High-resolution deep sequencing reveals biodiversity, population structure, and persistence of HIV-1 quasispecies within host ecosystems

Retrovirology

Maureen M Goodenow²  John W Sleasman³  William G Farmerie¹  Wilton B Williams²  Marco Salemi²  Brent P Gardner²  Amanda C Lowe²  Wei Hou⁴  Yijun Sun¹  Li Liu¹  Li Yin² 

[1] Interdisciplinary Center for Biotechnology Research, University of Florida, Gainesville, FL, USA;Department of Pathology, Immunology and Laboratory Medicine, College of Medicine, University of Florida, 2033 Mowry Road, PO Box 103633, Gainesville, FL, 32610-3633, USA;Department of Pediatrics, Division of Allergy, Immunology and Rheumatology, College of Medicine, University of South Florida, and All Children’s Hospital, St. Petersburg, FL, USA;Department of Epidemiology and Health Policy Research, College of Medicine and Department of Biostatistics, College of Public Health, University of Florida, Gainesville, FL, USA

关键词: Most recent common ancestor;    Founder virus persistence;    Pyrosequencing;    Fitness;    Quasispecies;    Population structure;    Biodiversity;    HIV-1 envelope V3;   

Others  :  1209216
DOI  :  10.1186/1742-4690-9-108

 received in 2012-10-25, accepted in 2012-11-20,  发布年份 2012

【 摘 要 】

Background

Deep sequencing provides the basis for analysis of biodiversity of taxonomically similar organisms in an environment. While extensively applied to microbiome studies, population genetics studies of viruses are limited. To define the scope of HIV-1 population biodiversity within infected individuals, a suite of phylogenetic and population genetic algorithms was applied to HIV-1 envelope hypervariable domain 3 (Env V3) within peripheral blood mononuclear cells from a group of perinatally HIV-1 subtype B infected, therapy-naïve children.

Results

Biodiversity of HIV-1 Env V3 quasispecies ranged from about 70 to 270 unique sequence clusters across individuals. Viral population structure was organized into a limited number of clusters that included the dominant variants combined with multiple clusters of low frequency variants. Next generation viral quasispecies evolved from low frequency variants at earlier time points through multiple non-synonymous changes in lineages within the evolutionary landscape. Minor V3 variants detected as long as four years after infection co-localized in phylogenetic reconstructions with early transmitting viruses or with subsequent plasma virus circulating two years later.

Conclusions

Deep sequencing defines HIV-1 population complexity and structure, reveals the ebb and flow of dominant and rare viral variants in the host ecosystem, and identifies an evolutionary record of low-frequency cell-associated viral V3 variants that persist for years. Bioinformatics pipeline developed for HIV-1 can be applied for biodiversity studies of virome populations in human, animal, or plant ecosystems.

