Abstract
The Microviridae are increasingly becoming recognized as one of the most globally ubiquitous and highly diverse virus families, and as such, provide an advantageous model for studying virus evolution and adaptation. Here, we utilize microvirus sequences from diverse physiochemical environments, including novel sequences from a high-temperature acidic lake, to chart the outcome of natural selection in the main structural protein of the virus. Each icosahedral microvirus virion is composed of sixty identical capsid proteins that interact along twofold, threefold and fivefold symmetry axis interfaces to encapsidate a small, circular, single-stranded DNA genome. Viable assembly of the virus is guided by scaffolding proteins, which coordinate inter-subunit contacts between the capsid proteins. Structure-based analysis indicates that amino acid sequence conservation is predominantly localized to the twofold axis interface. While preservation of this quaternary interface appears to be essential, tertiary and secondary structural features of the capsid protein are permissive to considerable sequence variation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abrescia NG, Bamford DH, Grimes JM, Stuart DI (2012) Structure unifies the viral universe. Annu Rev Biochem 81:795
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389
Arai N, Kornberg A (1981) Rep protein as a helicase in an active, isolatable replication fork of duplex phi X174 DNA. J Biol Chem 256:5294
Bamford DH, Burnett RM, Stuart DI (2002) Evolution of viral structure. Theor Popul Biol 61:461
Brentlinger KL, Hafenstein S, Novak CR, Fane BA, Borgon R, McKenna R, Agbandje-McKenna M (2002) Microviridae, a family divided: isolation, characterization, and genome sequence of phiMH2K, a bacteriophage of the obligate intracellular parasitic bacterium Bdellovibrio bacteriovorus. J Bacteriol 184:1089
Bryson V, Vogel HJ, University Rutgers, Rutgers University. Institute of Microbiology (1965) Evolving genes and proteins; a symposium held at the Institute of Microbiology of Rutgers, with support from the National Science Foundation. Academic Press, New York
Cherwa JE, Organtini LJ, Ashley RE, Hafenstein SL, Fane BA (2011) In vitro assembly of the øX174 procapsid from external scaffolding protein oligomers and early pentameric assembly intermediates. J Mol Biol 412:387
Chipman PR, Agbandje-McKenna M, Renaudin J, Baker TS, McKenna R (1998) Structural analysis of the Spiroplasma virus, SpV4: implications for evolutionary variation to obtain host diversity among the Microviridae. Structure 6:135
Clarke IN, Cutcliffe LT, Everson JS, Garner SA, Lambden PR, Pead PJ, Pickett MA, Brentlinger KL, Fane BA (2004) Chlamydiaphage Chp2, a skeleton in the phiX174 closet: scaffolding protein and procapsid identification. J Bacteriol 186:7571
Cuevas JM, Duffy S, Sanjuán R (2009) Point mutation rate of bacteriophage PhiX174. Genetics 183:747
Diemer GS, Stedman KM (2012) A novel virus genome discovered in an extreme environment suggests recombination between unrelated groups of RNA and DNA viruses. Biol Direct 7:13
Dokland T, McKenna R, Ilag LL, Bowman BR, Incardona NL, Fane BA, Rossmann MG (1997) Structure of a viral procapsid with molecular scaffolding. Nature 389:308
Duffy S, Shackelton LA, Holmes EC (2008) Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 9:267
Fane B, Brentlinger K, Burch A, Chen M, Hafenstein S, Moore E, Novak C, Uchiyama A (2006) The microviridae. In: Calendar R, Abedon ST (eds) The Bacteriophages. Oxford University Press, New York, pp 129–145
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368
Garner SA, Everson JS, Lambden PR, Fane BA, Clarke IN (2004) Isolation, molecular characterisation and genome sequence of a bacteriophage (Chp3) from Chlamydophila pecorum. Virus Genes 28:207
Hopkins M, Kailasan S, Cohen A, Roux S, Tucker KP, Shevenell A, Agbandje-McKenna M, Breitbart M (2014) Diversity of environmental single-stranded DNA phages revealed by PCR amplification of the partial major capsid protein. ISME J 8:2093
Humphrey W, Dalke A, Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph 14:33
Jazwinski SM, Kornberg A (1975) DNA replication in vitro starting with an intact phiX174 phage. Proc Natl Acad Sci USA 72:3863
Khayat R, Tang L, Larson ET, Lawrence CM, Young M, Johnson JE (2005) Structure of an archaeal virus capsid protein reveals a common ancestry to eukaryotic and bacterial viruses. Proc Natl Acad Sci USA 102:18944
Kosakovsky Pond SL, Frost SD (2005) Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22:1208
Krupovic M, Forterre P (2011) Microviridae goes temperate: microvirus-related proviruses reside in the genomes of Bacteroidetes. PLoS ONE 6:e19893
Labonté JM, Suttle CA (2013) Metagenomic and whole-genome analysis reveals new lineages of gokushoviruses and biogeographic separation in the sea. Front Microbiol 4:404
Labonté JM, Hallam SJ, Suttle CA (2015) Previously unknown evolutionary groups dominate the ssDNA gokushoviruses in oxic and anoxic waters of a coastal marine environment. Front Microbiol 6:315
Liu Y, Bahar I (2012) Sequence evolution correlates with structural dynamics. Mol Biol Evol 29:2253
