Acquisition of functions on the outer capsid surface during evolution of double-stranded RNA fungal viruses

Carlos P. Mata, Daniel Luque, Josué Gómez-Blanco, Javier M. Rodríguez, José M. González, Nobuhiro Suzuki, Said A. Ghabrial, José L. Carrascosa, Benes L. Trus, José R. Castón

Research output: Contribution to journalArticle

8 Citations (Scopus)

Abstract

Unlike their counterparts in bacterial and higher eukaryotic hosts, most fungal viruses are transmitted intracellularly and lack an extracellular phase. Here we determined the cryo-EM structure at 3.7 Å resolution of Rosellinia necatrix quadrivirus 1 (RnQV1), a fungal double-stranded (ds)RNA virus. RnQV1, the type species of the family Quadriviridae, has a multipartite genome consisting of four monocistronic segments. Whereas most dsRNA virus capsids are based on dimers of a single protein, the ~450-Å-diameter, T = 1 RnQV1 capsid is built of P2 and P4 protein heterodimers, each with more than 1000 residues. Despite a lack of sequence similarity between the two proteins, they have a similar α-helical domain, the structural signature shared with the lineage of the dsRNA bluetongue virus-like viruses. Domain insertions in P2 and P4 preferential sites provide additional functions at the capsid outer surface, probably related to enzyme activity. The P2 insertion has a fold similar to that of gelsolin and profilin, two actin-binding proteins with a function in cytoskeleton metabolism, whereas the P4 insertion suggests protease activity involved in cleavage of the P2 383-residue C-terminal region, absent in the mature viral particle. Our results indicate that the intimate virus-fungus partnership has altered the capsid genome-protective and/or receptor-binding functions. Fungal virus evolution has tended to allocate enzyme activities to the virus capsid outer surface.

Original languageEnglish
Article numbere1006755
JournalPLoS Pathogens
Volume13
Issue number12
DOIs
Publication statusPublished - Dec 1 2017

Fingerprint

Double-Stranded RNA
Capsid
RNA Viruses
Viruses
Fungal RNA
Profilins
Genome
Gelsolin
Bluetongue virus
Microfilament Proteins
Proteins
Enzymes
Cytoskeleton
Virion
Peptide Hydrolases
Fungi
Fungal Viruses

ASJC Scopus subject areas

  • Parasitology
  • Microbiology
  • Immunology
  • Molecular Biology
  • Genetics
  • Virology

Cite this

Mata, C. P., Luque, D., Gómez-Blanco, J., Rodríguez, J. M., González, J. M., Suzuki, N., ... Castón, J. R. (2017). Acquisition of functions on the outer capsid surface during evolution of double-stranded RNA fungal viruses. PLoS Pathogens, 13(12), [e1006755]. https://doi.org/10.1371/journal.ppat.1006755

Acquisition of functions on the outer capsid surface during evolution of double-stranded RNA fungal viruses. / Mata, Carlos P.; Luque, Daniel; Gómez-Blanco, Josué; Rodríguez, Javier M.; González, José M.; Suzuki, Nobuhiro; Ghabrial, Said A.; Carrascosa, José L.; Trus, Benes L.; Castón, José R.

In: PLoS Pathogens, Vol. 13, No. 12, e1006755, 01.12.2017.

Research output: Contribution to journalArticle

Mata, CP, Luque, D, Gómez-Blanco, J, Rodríguez, JM, González, JM, Suzuki, N, Ghabrial, SA, Carrascosa, JL, Trus, BL & Castón, JR 2017, 'Acquisition of functions on the outer capsid surface during evolution of double-stranded RNA fungal viruses', PLoS Pathogens, vol. 13, no. 12, e1006755. https://doi.org/10.1371/journal.ppat.1006755
Mata, Carlos P. ; Luque, Daniel ; Gómez-Blanco, Josué ; Rodríguez, Javier M. ; González, José M. ; Suzuki, Nobuhiro ; Ghabrial, Said A. ; Carrascosa, José L. ; Trus, Benes L. ; Castón, José R. / Acquisition of functions on the outer capsid surface during evolution of double-stranded RNA fungal viruses. In: PLoS Pathogens. 2017 ; Vol. 13, No. 12.
@article{b3fa601e83a1401495b5bc5775457f9e,
title = "Acquisition of functions on the outer capsid surface during evolution of double-stranded RNA fungal viruses",
abstract = "Unlike their counterparts in bacterial and higher eukaryotic hosts, most fungal viruses are transmitted intracellularly and lack an extracellular phase. Here we determined the cryo-EM structure at 3.7 {\AA} resolution of Rosellinia necatrix quadrivirus 1 (RnQV1), a fungal double-stranded (ds)RNA virus. RnQV1, the type species of the family Quadriviridae, has a multipartite genome consisting of four monocistronic segments. Whereas most dsRNA virus capsids are based on dimers of a single protein, the ~450-{\AA}-diameter, T = 1 RnQV1 capsid is built of P2 and P4 protein heterodimers, each with more than 1000 residues. Despite a lack of sequence similarity between the two proteins, they have a similar α-helical domain, the structural signature shared with the lineage of the dsRNA bluetongue virus-like viruses. Domain insertions in P2 and P4 preferential sites provide additional functions at the capsid outer surface, probably related to enzyme activity. The P2 insertion has a fold similar to that of gelsolin and profilin, two actin-binding proteins with a function in cytoskeleton metabolism, whereas the P4 insertion suggests protease activity involved in cleavage of the P2 383-residue C-terminal region, absent in the mature viral particle. Our results indicate that the intimate virus-fungus partnership has altered the capsid genome-protective and/or receptor-binding functions. Fungal virus evolution has tended to allocate enzyme activities to the virus capsid outer surface.",
author = "Mata, {Carlos P.} and Daniel Luque and Josu{\'e} G{\'o}mez-Blanco and Rodr{\'i}guez, {Javier M.} and Gonz{\'a}lez, {Jos{\'e} M.} and Nobuhiro Suzuki and Ghabrial, {Said A.} and Carrascosa, {Jos{\'e} L.} and Trus, {Benes L.} and Cast{\'o}n, {Jos{\'e} R.}",
year = "2017",
month = "12",
day = "1",
doi = "10.1371/journal.ppat.1006755",
language = "English",
volume = "13",
journal = "PLoS Pathogens",
issn = "1553-7366",
publisher = "Public Library of Science",
number = "12",

