1932

Abstract

Viral metagenomics has expanded our knowledge of the ecology of uncultured viruses, within both environmental (e.g., terrestrial and aquatic) and host-associated (e.g., plants and animals, including humans) contexts. Here, we emphasize the implementation of an ecological framework in viral metagenomic studies to address questions in virology rarely considered ecological, which can change our perception of viruses and how they interact with their surroundings. An ecological framework explicitly considers diverse variants of viruses in populations that make up communities of interacting viruses, with ecosystem-level effects. It provides a structure for the study of the diversity, distributions, dynamics, and interactions of viruses with one another, hosts, and the ecosystem, including interactions with abiotic factors. An ecological framework in viral metagenomics stands poised to broadly expand our knowledge in basic and applied virology. We highlight specific fundamental research needs to capitalize on its potential and advance the field.

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2021-09-29
2024-10-03
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Literature Cited

  1. 1. 
    Roux S, Paez-Espino D, Chen IA, Palaniappan K, Ratner A et al. 2020. IMG/VR v3: an integrated ecological and evolutionary framework for interrogating genomes of uncultivated viruses. Nucleic Acids Res 49:D764–75
    [Google Scholar]
  2. 2. 
    Shi M, Lin XD, Tian JH, Chen LJ, Chen X et al. 2016. Redefining the invertebrate RNA virosphere. Nature 540:539–43
    [Google Scholar]
  3. 3. 
    Tisza MJ, Pastrana DV, Welch NL, Stewart B, Peretti A et al. 2020. Discovery of several thousand highly diverse circular DNA viruses. eLife 9:e51971
    [Google Scholar]
  4. 4. 
    Breitbart M, Salamon P, Andresen B, Mahaffy JM, Segall AM et al. 2002. Genomic analysis of uncultured marine viral communities. PNAS 99:14250–55
    [Google Scholar]
  5. 5. 
    Brum JR, Ignacio-Espinoza JC, Roux S, Doulcier G, Acinas SG et al. 2015. Patterns and ecological drivers of ocean viral communities. Science 348:1261498
    [Google Scholar]
  6. 6. 
    Paez-Espino D, Eloe-Fadrosh EA, Pavlopoulos GA, Thomas AD, Huntemann M et al. 2016. Uncovering Earth's virome. Nature 536:425–30
    [Google Scholar]
  7. 7. 
    Emerson JB, Roux S, Brum JR, Bolduc B, Woodcroft BJ et al. 2018. Host-linked soil viral ecology along a permafrost thaw gradient. Nat. Microbiol. 3:870–80
    [Google Scholar]
  8. 8. 
    Zhong ZP, Rapp JZ, Wainaina JM, Solonenko NE, Maughan H et al. 2020. Viral ecogenomics of arctic cryopeg brine and sea ice. mSystems 5:e00246-20
    [Google Scholar]
  9. 9. 
    Bellas CM, Schroeder DC, Edwards A, Barker G, Anesio AM. 2020. Flexible genes establish widespread bacteriophage pan-genomes in cryoconite hole ecosystems. Nat. Commun. 11:4403
    [Google Scholar]
  10. 10. 
    Trubl G, Jang HB, Roux S, Emerson JB, Solonenko N et al. 2018. Soil viruses are underexplored players in ecosystem carbon processing. mSystems 3:e00076-18
    [Google Scholar]
  11. 11. 
    Gregory AC, Zayed AA, Conceicao-Neto N, Temperton B, Bolduc B et al. 2019. Marine DNA viral macro- and microdiversity from pole to pole. Cell 177:1109–23.e14
    [Google Scholar]
  12. 12. 
    Rosenwasser S, Ziv C, Creveld SGV, Vardi A. 2016. Virocell metabolism: metabolic innovations during host-virus interactions in the ocean. Trends Microbiol 24:821–32
    [Google Scholar]
  13. 13. 
    Zimmerman AE, Howard-Varona C, Needham DM, John SG, Worden AZ et al. 2020. Metabolic and biogeochemical consequences of viral infection in aquatic ecosystems. Nat. Rev. Microbiol. 18:21–34
    [Google Scholar]
  14. 14. 
    Fuchsman CA, Palevsky HI, Widner B, Duffy M, Carlson MCG et al. 2019. Cyanobacteria and cyanophage contributions to carbon and nitrogen cycling in an oligotrophic oxygen-deficient zone. ISME J 13:2714–26
    [Google Scholar]
  15. 15. 
    Secor PR, Sweere JM, Michaels LA, Malkovskiy AV, Lazzareschi D et al. 2015. Filamentous bacteriophage promote biofilm assembly and function. Cell Host Microbe 18:549–59
    [Google Scholar]
  16. 16. 
    Chatterjee A, Willett JLE, Dunny GM, Duerkop BA. 2021. Phage infection and sub-lethal antibiotic exposure mediate Enterococcus faecalis type VII secretion system dependent inhibition of bystander bacteria. PLOS Genet 17:e1009204
    [Google Scholar]
  17. 17. 
    Díaz-Muñoz SL. 2019. Uncovering virus-virus interactions by unifying approaches and harnessing high-throughput tools. mSystems 4:3e00121-19
    [Google Scholar]
  18. 18. 
    Munson-McGee JH, Peng S, Dewerff S, Stepanauskas R, Whitaker RJ et al. 2018. A virus or more in (nearly) every cell: ubiquitous networks of virus-host interactions in extreme environments. ISME J 12:1706–14
    [Google Scholar]
  19. 19. 
    Temmam S, Chretien D, Bigot T, Dufour E, Petres S et al. 2019. Monitoring silent spillovers before emergence: a pilot study at the tick/human interface in Thailand. Front. Microbiol. 10:2315
    [Google Scholar]
  20. 20. 
    Plowright RK, Parrish CR, McCallum H, Hudson PJ, Ko AI et al. 2017. Pathways to zoonotic spillover. Nat. Rev. Microbiol. 15:502–10
    [Google Scholar]
  21. 21. 
    Duerkop BA, Hooper LV. 2013. Resident viruses and their interactions with the immune system. Nat. Immunol. 14:654–59
    [Google Scholar]
  22. 22. 
    Rascovan N, Duraisamy R, Desnues C. 2016. Metagenomics and the human virome in asymptomatic individuals. Annu. Rev. Microbiol. 70:125–41
    [Google Scholar]
  23. 23. 
