Journal:  MBio       Date:  2015-03-31       Impact factor: 7.867

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  13 in total

1.  Tolerance of Sulfolobus SMV1 virus to the immunity of I-A and III-B CRISPR-Cas systems in Sulfolobus islandicus.

Authors:  Tong Guo; Wenyuan Han; Qunxin She
Journal:  RNA Biol       Date:  2018-07-09       Impact factor: 4.652

2.  A Novel Type of Polyhedral Viruses Infecting Hyperthermophilic Archaea.

Authors:  Ying Liu; Sonoko Ishino; Yoshizumi Ishino; Gérard Pehau-Arnaudet; Mart Krupovic; David Prangishvili
Journal:  J Virol       Date:  2017-06-09       Impact factor: 5.103

3.  Interaction of extremophilic archaeal viruses with human and mouse complement system and viral biodistribution in mice.

Authors:  Linping Wu; Kristine Buch Uldahl; Fangfang Chen; Halli Benasutti; Deborah Logvinski; Vivian Vu; Nirmal K Banda; Xu Peng; Dmitri Simberg; Seyed Moein Moghimi
Journal:  Mol Immunol       Date:  2017-08-30       Impact factor: 4.407

Review 4.  The enigmatic archaeal virosphere.

Authors:  David Prangishvili; Dennis H Bamford; Patrick Forterre; Jaime Iranzo; Eugene V Koonin; Mart Krupovic
Journal:  Nat Rev Microbiol       Date:  2017-11-10       Impact factor: 60.633

5.  Microhomology-Mediated High-Throughput Gene Inactivation Strategy for the Hyperthermophilic Crenarchaeon Sulfolobus islandicus.

Authors:  Changyi Zhang; Rachel J Whitaker
Journal:  Appl Environ Microbiol       Date:  2017-12-15       Impact factor: 4.792

6.  Structural studies of Acidianus tailed spindle virus reveal a structural paradigm used in the assembly of spindle-shaped viruses.

Authors:  Rebecca Hochstein; Daniel Bollschweiler; Sanjay Dharmavaram; Nathanael G Lintner; Jürgen M Plitzko; Robijn Bruinsma; Harald Engelhardt; Mark J Young; William S Klug; C Martin Lawrence
Journal:  Proc Natl Acad Sci U S A       Date:  2018-02-12       Impact factor: 11.205

7.  SMV1, an extremely stable thermophilic virus platform for nanoparticle trafficking in the mammalian GI tract.

Authors:  K B Uldahl; S T Walk; S C Olshefsky; M J Young; X Peng
Journal:  J Appl Microbiol       Date:  2017-10-10       Impact factor: 3.772

8.  Spindle-shaped archaeal viruses evolved from rod-shaped ancestors to package a larger genome.

Authors:  Fengbin Wang; Virginija Cvirkaite-Krupovic; Matthijn Vos; Leticia C Beltran; Mark A B Kreutzberger; Jean-Marie Winter; Zhangli Su; Jun Liu; Stefan Schouten; Mart Krupovic; Edward H Egelman
Journal:  Cell       Date:  2022-03-23       Impact factor: 66.850

9.  A filamentous archaeal virus is enveloped inside the cell and released through pyramidal portals.

Authors:  Diana P Baquero; Anastasia D Gazi; Martin Sachse; Junfeng Liu; Christine Schmitt; Maryse Moya-Nilges; Stefan Schouten; David Prangishvili; Mart Krupovic
Journal:  Proc Natl Acad Sci U S A       Date:  2021-08-10       Impact factor: 11.205

10.  The biology of thermoacidophilic archaea from the order Sulfolobales.

Authors:  April M Lewis; Alejandra Recalde; Christopher Bräsen; James A Counts; Phillip Nussbaum; Jan Bost; Larissa Schocke; Lu Shen; Daniel J Willard; Tessa E F Quax; Eveline Peeters; Bettina Siebers; Sonja-Verena Albers; Robert M Kelly
Journal:  FEMS Microbiol Rev       Date:  2021-08-17       Impact factor: 16.408

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