}

TY - JOUR

T1 - Acquisition of functions on the outer capsid surface during evolution of double-stranded RNA fungal viruses

AU - Mata, Carlos P.

AU - Luque, Daniel

AU - Gómez-Blanco, Josué

AU - Rodríguez, Javier M.

AU - González, José M.

AU - Suzuki, Nobuhiro

AU - Ghabrial, Said A.

AU - Carrascosa, José L.

AU - Trus, Benes L.

AU - Castón, José R.

PY - 2017/12/1

Y1 - 2017/12/1

N2 - Unlike their counterparts in bacterial and higher eukaryotic hosts, most fungal viruses are transmitted intracellularly and lack an extracellular phase. Here we determined the cryo-EM structure at 3.7 Å resolution of Rosellinia necatrix quadrivirus 1 (RnQV1), a fungal double-stranded (ds)RNA virus. RnQV1, the type species of the family Quadriviridae, has a multipartite genome consisting of four monocistronic segments. Whereas most dsRNA virus capsids are based on dimers of a single protein, the ~450-Å-diameter, T = 1 RnQV1 capsid is built of P2 and P4 protein heterodimers, each with more than 1000 residues. Despite a lack of sequence similarity between the two proteins, they have a similar α-helical domain, the structural signature shared with the lineage of the dsRNA bluetongue virus-like viruses. Domain insertions in P2 and P4 preferential sites provide additional functions at the capsid outer surface, probably related to enzyme activity. The P2 insertion has a fold similar to that of gelsolin and profilin, two actin-binding proteins with a function in cytoskeleton metabolism, whereas the P4 insertion suggests protease activity involved in cleavage of the P2 383-residue C-terminal region, absent in the mature viral particle. Our results indicate that the intimate virus-fungus partnership has altered the capsid genome-protective and/or receptor-binding functions. Fungal virus evolution has tended to allocate enzyme activities to the virus capsid outer surface.

AB - Unlike their counterparts in bacterial and higher eukaryotic hosts, most fungal viruses are transmitted intracellularly and lack an extracellular phase. Here we determined the cryo-EM structure at 3.7 Å resolution of Rosellinia necatrix quadrivirus 1 (RnQV1), a fungal double-stranded (ds)RNA virus. RnQV1, the type species of the family Quadriviridae, has a multipartite genome consisting of four monocistronic segments. Whereas most dsRNA virus capsids are based on dimers of a single protein, the ~450-Å-diameter, T = 1 RnQV1 capsid is built of P2 and P4 protein heterodimers, each with more than 1000 residues. Despite a lack of sequence similarity between the two proteins, they have a similar α-helical domain, the structural signature shared with the lineage of the dsRNA bluetongue virus-like viruses. Domain insertions in P2 and P4 preferential sites provide additional functions at the capsid outer surface, probably related to enzyme activity. The P2 insertion has a fold similar to that of gelsolin and profilin, two actin-binding proteins with a function in cytoskeleton metabolism, whereas the P4 insertion suggests protease activity involved in cleavage of the P2 383-residue C-terminal region, absent in the mature viral particle. Our results indicate that the intimate virus-fungus partnership has altered the capsid genome-protective and/or receptor-binding functions. Fungal virus evolution has tended to allocate enzyme activities to the virus capsid outer surface.

UR - http://www.scopus.com/inward/record.url?scp=85039907800&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85039907800&partnerID=8YFLogxK

U2 - 10.1371/journal.ppat.1006755

DO - 10.1371/journal.ppat.1006755

M3 - Article

VL - 13

JO - PLoS Pathogens

JF - PLoS Pathogens

SN - 1553-7366

IS - 12

M1 - e1006755

ER -