    Koonin EV, Yutin N. 2020. The crAss-like phage group: how metagenomics reshaped the human virome. Trends Microbiol 28:349–59
    [Google Scholar]
  24. 24. 
    Creasy A, Rosario K, Leigh BA, Dishaw LJ, Breitbart M. 2018. Unprecedented diversity of ssDNA phages from the family Microviridae detected within the gut of a protochordate model organism (Ciona robusta). Viruses 10:8404
    [Google Scholar]
  25. 25. 
    Dutilh BE, Cassman N, McNair K, Sanchez SE, Silva GG et al. 2014. A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes. Nat. Commun. 5:4498
    [Google Scholar]
  26. 26. 
    Abt MC, Buffie CG, Susac B, Becattini S, Carter RA et al. 2016. TLR-7 activation enhances IL-22-mediated colonization resistance against vancomycin-resistant enterococcus. Sci. Transl. Med. 8:327ra25
    [Google Scholar]
  27. 27. 
    Ott SJ, Waetzig GH, Rehman A, Moltzau-Anderson J, Bharti R et al. 2017. Efficacy of sterile fecal filtrate transfer for treating patients with Clostridium difficile infection. Gastroenterology 152:799–811.e7
    [Google Scholar]
  28. 28. 
    Monaco CL, Gootenberg DB, Zhao G, Handley SA, Ghebremichael MS et al. 2016. Altered virome and bacterial microbiome in human immunodeficiency virus-associated acquired immunodeficiency syndrome. Cell Host Microbe 19:311–22
    [Google Scholar]
  29. 29. 
    Lysholm F, Wetterbom A, Lindau C, Darban H, Bjerkner A et al. 2012. Characterization of the viral microbiome in patients with severe lower respiratory tract infections, using metagenomic sequencing. PLOS ONE 7:e30875
    [Google Scholar]
  30. 30. 
    Willner D, Furlan M, Haynes M, Schmieder R, Angly FE et al. 2009. Metagenomic analysis of respiratory tract DNA viral communities in cystic fibrosis and non-cystic fibrosis individuals. PLOS ONE 4:e7370
    [Google Scholar]
  31. 31. 
    Reyes A, Haynes M, Hanson N, Angly FE, Heath AC et al. 2010. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466:334–38
    [Google Scholar]
  32. 32. 
    Minot S, Sinha R, Chen J, Li H, Keilbaugh SA et al. 2011. The human gut virome: inter-individual variation and dynamic response to diet. Genome Res 21:1616–25
    [Google Scholar]
  33. 33. 
    Pride DT, Salzman J, Haynes M, Rohwer F, Davis-Long C et al. 2012. Evidence of a robust resident bacteriophage population revealed through analysis of the human salivary virome. ISME J 6:915–26
    [Google Scholar]
  34. 34. 
    Chatterjee A, Duerkop BA. 2018. Beyond bacteria: bacteriophage-eukaryotic host interactions reveal emerging paradigms of health and disease. Front. Microbiol. 9:1394
    [Google Scholar]
  35. 35. 
    Hannigan GD, Meisel JS, Tyldsley AS, Zheng Q, Hodkinson BP et al. 2015. The human skin double-stranded DNA virome: topographical and temporal diversity, genetic enrichment, and dynamic associations with the host microbiome. mBio 6:e01578-15
    [Google Scholar]
  36. 36. 
    Abeles SR, Robles-Sikisaka R, Ly M, Lum AG, Salzman J et al. 2014. Human oral viruses are personal, persistent and gender-consistent. ISME J. 8:1753–67
    [Google Scholar]
  37. 37. 
    Gregory AC, Zablocki O, Zayed AA, Howell A, Bolduc B, Sullivan MB. 2020. The gut virome database reveals age-dependent patterns of virome diversity in the human gut. Cell Host Microbe 28:724–40.e8
    [Google Scholar]
  38. 38. 
    Kernbauer E, Ding Y, Cadwell K. 2014. An enteric virus can replace the beneficial function of commensal bacteria. Nature 516:94–98
    [Google Scholar]
  39. 39. 
    Van Belleghem JD, Dabrowska K, Vaneechoutte M, Barr JJ, Bollyky PL. 2018. Interactions between bacteriophage, bacteria, and the mammalian immune system. Viruses 11:10
    [Google Scholar]
  40. 40. 
    Koskella B, Lin DM, Buckling A, Thompson JN. 2012. The costs of evolving resistance in heterogeneous parasite environments. Proc. R. Soc. B 279:1896–903
    [Google Scholar]
  41. 41. 
    Modi SR, Lee HH, Spina CS, Collins JJ. 2013. Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome. Nature 499:219–22
    [Google Scholar]
  42. 42. 
    Adler BA, Kazakov AE, Zhong C, Lui H, Kutter Eet al 2021. The genetic basis of phage susceptibility, cross-resistance and host-range in Salmonella. bioRxiv 2020.04.27.058388. https://doi.org/10.1101/2020.04.27.058388
    [Crossref]
  43. 43. 
    Chatterjee A, Willett JLE, Nguyen UT, Monogue B, Palmer KL et al. 2020. Parallel genomics uncover novel enterococcal-bacteriophage interactions. mBio 11:e03120-19
    [Google Scholar]
  44. 44. 
    Soffer N, Woolston J, Li M, Das C, Sulakvelidze A. 2017. Bacteriophage preparation lytic for Shigella significantly reduces Shigella sonnei contamination in various foods. PLOS ONE 12:e0175256
    [Google Scholar]
  45. 45. 
    Roux S, Adriaenssens EM, Dutilh BE, Koonin EV, Kropinski AM et al. 2019. Minimum information about an uncultivated virus genome (MIUViG). Nat. Biotechnol. 37:29–37
    [Google Scholar]
  46. 46. 
    Kazlauskas D, Varsani A, Koonin EV, Krupovic M. 2019. Multiple origins of prokaryotic and eukaryotic single-stranded DNA viruses from bacterial and archaeal plasmids. Nat. Commun. 10:3425
    [Google Scholar]
  47. 47. 
    Koonin EV, Dolja VV, Krupovic M, Varsani A, Wolf YI et al. 2020. Global organization and proposed megataxonomy of the virus world. Microbiol. . Mol. Biol. Rev. 84:e00061-19
    [Google Scholar]
  48. 48. 