McKenna R, Xia D, Willingmann P, Ilag LL, Krishnaswamy S, Rossmann MG, Olson NH, Baker TS, Incardona NL (1992) Atomic structure of single-stranded DNA bacteriophage phi X174 and its functional implications. Nature 355:137
McKenna R, Ilag LL, Rossmann MG (1994) Analysis of the single-stranded DNA bacteriophage phi X174, refined at a resolution of 3.0 A. J Mol Biol 237:517
McMacken R, Kornberg A (1978) A multienzyme system for priming the replication of phiX174 viral DNA. J Biol Chem 253:3313
Morais MC, Fisher M, Kanamaru S, Przybyla L, Burgner J, Fane BA, Rossmann MG (2004) Conformational switching by the scaffolding protein D directs the assembly of bacteriophage phiX174. Mol Cell 15:991
Needleman SB, Wunsch CD (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 48:443
Pei J, Grishin NV (2001) AL2CO: calculation of positional conservation in a protein sequence alignment. Bioinformatics 17:700
Pei J, Tang M, Grishin NV (2008) PROMALS3D web server for accurate multiple protein sequence and structure alignments. Nucleic Acids Res 36:W30
Petersen TN, Nielsen M, Lundegaard C, Lund O (2010) CPHmodels-3.0-remote homology modeling using structure-guided sequence profiles. Nucleic Acids Res 38:W576
Pond SL, Frost SD, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676
Poon A, Chao L (2005) The rate of compensatory mutation in the DNA bacteriophage phiX174. Genetics 170:989
Prevelige P, Fane B (2012) Building the machines: scaffolding protein functions during bacteriophage morphogenesis. Adv Exp Med Biol 726:325
Roberts E, Eargle J, Wright D, Luthey-Schulten Z (2006) MultiSeq: unifying sequence and structure data for evolutionary analysis. BMC Bioinformatics 7:382
Rosario K, Dayaram A, Marinov M, Ware J, Kraberger S, Stainton D, Breitbart M, Varsani A (2012) Diverse circular ssDNA viruses discovered in dragonflies (Odonata: Epiprocta). J Gen Virol 93:2668
Roux S, Enault F, Robin A, Ravet V, Personnic S, Theil S, Colombet J, Sime-Ngando T, Debroas D (2012a) Assessing the diversity and specificity of two freshwater viral communities through metagenomics. PLoS ONE 7:e33641
Roux S, Krupovic M, Poulet A, Debroas D, Enault F (2012b) Evolution and diversity of the Microviridae viral family through a collection of 81 new complete genomes assembled from virome reads. PLoS ONE 7:e40418
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406
Sanger F, Air GM, Barrell BG, Brown NL, Coulson AR, Fiddes CA, Hutchison CA, Slocombe PM, Smith M (1977) Nucleotide sequence of bacteriophage phi X174 DNA. Nature 265:687
Siering PL, Wolfe GV, Wilson MS, Yip AN, Carey CM, Wardman CD, Shapiro RS, Stedman KM, Kyle J, Yuan T, Van Nostrand JD, He Z, Zhou J (2013) Microbial biogeochemistry of Boiling Springs Lake: a physically dynamic, oligotrophic, low-pH geothermal ecosystem. Geobiology 11:356
Suzuki Y, Gojobori T (1999) A method for detecting positive selection at single amino acid sites. Mol Biol Evol 16:1315
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725
Tucker KP, Parsons R, Symonds EM, Breitbart M (2011) Diversity and distribution of single-stranded DNA phages in the North Atlantic Ocean. ISME J 5:822
Wernersson R, Pedersen AG (2003) RevTrans: multiple alignment of coding DNA from aligned amino acid sequences. Nucleic Acids Res 31:3537
Yooseph S, Sutton G, Rusch DB, Halpern AL, Williamson SJ, Remington K, Eisen JA, Heidelberg KB, Manning G, Li W, Jaroszewski L, Cieplak P, Miller CS, Li H, Mashiyama ST, Joachimiak MP, van Belle C, Chandonia JM, Soergel DA, Zhai Y, Natarajan K, Lee S, Raphael BJ, Bafna V, Friedman R, Brenner SE, Godzik A, Eisenberg D, Dixon JE, Taylor SS, Strausberg RL, Frazier M, Venter JC (2007) The Sorcerer II Global Ocean Sampling expedition: expanding the universe of protein families. PLoS Biol 5:e16
Acknowledgments
Two gokushovirus sequences used in this study were identified from a metagenomic survey of Boiling Springs Lake, located in Lassen Volcanic National Park, USA. Samples were acquired with a research permit from the National Park Service (LAVO-2008-SCI-0030), as part of the Boiling Springs Lake Microbial Observatory project supported by the National Science Foundation Grant MCB0702020 to K.M.S. Metagenomic sequencing of the Boiling Springs Lake phage samples (GAIR4 and GNX3R) was funded in part by the Gordon and Betty Moore Foundation through a Grant to the Broad Institute. Additional funding was provided by Portland State University. Thanks also to anonymous reviewers whose comments greatly improved the manuscript.
Funding
This study was funded by the National Science Foundation (Grant Number MCB0702020). Metagenomic sequencing of the Boiling Springs Lake phage samples (GAIR4 and GNX3R) was funded in part by the Gordon and Betty Moore Foundation through a Grant to the Broad Institute. Both G.S.D. and K.M.S were partially supported by funding from Portland State University.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Diemer, G.S., Stedman, K.M. Modeling Microvirus Capsid Protein Evolution Utilizing Metagenomic Sequence Data. J Mol Evol 83, 38–49 (2016). https://doi.org/10.1007/s00239-016-9751-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00239-016-9751-y