【 授权许可】

   
2012 Yin et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】

• [1]Garcia-Arriaza J, Domingo E, Briones C: Characterization of minority subpopulations in the mutant spectrum of HIV-1 quasispecies by successive specific amplifications. Virus Res 2007, 129(2):123-134.
• [2]Paredes R, Clotet B: Clinical management of HIV-1 resistance. Antiviral Res 2010, 85(1):245-265.
• [3]Boutwell CL, Rolland MM, Herbeck JT, Mullins JI, Allen TM: Viral evolution and escape during acute HIV-1 infection. J Infect Dis 2010, 202(Suppl 2):S309-314.
• [4]Goodenow M, Huet T, Saurin W, Kwok S, Sninsky J, Wain-Hobson S: HIV-1 isolates are rapidly evolving quasispecies: evidence for viral mixtures and preferred nucleotide substitutions. J Acquir Immune Defic Syndr 1989, 2(4):344-352.
• [5]Lamers SL, Sleasman JW, She JX, Barrie KA, Pomeroy SM, Barrett DJ, Goodenow MM: Independent variation and positive selection in env V1 and V2 domains within maternal-infant strains of human immunodeficiency virus type 1 in vivo. J Virol 1993, 67(7):3951-3960.
• [6]Lamers SL, Sleasman JW, She JX, Barrie KA, Pomeroy SM, Barrett DJ, Goodenow MM: Persistence of multiple maternal genotypes of human immunodeficiency virus type I in infants infected by vertical transmission. J Clin Invest 1994, 93(1):380-390.
• [7]Nickle DC, Shriner D, Mittler JE, Frenkel LM, Mullins JI: Importance and detection of virus reservoirs and compartments of HIV infection. Curr Opin Microbiol 2003, 6(4):410-416.
• [8]Nowak MA, May RM, Anderson RM: The evolutionary dynamics of HIV-1 quasispecies and the development of immunodeficiency disease. AIDS 1990, 4(11):1095-1103.
• [9]Salemi M, Burkhardt BR, Gray RR, Ghaffari G, Sleasman JW, Goodenow MM: Phylodynamics of HIV-1 in lymphoid and non-lymphoid tissues reveals a central role for the thymus in emergence of CXCR4-using quasispecies. PLoS One 2007, 2(9):e950.
• [10]Simmonds P, Balfe P, Ludlam CA, Bishop JO, Brown AJ: Analysis of sequence diversity in hypervariable regions of the external glycoprotein of human immunodeficiency virus type 1. J Virol 1990, 64(12):5840-5850.
• [11]Wolinsky SM, Wike CM, Korber BT, Hutto C, Parks WP, Rosenblum LL, Kunstman KJ, Furtado MR, Munoz JL: Selective transmission of human immunodeficiency virus type-1 variants from mothers to infants. Science 1992, 255(5048):1134-1137.
• [12]Simen BB, Simons JF, Hullsiek KH, Novak RM, Macarthur RD, Baxter JD, Huang C, Lubeski C, Turenchalk GS, Braverman MS, Desany B, Rothberg JM, Egholm M, Kozal MJ: Low-abundance drug-resistant viral variants in chronically HIV-infected, antiretroviral treatment-naive patients significantly impact treatment outcomes. J Infect Dis 2009, 199(5):693-701.
• [13]Tsibris AM, Korber B, Arnaout R, Russ C, Lo CC, Leitner T, Gaschen B, Theiler J, Paredes R, Su Z, Hughes MD, Gulick RM, Greaves W, Coakley E, Flexner C, Nusbaum C, Kuritzkes DR: Quantitative deep sequencing reveals dynamic HIV-1 escape and large population shifts during CCR5 antagonist therapy in vivo. PLoS One 2009, 4(5):e5683.
• [14]Henn MR, Boutwell CL, Charlebois P, Lennon NJ, Power KA, Macalalad AR, Berlin AM, Malboeuf CM, Ryan EM, Gnerre S, Zody MC, Erlich RL, Green LM, Berical A, Wang Y, Casali M, Streeck H, Bloom AK, Dudek T, Tully D, Newman R, Axten KL, Gladden AD, Battis L, Kemper M, Zeng Q, Shea TP, Gujja S, Zedlack C, Gasser O, Brander C, Hess C, Gunthard HF, Brumme ZL, Brumme CJ, Bazner S, Rychert J, Tinsley JP, Mayer KH, Rosenberg E, Pereyra F, Levin JZ, Young SK, Jessen H, Altfeld M, Birren BW, Walker BD, Allen TM: Whole genome deep sequencing of HIV-1 reveals the impact of early minor variants upon immune recognition during acute infection. PLoS Pathog 2012, 8(3):e1002529.
• [15]Poon AF, Swenson LC, Dong WW, Deng W, Kosakovsky Pond SL, Brumme ZL, Mullins JI, Richman DD, Harrigan PR, Frost SD: Phylogenetic analysis of population-based and deep sequencing data to identify coevolving sites in the nef gene of HIV-1. Mol Biol Evol 2009, 27(4):819-832.
• [16]Eriksson N, Pachter L, Mitsuya Y, Rhee SY, Wang C, Gharizadeh B, Ronaghi M, Shafer RW, Beerenwinkel N: Viral population estimation using pyrosequencing. PLoS Comput Biol 2008, 4(4):e1000074.
• [17]Bimber BN, Burwitz BJ, O’Connor S, Detmer A, Gostick E, Lank SM, Price DA, Hughes A, O’Connor D: Ultradeep pyrosequencing detects complex patterns of CD8+ T-lymphocyte escape in simian immunodeficiency virus-infected macaques. J Virol 2009, 83(16):8247-8253.
• [18]Boyd SD, Marshall EL, Merker JD, Maniar JM, Zhang LN, Sahaf B, Jones CD, Simen BB, Hanczaruk B, Nguyen KD, Nadeau KC, Egholm M, Miklos DB, Zehnder JL, Fire AZ: Measurement and clinical monitoring of human lymphocyte clonality by massively parallel VDJ pyrosequencing. Sci Transl Med 2009, 1(12):12ra23.
• [19]Goodman AL, McNulty NP, Zhao Y, Leip D, Mitra RD, Lozupone CA, Knight R, Gordon JI: Identifying genetic determinants needed to establish a human gut symbiont in its habitat. Cell Host Microbe 2009, 6(3):279-289.