    Simmonds P, Adams MJ, Benko M, Breitbart M, Brister JR et al. 2017. Consensus statement: virus taxonomy in the age of metagenomics. Nat. Rev. Microbiol. 15:161–68
    [Google Scholar]
  49. 49. 
    Zhou P, Yang XL, Wang XG, Hu B, Zhang L et al. 2020. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature 579:270–73
    [Google Scholar]
  50. 50. 
    Pappas N, Roux S, Hölzer M, Lamkiewicz K, Mock F et al. 2021. Virus bioinformatics. Encyclopedia of Virology DH Bamford, M Zuckerman 124–32 Amsterdam: Academic, 4th ed..
    [Google Scholar]
  51. 51. 
    Trubl G, Hyman P, Roux S, Abedon ST. 2020. Coming-of-age characterization of soil viruses: a user's guide to virus isolation, detection within metagenomes, and viromics. Soil Syst 4:23
    [Google Scholar]
  52. 52. 
    Zhang YZ, Chen YM, Wang W, Qin XC, Holmes EC. 2019. Expanding the RNA virosphere by unbiased metagenomics. Annu. Rev. Virol. 6:119–39
    [Google Scholar]
  53. 53. 
    Guo J, Bolduc B, Zayed A, Varsani A, Dominguez-Huerta G et al. 2021. VirSorter2: a multi-classifier, expert-guided approach to detect diverse DNA and RNA viruses. Microbiome 9:37
    [Google Scholar]
  54. 54. 
    Tisza MJ, Belford AK, Domínguez-Huerta G, Bolduc B, Buck CB. 2021. Cenote-Taker 2 democratizes virus discovery and sequence annotation. Virus Evol. 7:veaa100
    [Google Scholar]
  55. 55. 
    Hyman P, Trubl G, Abedon ST. 2021. Virus-like particle: evolving meanings in different disciplines. Phage 2:11–15
    [Google Scholar]
  56. 56. 
    Sommers P, Fontenele RS, Kringen T, Kraberger S, Porazinska DL et al. 2019. Single-stranded DNA viruses in Antarctic cryoconite holes. Viruses 11:1022
    [Google Scholar]
  57. 57. 
    Santos-Medellin C, Zinke LA, ter Horst AM, Gelardi DL, Parikh SJ, Emerson JB. 2021. Viromes outperform total metagenomes in revealing the spatiotemporal patterns of agricultural soil viral communities. ISME J https://doi.org/10.1038/s41396-021-00897-y
    [Crossref] [Google Scholar]
  58. 58. 
    Thurber RV, Haynes M, Breitbart M, Wegley L, Rohwer F. 2009. Laboratory procedures to generate viral metagenomes. Nat. Protoc. 4:470–83
    [Google Scholar]
  59. 59. 
    Trubl G, Solonenko N, Chittick L, Solonenko SA, Rich VI, Sullivan MB. 2016. Optimization of viral resuspension methods for carbon-rich soils along a permafrost thaw gradient. PeerJ 4:e1999
    [Google Scholar]
  60. 60. 
    Trubl G, Roux S, Solonenko N, Li YF, Bolduc B et al. 2019. Towards optimized viral metagenomes for double-stranded and single-stranded DNA viruses from challenging soils. PeerJ 7:e7265
    [Google Scholar]
  61. 61. 
    Breitbart M, Hewson I, Felts B, Mahaffy JM, Nulton J et al. 2003. Metagenomic analyses of an uncultured viral community from human feces. J. Bacteriol. 185:6220–23
    [Google Scholar]
  62. 62. 
    Hjelmso MH, Hellmer M, Fernandez-Cassi X, Timoneda N, Lukjancenko O et al. 2017. Evaluation of methods for the concentration and extraction of viruses from sewage in the context of metagenomic sequencing. PLOS ONE 12:e0170199
    [Google Scholar]
  63. 63. 
    Bernardo P, Charles-Dominique T, Barakat M, Ortet P, Fernandez E et al. 2018. Geometagenomics illuminates the impact of agriculture on the distribution and prevalence of plant viruses at the ecosystem scale. ISME J 12:173–84
    [Google Scholar]
  64. 64. 
    Vega Thurber RL, Barott KL, Hall D, Liu H, Rodriguez-Mueller B et al. 2008. Metagenomic analysis indicates that stressors induce production of herpes-like viruses in the coral Porites compressa. PNAS 105:18413–18
    [Google Scholar]
  65. 65. 
    Zolotukhin S, Byrne BJ, Mason E, Zolotukhin I, Potter M et al. 1999. Recombinant adeno-associated virus purification using novel methods improves infectious titer and yield. Gene Ther 6:973–85
    [Google Scholar]
  66. 66. 
    Sun G, Xiao J, Wang H, Gong C, Pan Y et al. 2014. Efficient purification and concentration of viruses from a large body of high turbidity seawater. MethodsX 1:197–206
    [Google Scholar]
  67. 67. 
    John SG, Mendez CB, Deng L, Poulos B, Kauffman AK et al. 2011. A simple and efficient method for concentration of ocean viruses by chemical flocculation. Environ. Microbiol. Rep. 3:195–202
    [Google Scholar]
  68. 68. 
    Reichart NJ, Jay ZJ, Krukenberg V, Parker AE, Spietz RL, Hatzenpichler R. 2020. Activity-based cell sorting reveals responses of uncultured archaea and bacteria to substrate amendment. ISME J 14:2851–61
    [Google Scholar]
  69. 69. 
    Allen LZ, Ishoey T, Novotny MA, McLean JS, Lasken RS, Williamson SJ. 2011. Single virus genomics: a new tool for virus discovery. PLOS ONE 6:e17722
    [Google Scholar]
  70. 70. 
    Martinez-Garcia M, Martinez-Hernandez F, Martínez JM 2020. Single-virus genomics: studying uncultured viruses, one at a time. Encyclopedia of Virology DH Bamford, M Zuckerman 184–90 Amsterdam: Academic, 4th ed..
    [Google Scholar]
  71. 71. 
    Roux S, Emerson JB, Eloe-Fadrosh EA, Sullivan MB. 2017. Benchmarking viromics: an in silico evaluation of metagenome-enabled estimates of viral community composition and diversity. PeerJ 5:e3817
    [Google Scholar]
  72. 72. 
    Varsani A, Lefeuvre P, Roumagnac P, Martin D. 2018. Notes on recombination and reassortment in multipartite/segmented viruses. Curr. Opin. Virol. 33:156–66
    [Google Scholar]
  73. 73. 
    Martinez-Hernandez F, Fornas O, Lluesma Gomez M, Bolduc B, de la Cruz Pena MJ et al. 2017. Single-virus genomics reveals hidden cosmopolitan and abundant viruses. Nat. Commun. 8:15892
    [Google Scholar]
  74. 74. 
    de la Cruz Pena MJ, Martinez-Hernandez F, Garcia-Heredia I, Lluesma Gomez M, Fornas O, Martinez-Garcia M 2018. Deciphering the human virome with single-virus genomics and metagenomics. Viruses 10:3113
    [Google Scholar]
  75. 75. 
    Martínez JM, Martinez-Hernandez F, Martinez-Garcia M. 2020. Single-virus genomics and beyond. Nat. Rev. Microbiol. 18:705–16
    [Google Scholar]
  76. 76. 
    Lefeuvre P, Martin DP, Elena SF, Shepherd DN, Roumagnac P, Varsani A. 2019. Evolution and ecology of plant viruses. Nat. Rev. Microbiol. 17:632–44
    [Google Scholar]
  77. 77. 
    Roux S, Solonenko NE, Dang VT, Poulos BT, Schwenck SM et al. 2016. Towards quantitative viromics for both double-stranded and single-stranded DNA viruses. PeerJ 4:e2777
    [Google Scholar]
  78. 78. 
    Okada R, Kiyota E, Moriyama H, Fukuhara T, Natsuaki T. 2015. A simple and rapid method to purify viral dsRNA from plant and fungal tissue. J. Gen. Plant Pathol. 81:103–7
    [Google Scholar]
  79. 79. 
    Lukács N. 1994. Detection of virus infection in plants and differentiation between coexisting viruses by monoclonal antibodies to double-stranded RNA. J. Virol. Methods 47:255–72
    [Google Scholar]
  80. 80. 
    Seguin J, Rajeswaran R, Malpica-Lopez N, Martin RR, Kasschau K et al. 2014. De novo reconstruction of consensus master genomes of plant RNA and DNA viruses from siRNAs. PLOS ONE 9:e88513
    [Google Scholar]
  81. 81. 
    Wu Q, Luo Y, Lu R, Lau N, Lai EC et al. 2010. Virus discovery by deep sequencing and assembly of virus-derived small silencing RNAs. PNAS 107:1606–11
    [Google Scholar]
  82. 82. 
    Logsdon GA, Vollger MR, Eichler EE. 2020. Long-read human genome sequencing and its applications. Nat. Rev. Genet. 21:597–614
    [Google Scholar]
  83. 83. 
    Zablocki O, Michelsen M, Burris M, Solonenko N, Warwick-Dugdale J et al. 2020. VirION2: a short- and long-read sequencing and informatics workflow to study the genomic diversity of viruses in nature. PeerJ 9:e11088
    [Google Scholar]
  84. 84. 
    Edwards RA, McNair K, Faust K, Raes J, Dutilh BE. 2016. Computational approaches to predict bacteriophage-host relationships. FEMS Microbiol. Rev. 40:258–72
    [Google Scholar]
  85. 85. 
    Bikel S, Valdez-Lara A, Cornejo-Granados F, Rico K, Canizales-Quinteros S et al. 2015. Combining metagenomics, metatranscriptomics and viromics to explore novel microbial interactions: towards a systems-level understanding of human microbiome. Comput. Struct. Biotechnol. J. 13:390–401
    [Google Scholar]
  86. 86. 
    Sieradzki ET, Ignacio-Espinoza JC, Needham DM, Fichot EB, Fuhrman JA. 2019. Dynamic marine viral infections and major contribution to photosynthetic processes shown by spatiotemporal picoplankton metatranscriptomes. Nat. Commun. 10:1169
    [Google Scholar]
  87. 87. 
    Rostol JT, Marraffini L. 2019. Ph)ighting phages: how bacteria resist their parasites. Cell Host Microbe 25:184–94
    [Google Scholar]
  88. 88. 
    Howard-Varona C, Hargreaves KR, Solonenko NE, Markillie LM, White RA 3rd et al. 2018. Multiple mechanisms drive phage infection efficiency in nearly identical hosts. ISME J 12:1605–18
    [Google Scholar]
  89. 89. 
    Howard-Varona C, Lindback MM, Bastien GE, Solonenko N, Zayed AA et al. 2020. Phage-specific metabolic reprogramming of virocells. ISME J 14:881–95
    [Google Scholar]
  90. 90. 
    Starr EP, Shi S, Blazewicz SJ, Probst AJ, Herman DJ et al. 2018. Stable isotope informed genome-resolved metagenomics reveals that Saccharibacteria utilize microbially-processed plant-derived carbon. Microbiome 6:122
    [Google Scholar]
  91. 91. 
    Barnett SE, Buckley DH. 2020. Simulating metagenomic stable isotope probing datasets with MetaSIPSim. BMC Bioinform. 21:37
    [Google Scholar]
  92. 92. 
    Dumont MG, García MH. 2019. Stable Isotope Probing New York: Humana
    [Google Scholar]
  93. 93. 
    Haig SJ, Schirmer M, D'Amore R, Gibbs J, Davies RL et al. 2015. Stable-isotope probing and metagenomics reveal predation by protozoa drives E. coli removal in slow sand filters. ISME J 9:797–808
    [Google Scholar]
  94. 94. 
    Trubl G, Kimbrel JA, Liquet-Gonzalez J, Nuccio EE, Weber PK et al. 2021. Ecology of active viruses and their bacterial hosts in frozen Arctic peat soil revealed with H218O stable isotope probing metagenomics. bioRxiv 2021.01.25.428156. https://doi.org/10.1101/2021.01.25.428156
    [Crossref]
  95. 95. 
    Blazewicz SJ, Hungate BA, Koch BJ, Nuccio EE, Morrissey E et al. 2020. Taxon-specific microbial growth and mortality patterns reveal distinct temporal population responses to rewetting in a California grassland soil. ISME J 14:1520–32
    [Google Scholar]
  96. 96. 