• [20]Hamady M, Knight R: Microbial community profiling for human microbiome projects: tools, techniques, and challenges. Genome Res 2009, 19(7):1141-1152.
• [21]Keijser BJ, Zaura E, Huse SM, van der Vossen JM, Schuren FH, Montijn RC, ten Cate JM, Crielaard W: Pyrosequencing analysis of the oral microflora of healthy adults. J Dent Res 2008, 87(11):1016-1020.
• [22]McCaig AE, Glover LA, Prosser JI: Molecular analysis of bacterial community structure and diversity in unimproved and improved upland grass pastures. Appl Environ Microbiol 1999, 65(4):1721-1730.
• [23]Schloss PD, Handelsman J: Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 2005, 71(3):1501-1506.
• [24]Sogin ML, Morrison HG, Huber JA, Mark WD, Huse SM, Neal PR, Arrieta JM, Herndl GJ: Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci U S A 2006, 103(32):12115-12120.
• [25]Sun Y, Cai Y, Liu L, Yu F, Farrell ML, McKendree W, Farmerie W: ESPRIT: estimating species richness using large collections of 16S rRNA pyrosequences. Nucleic Acids Res 2009, 37(10):e76.
• [26]Weinstein JA, Jiang N, White RA III, Fisher DS, Quake SR: High-throughput sequencing of the zebrafish antibody repertoire. Science 2009, 324(5928):807-810.
• [27]Campbell A: Save those molecules: molecular biodiversity and life. Journal of Applied Ecology 2003, 40(2):193-203.
• [28]Newton AC: Forest Ecology and preservation: A Handbook of Techniques. Oxford: Illustarted Edition edition; 1999.
• [29]Human Microbiome Project Consortium: Structure, function and diversity of the healthy human microbiome. Nature 2012, 486(7402):207-214.
• [30]Ho SK, Perez EE, Rose SL, Coman RM, Lowe AC, Hou W, Ma C, Lawrence RM, Dunn BM, Sleasman JW, Goodenow MM: Genetic determinants in HIV-1 Gag and Env V3 are related to viral response to combination antiretroviral therapy with a protease inhibitor. AIDS 2009, 23(13):1631-1640.
• [31]Rozera G, Abbate I, Bruselles A, Vlassi C, D’Offizi G, Narciso P, Chillemi G, Prosperi M, Ippolito G, Capobianchi MR: Massively parallel pyrosequencing highlights minority variants in the HIV-1 env quasispecies deriving from lymphomonocyte sub-populations. Retrovirology 2009, 6:15. BioMed Central Full Text
• [32]Domingo E, Holland JJ: RNA virus mutations and fitness for survival. Annu Rev Microbiol 1997, 51:151-178.
• [33]Eigen M: On the nature of virus quasispecies. Trends Microbiol 1996, 4(6):216-218.
• [34]Lauring AS, Andino R: Quasispecies theory and the behavior of RNA viruses. PLoS Pathog 2010, 6(7):e1001005.
• [35]Paladin FJ, Monzon OT, Tsuchie H, Aplasca MR, Learn GH Jr, Kurimura T: Genetic subtypes of HIV-1 in the Philippines. AIDS 1998, 12(3):291-300.
• [36]Los Alamos data base 2012. http://www.hiv.lanl.gov/content/index webcite.
• [37]Redd AD, Collinson-Streng AN, Chatziandreou N, Mullis CE, Laeyendecker O, Martens C, Ricklefs S, Kiwanuka N, Nyein PH, Lutalo T, Grabowski MK, Kong X, Manucci J, Sewankambo N, Wawer MJ, Gray RH, Porcella SF, Fauci AS, Sagar M, Serwadda D, Quinn TC: Previously transmitted HIV-1 strains are preferentially selected during subsequent sexual transmissions. J Infect Dis 2012, 206(9):1433-1442.
• [38]Coberley CR, Kohler JJ, Brown JN, Oshier JT, Baker HV, Popp MP, Sleasman JW, Goodenow MM: Impact on genetic networks in human macrophages by a CCR5 strain of human immunodeficiency virus type 1. J Virol 2004, 78(21):11477-11486.
• [39]Ghaffari G, Tuttle DL, Briggs D, Burkhardt BR, Bhatt D, Andiman WA, Sleasman JW, Goodenow MM: Complex determinants in human immunodeficiency virus type 1 envelope gp120 mediate CXCR4-dependent infection of macrophages. J Virol 2005, 79(21):13250-13261.
• [40]Schmidt HA, Strimmer K, Vingron M, von HA: TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 2002, 18(3):502-504.
• [41]Strimmer K, von Haeseler A: Likelihood-mapping: a simple method to visualize phylogenetic content of a sequence alignment. Proc Natl Acad Sci U S A 1997, 94:6815-6819.
• [42]Xia X, Xie Z, Salemi M, Chen L, Wang Y: An index of substitution saturation and its application. Mol Phylogenet Evol 2003, 26:1-7.
• [43]Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O: New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010, 59(3):307-321.
• [44]Swofford DSJ: Phylogeny inference based on parsimony and other methods with PAUP*. In The Phylogenetic Handbook-a Practical Approach to DNA and Protein Phylogeny. 2nd edition. Edited by Lemey P, Salemi M, Vandamme A-M. New York: Cambrige University Press; 2003:160-206.
• [45]Gray RR, Veras NM, Santos LA, Salemi M: Evolutionary characterization of the West Nile Virus complete genome. Mol Phylogenet Evol 2010, 56(1):195-200.
• [46]Veras NM, Gray RR, Brigido LF, Rodrigues R, Salemi M: High-resolution phylogenetics and phylogeography of human immunodeficiency virus type 1 subtype C epidemic in South America. J Gen Virol 2011, 92(Pt 7):1698-1709.
• [47]Yang Z: PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 1997, 13(5):555-556.