    Sieradzki ET, Koch BJ, Greenlon A, Sachdeva R, Malmstrom RR et al. 2020. Measurement error and resolution in quantitative stable isotope probing: implications for experimental design. mSystems 5:e00151-20
    [Google Scholar]
  97. 97. 
    Kolb HC, Finn MG, Sharpless KB. 2001. Click chemistry: diverse chemical function from a few good reactions. Angew. Chem. 40:2004–21
    [Google Scholar]
  98. 98. 
    Kiick KL, Saxon E, Tirrell DA, Bertozzi CR 2002. Incorporation of azides into recombinant proteins for chemoselective modification by the Staudinger ligation. PNAS 99:19–24
    [Google Scholar]
  99. 99. 
    Samo TJ, Smriga S, Malfatti F, Sherwood BP, Azam F. 2014. Corrigendum: broad distribution and high proportion of protein synthesis active marine bacteria revealed by click chemistry at the single cell level. Front. Mar. Sci. 1:60
    [Google Scholar]
  100. 100. 
    Muller TG, Sakin V, Muller B. 2019. A spotlight on viruses—application of click chemistry to visualize virus-cell interactions. Molecules 24:481
    [Google Scholar]
  101. 101. 
    Pett-Ridge J, Weber PK. 2012. NanoSIP: NanoSIMS applications for microbial biology. Methods Mol. Biol. 881:375–408
    [Google Scholar]
  102. 102. 
    Pasulka AL, Thamatrakoln K, Kopf SH, Guan Y, Poulos B et al. 2018. Interrogating marine virus-host interactions and elemental transfer with BONCAT and nanoSIMS-based methods. Environ. Microbiol. 20:671–92
    [Google Scholar]
  103. 103. 
    Gates SD, Condit RC, Moussatche N, Stewart BJ, Malkin AJ, Weber PK. 2018. High initial sputter rate found for vaccinia virions using isotopic labeling, NanoSIMS, and AFM. Anal. Chem. 90:1613–20
    [Google Scholar]
  104. 104. 
    Pacton M, Wacey D, Corinaldesi C, Tangherlini M, Kilburn MR et al. 2014. Viruses as new agents of organomineralization in the geological record. Nat. Commun. 5:4298
    [Google Scholar]
  105. 105. 
    Baran N, Goldin S, Maidanik I, Lindell D. 2018. Quantification of diverse virus populations in the environment using the polony method. Nat. Microbiol. 3:62–72
    [Google Scholar]
  106. 106. 
    Castillo YM, Mangot JF, Benites LF, Logares R, Kuronishi M et al. 2019. Assessing the viral content of uncultured picoeukaryotes in the global-ocean by single cell genomics. Mol. Ecol. 28:4272–89
    [Google Scholar]
  107. 107. 
    Mruwat N, Carlson MCG, Goldin S, Ribalet F, Kirzner S et al. 2021. A single-cell polony method reveals low levels of infected Prochlorococcus in oligotrophic waters despite high cyanophage abundances. ISME J 15:41–54
    [Google Scholar]
  108. 108. 
    Allers E, Moraru C, Duhaime MB, Beneze E, Solonenko N et al. 2013. Single-cell and population level viral infection dynamics revealed by phageFISH, a method to visualize intracellular and free viruses. Environ. Microbiol. 15:2306–18
    [Google Scholar]
  109. 109. 
    Barrero-Canosa J, Moraru C. 2019. PhageFISH for monitoring phage infections at single cell level. Methods Mol. Biol. 1898:1–26
    [Google Scholar]
  110. 110. 
    Vincent F, Sheyn U, Porat Z, Vardi A. 2021. Visualizing active viral infection reveals diverse cell fates in synchronized algal bloom demise. PNAS 118:e2021586118
    [Google Scholar]
  111. 111. 
    Deng L, Ignacio-Espinoza JC, Gregory AC, Poulos BT, Weitz JS et al. 2014. Viral tagging reveals discrete populations in Synechococcus viral genome sequence space. Nature 513:242–45
    [Google Scholar]
  112. 112. 
    Dzunkova M, Low SJ, Daly JN, Deng L, Rinke C, Hugenholtz P. 2019. Defining the human gut host-phage network through single-cell viral tagging. Nat. Microbiol. 4:2192–203
    [Google Scholar]
  113. 113. 
    Marbouty M, Baudry L, Cournac A, Koszul R. 2017. Scaffolding bacterial genomes and probing host-virus interactions in gut microbiome by proximity ligation (chromosome capture) assay. Sci. Adv. 3:e1602105
    [Google Scholar]
  114. 114. 
    Marbouty M, Thierry A, Milluit GA, Koszul R. 2021. MetaHiC phage-bacteria infection network reveals active cycling phages of the healthy human gut. eLife 10:e60608
    [Google Scholar]
  115. 115. 
    Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T et al. 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:289–93
    [Google Scholar]
  116. 116. 
    Kim KD, Tanizawa H, De Leo A, Vladimirova O, Kossenkov A et al. 2020. Epigenetic specifications of host chromosome docking sites for latent Epstein-Barr virus. Nat. Commun. 11:877
    [Google Scholar]
  117. 117. 
    Nagano T, Lubling Y, Yaffe E, Wingett SW, Dean W et al. 2015. Single-cell Hi-C for genome-wide detection of chromatin interactions that occur simultaneously in a single cell. Nat. Protoc. 10:1986–2003
    [Google Scholar]
  118. 118. 
    Díaz-Muñoz SL, Sanjuan R, West S. 2017. Sociovirology: conflict, cooperation, and communication among viruses. Cell Host Microbe 22:437–41
    [Google Scholar]
  119. 119. 
    Turner PE, Chao L. 1999. Prisoner's dilemma in an RNA virus. Nature 398:441–43
    [Google Scholar]
  120. 120. 
    DaPalma T, Doonan BP, Trager NM, Kasman LM. 2010. A systematic approach to virus-virus interactions. Virus Res 149:1–9
    [Google Scholar]
  121. 121. 
    Novick RP, Christie GE, Penades JR. 2010. The phage-related chromosomal islands of Gram-positive bacteria. Nat. Rev. Microbiol. 8:541–51
    [Google Scholar]
  122. 122. 
    Penades JR, Christie GE. 2015. The phage-inducible chromosomal islands: a family of highly evolved molecular parasites. Annu. Rev. Virol. 2:181–201
    [Google Scholar]
  123. 123. 
    Ryu W-S 2017. Subviral agents and prions. Molecular Virology of Human Pathogenic Viruses W-S Ryu 277–88 San Diego, CA: Elsevier
    [Google Scholar]
  124. 124. 
    Krupovic M 2020. Plant satellite viruses (Albetovirus, Aumaivirus, Papanivirus, Virtovirus). Encyclopedia of Virology DH Bamford, M Zuckerman 581–85 Amsterdam: Academic , 4th ed..
    [Google Scholar]
  125. 125. 
    Desnues C, Raoult D. 2010. Inside the lifestyle of the virophage. Intervirology 53:293–303
    [Google Scholar]
  126. 126. 
    Alves C, Branco C, Cunha C. 2013. Hepatitis delta virus: a peculiar virus. Adv. Virol. 2013.560105
    [Google Scholar]
  127. 127. 
    Gnanasekaran P, KishoreKumar R, Bhattacharyya D, Vinoth Kumar R, Chakraborty S 2019. Multifaceted role of geminivirus associated betasatellite in pathogenesis. Mol. Plant Pathol. 20:1019–33
    [Google Scholar]
  128. 128. 
    Frigols B, Quiles-Puchalt N, Mir-Sanchis I, Donderis J, Elena SF et al. 2015. Virus satellites drive viral evolution and ecology. PLOS Genet 11:e1005609
    [Google Scholar]
  129. 129. 
    Vignuzzi M, Lopez CB. 2019. Defective viral genomes are key drivers of the virus-host interaction. Nat. Microbiol. 4:1075–87
    [Google Scholar]
  130. 130. 
    Brooke CB. 2017. Population diversity and collective interactions during influenza virus infection. J. Virol. 91:e01164-17
    [Google Scholar]
  131. 131. 
    Alnaji FG, Holmes JR, Rendon G, Vera JC, Fields CJ et al. 2019. Sequencing framework for the sensitive detection and precise mapping of defective interfering particle-associated deletions across influenza A and B viruses. J. Virol. 93:e00354-19
    [Google Scholar]
  132. 132. 
    Ng TF, Duffy S, Polston JE, Bixby E, Vallad GE, Breitbart M. 2011. Exploring the diversity of plant DNA viruses and their satellites using vector-enabled metagenomics on whiteflies. PLOS ONE 6:e19050
    [Google Scholar]
  133. 133. 
    Roux S, Chan LK, Egan R, Malmstrom RR, McMahon KD, Sullivan MB. 2017. Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics. Nat. Commun. 8:858
    [Google Scholar]
  134. 134. 
    Zhou J, Zhang W, Yan S, Xiao J, Zhang Y et al. 2013. Diversity of virophages in metagenomic data sets. J. Virol. 87:4225–36
    [Google Scholar]
  135. 135. 
    Paez-Espino D, Zhou J, Roux S, Nayfach S, Pavlopoulos GA et al. 2019. Diversity, evolution, and classification of virophages uncovered through global metagenomics. Microbiome 7:157
    [Google Scholar]
  136. 136. 
    Yau S, Lauro FM, DeMaere MZ, Brown MV, Thomas T et al. 2011. Virophage control of antarctic algal host-virus dynamics. PNAS 108:6163–68
    [Google Scholar]
  137. 137. 
    Schulz F, Roux S, Paez-Espino D, Jungbluth S, Walsh DA et al. 2020. Giant virus diversity and host interactions through global metagenomics. Nature 578:432–36
    [Google Scholar]
  138. 138. 
    Schulz F, Alteio L, Goudeau D, Ryan EM, Yu FB et al. 2018. Hidden diversity of soil giant viruses. Nat. Commun. 9:4881
    [Google Scholar]
  139. 139. 
    Zhang W, Zhou J, Liu T, Yu Y, Pan Y et al. 2015. Four novel algal virus genomes discovered from Yellowstone Lake metagenomes. Sci. Rep. 5:15131
    [Google Scholar]
  140. 140. 
    Backstrom D, Yutin N, Jorgensen SL, Dharamshi J, Homa F et al. 2019. Virus genomes from deep sea sediments expand the ocean megavirome and support independent origins of viral gigantism. mBio 10:e02497–18
    [Google Scholar]
  141. 141. 
    Leeks A, Sanjuan R, West SA. 2019. The evolution of collective infectious units in viruses. Virus Res 265:94–101
    [Google Scholar]
  142. 142. 
    Domingo-Calap P, Mora-Quilis L, Sanjuan R 2020. Social bacteriophages. Microorganisms 8:533
    [Google Scholar]
  143. 143. 
    Erez Z, Steinberger-Levy I, Shamir M, Doron S, Stokar-Avihail A et al. 2017. Communication between viruses guides lysis-lysogeny decisions. Nature 541:488–93
    [Google Scholar]
  144. 144. 
    Borges AL, Zhang JY, Rollins MF, Osuna BA, Wiedenheft B, Bondy-Denomy J. 2018. Bacteriophage cooperation suppresses CRISPR-Cas3 and Cas9 immunity. Cell 174:917–25.e10
    [Google Scholar]
  145. 145. 
    Landsberger M, Gandon S, Meaden S, Rollie C, Chevallereau A et al. 2018. Anti-CRISPR phages cooperate to overcome CRISPR-Cas immunity. Cell 174:908–16.e12
    [Google Scholar]
  146. 146. 
    Roux S, Krupovic M, Poulet A, Debroas D, Enault F. 2012. Evolution and diversity of the Microviridae viral family through a collection of 81 new complete genomes assembled from virome reads. PLOS ONE 7:e40418
    [Google Scholar]
  147. 147. 
    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
    [Google Scholar]
  148. 148. 
    de la Higuera I, Kasun GW, Torrance EL, Pratt AA, Maluenda A et al. 2020. Unveiling crucivirus diversity by mining metagenomic data. mBio 11:e01410–20
    [Google Scholar]
  149. 149. 
    Díaz-Muñoz SL. 2017. Viral coinfection is shaped by host ecology and virus-virus interactions across diverse microbial taxa and environments. Virus Evol 3:vex011
    [Google Scholar]
  150. 150. 
    Roux S, Hallam SJ, Woyke T, Sullivan MB. 2015. Viral dark matter and virus-host interactions resolved from publicly available microbial genomes. eLife 4:e08490
    [Google Scholar]
  151. 151. 
    Labonte JM, Swan BK, Poulos B, Luo H, Koren S et al. 2015. Single-cell genomics-based analysis of virus-host interactions in marine surface bacterioplankton. ISME J 9:2386–99
    [Google Scholar]
  152. 152. 
    McCallin S, Alam Sarker S, Barretto C, Sultana S, Berger B et al. 2013. Safety analysis of a Russian phage cocktail: from metagenomic analysis to oral application in healthy human subjects. Virology 443:187–96
    [Google Scholar]
  153. 153. 
    Fujimoto K, Kimura Y, Shimohigoshi M, Satoh T, Sato S et al. 2020. Metagenome data on intestinal phage-bacteria associations aids the development of phage therapy against pathobionts. Cell Host Microbe 28:380–89.e9
    [Google Scholar]
  154. 154. 
    Kahn LH, Bergeron G, Bourassa MW, De Vegt B, Gill J et al. 2019. From farm management to bacteriophage therapy: strategies to reduce antibiotic use in animal agriculture. Ann. N. Y. Acad. Sci. 1441:31–39
    [Google Scholar]
  155. 155. 
    Fernandez L, Gutierrez D, Rodriguez A, Garcia P. 2018. Application of bacteriophages in the agro-food sector: a long way toward approval. Front. Cell Infect. Microbiol. 8:296
    [Google Scholar]
  156. 156. 
    Schoenfeld T, Liles M, Wommack KE, Polson SW, Godiska R, Mead D 2010. Functional viral metagenomics and the next generation of molecular tools. Trends Microbiol 18:20–29
    [Google Scholar]
  157. 157. 
    Yang H, Schmitt-Wagner D, Stingl U, Brune A. 2005. Niche heterogeneity determines bacterial community structure in the termite gut (Reticulitermes santonensis). Environ. Microbiol. 7:916–32
    [Google Scholar]
  158. 158. 
    Heilmann S, Sneppen K, Krishna S 2012. Coexistence of phage and bacteria on the boundary of self-organized refuges. PNAS 109:12828–33
    [Google Scholar]
  159. 159. 
    Brockhurst MA, Buckling A, Rainey PB. 2006. Spatial heterogeneity and the stability of host-parasite coexistence. J. Evol. Biol. 19:374–79
    [Google Scholar]
  160. 160. 
    De Sordi L, Khanna V, Debarbieux L. 2017. The gut microbiota facilitates drifts in the genetic diversity and infectivity of bacterial viruses. Cell Host Microbe 22:801–8.e3
    [Google Scholar]
  161. 161. 
    Galtier M, De Sordi L, Maura D, Arachchi H, Volant S et al. 2016. Bacteriophages to reduce gut carriage of antibiotic resistant uropathogens with low impact on microbiota composition. Environ. Microbiol. 18:2237–45
    [Google Scholar]
  162. 162. 
    Hsu BB, Gibson TE, Yeliseyev V, Liu Q, Lyon L et al. 2019. Dynamic modulation of the gut microbiota and metabolome by bacteriophages in a mouse model. Cell Host Microbe 25:803–14.e5
    [Google Scholar]
  163. 163. 
    Keen EC, Dantas G. 2018. Close encounters of three kinds: bacteriophages, commensal bacteria, and host immunity. Trends Microbiol 26:943–54
    [Google Scholar]
  164. 164. 
    Norman JM, Handley SA, Baldridge MT, Droit L, Liu CY et al. 2015. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell 160:447–60
    [Google Scholar]
  165. 165. 
    Wang W, Jovel J, Halloran B, Wine E, Patterson J et al. 2015. Metagenomic analysis of microbiome in colon tissue from subjects with inflammatory bowel diseases reveals interplay of viruses and bacteria. Inflamm. Bowel Dis. 21:1419–27
    [Google Scholar]
  166. 166. 
    Reyes A, Blanton LV, Cao S, Zhao G, Manary M et al. 2015. Gut DNA viromes of Malawian twins discordant for severe acute malnutrition. PNAS 112:11941–46
    [Google Scholar]
  167. 167. 
    Kang DW, Adams JB, Gregory AC, Borody T, Chittick L et al. 2017. Microbiota transfer therapy alters gut ecosystem and improves gastrointestinal and autism symptoms: an open-label study. Microbiome 5:10
    [Google Scholar]
  168. 168. 
    Lim ES, Wang D, Holtz LR. 2016. The bacterial microbiome and virome milestones of infant development. Trends Microbiol 24:801–10
    [Google Scholar]
  169. 169. 
    Lee JY, Mannaa M, Kim Y, Kim J, Kim GT, Seo YS. 2019. Comparative analysis of fecal microbiota composition between rheumatoid arthritis and osteoarthritis patients. Genes 10:748
    [Google Scholar]
  170. 170. 
    Scher JU, Sczesnak A, Longman RS, Segata N, Ubeda C et al. 2013. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. eLife 2:e01202
    [Google Scholar]
  171. 171. 
    Ma Y, You X, Mai G, Tokuyasu T, Liu C. 2018. A human gut phage catalog correlates the gut phageome with type 2 diabetes. Microbiome 6:24
    [Google Scholar]
  172. 172. 
    Tetz G, Brown SM, Hao Y, Tetz V. 2019. Type 1 diabetes: an association between autoimmunity, the dynamics of gut amyloid-producing E. coli and their phages. Sci. Rep. 9:9685
    [Google Scholar]
  173. 173. 
    Minot SS, Willis AD. 2019. Clustering co-abundant genes identifies components of the gut microbiome that are reproducibly associated with colorectal cancer and inflammatory bowel disease. Microbiome 7:110
    [Google Scholar]
  174. 174. 
    Yu AI, Zhao L, Eaton KA, Ho S, Chen J et al. 2020. Gut microbiota modulate CD8 T cell responses to influence colitis-associated tumorigenesis. Cell Rep 31:107471
    [Google Scholar]
  175. 175. 
    Anantharaman K, Duhaime MB, Breier JA, Wendt KA, Toner BM, Dick GJ. 2014. Sulfur oxidation genes in diverse deep-sea viruses. Science 344:757–60
    [Google Scholar]
  176. 176. 
    Sullivan MB, Coleman ML, Weigele P, Rohwer F, Chisholm SW. 2005. Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLOS Biol. 3:e144
    [Google Scholar]
  177. 177. 
    Campbell DE, Ly LK, Ridlon JM, Hsiao A, Whitaker RJ, Degnan PH. 2020. Infection with bacteroides phage BV01 alters the host transcriptome and bile acid metabolism in a common human gut microbe. Cell Rep 32:108142
    [Google Scholar]
  178. 178. 
    Abeles SR, Ly M, Santiago-Rodriguez TM, Pride DT. 2015. Effects of long term antibiotic therapy on human oral and fecal viromes. PLOS ONE 10:e0134941
    [Google Scholar]
  179. 179. 
    Willner D, Furlan M, Schmieder R, Grasis JA, Pride DT et al. 2011. Metagenomic detection of phage-encoded platelet-binding factors in the human oral cavity. PNAS 108:Suppl. 14547–53
    [Google Scholar]
  180. 180. 
    Shaffer M, Borton MA, McGivern BB, Zayed AA, La Rosa SL et al. 2020. DRAM for distilling microbial metabolism to automate the curation of microbiome function. Nucleic Acids Res 48:8883–900
    [Google Scholar]
  181. 181. 
    Hily JM, Candresse T, Garcia S, Vigne E, Tanniere M et al. 2018. High-throughput sequencing and the viromic study of grapevine leaves: from the detection of grapevine-infecting viruses to the description of a new environmental Tymovirales member. Front. Microbiol. 9:1782
    [Google Scholar]
  182. 182. 
    Bacnik K, Kutnjak D, Pecman A, Mehle N, Tusek Znidaric M et al. 2020. Viromics and infectivity analysis reveal the release of infective plant viruses from wastewater into the environment. Water Res 177:115628
    [Google Scholar]
  183. 183. 
    Chang Y. 2020. Bacteriophage-derived endolysins applied as potent biocontrol agents to enhance food safety. Microorganisms 8:724
    [Google Scholar]
  184. 184. 
    Starr EP, Nuccio EE, Pett-Ridge J, Banfield JF, Firestone MK 2019. Metatranscriptomic reconstruction reveals RNA viruses with the potential to shape carbon cycling in soil. PNAS 116:25900–8
    [Google Scholar]
  185. 185. 
    Pratama AA, Terpstra J, de Oliveria ALM, Salles JF. 2020. The role of rhizosphere bacteriophages in plant health. Trends Microbiol 28:709–18
    [Google Scholar]
  186. 186. 
    Dunay E, Apakupakul K, Leard S, Palmer JL, Deem SL. 2018. Pathogen transmission from humans to great apes is a growing threat to primate conservation. EcoHealth 15:148–62
    [Google Scholar]
  187. 187. 
    Gustafson LL, Creekmore LH, Snekvik KR, Ferguson JA, Warg JV et al. 2018. A systematic surveillance programme for infectious salmon anaemia virus supports its absence in the Pacific Northwest of the United States. J. Fish Dis. 41:337–46
    [Google Scholar]
  188. 188. 
    Sokolow SH, Nova N, Pepin KM, Peel AJ, Pulliam JRC et al. 2019. Ecological interventions to prevent and manage zoonotic pathogen spillover. Philos. Trans. R. Soc. B 374:20180342
    [Google Scholar]
  189. 189. 
    Johnson PT, de Roode JC, Fenton A. 2015. Why infectious disease research needs community ecology. Science 349:1259504
    [Google Scholar]
  190. 190. 
    Mizuno CM, Ghai R, Rodriguez-Valera F. 2014. Evidence for metaviromic islands in marine phages. Front. Microbiol. 5:27
    [Google Scholar]
  191. 191. 
    Pascoal F, Costa R, Magalhaes C. 2020. The microbial rare biosphere: current concepts, methods and ecological principles. FEMS Microbiol. Ecol. 97:fiaa227
    [Google Scholar]
  192. 192. 
    Holmfeldt K, Solonenko N, Shah M, Corrier K, Riemann L et al. 2013. Twelve previously unknown phage genera are ubiquitous in global oceans. PNAS 110:12798–803
    [Google Scholar]
  193. 193. 
    Duhaime MB, Deng L, Poulos BT, Sullivan MB. 2012. Towards quantitative metagenomics of wild viruses and other ultra-low concentration DNA samples: a rigorous assessment and optimization of the linker amplification method. Environ. Microbiol. 14:2526–37
    [Google Scholar]
  194. 194. 
    Duhaime MB, Sullivan MB. 2012. Ocean viruses: rigorously evaluating the metagenomic sample-to-sequence pipeline. Virology 434:181–86
    [Google Scholar]
  195. 195. 
    French RK, Holmes EC. 2020. An ecosystems perspective on virus evolution and emergence. Trends Microbiol 28:165–75
    [Google Scholar]
  196. 196. 
    Fierer N. 2017. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat. Rev. Microbiol. 15:579–90
    [Google Scholar]
  197. 197. 
    Jarett JK, Dzunkova M, Schulz F, Roux S, Paez-Espino D et al. 2020. Insights into the dynamics between viruses and their hosts in a hot spring microbial mat. ISME J 14:2527–41
    [Google Scholar]
  198. 198. 
    Hillman BI, Cai G. 2013. The family Narnaviridae: simplest of RNA viruses. Adv. Virus Res. 86:149–76
    [Google Scholar]
  199. 199. 
    Sieradzki ET, Morando M, Fuhrman JA. 2021. Metagenomics and quantitative stable isotope probing offer insights into metabolism of polycyclic aromatic hydrocarbon degraders in chronically polluted seawater. mSystems 6:e00245-21
    [Google Scholar]
  200. 200. 
    Starr EP, Shi S, Blazewicz SJ, Koch BJ, Probst AJ et al. 2020. Stable isotope informed genome-resolved metagenomics uncovers potential trophic interactions in rhizosphere soil. bioRxiv 2020.08.21.262063. https://doi.org/10.1101/2020.08.21.262063
    [Crossref]
  201. 201. 
    Berjón-Otero M, Duponchel S, Hackl T, Fischer M. 2020. Visualization of giant virus particles using BONCAT labeling and STED microscopy. bioRxiv 2020.07.14.202192. https://doi.org/10.1101/2020.07.14.202192
    [Crossref]
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