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Diagnostic metagenomics: potential applications to bacterial, viral and parasitic infections

  • M. J. PALLEN (a1)


The term ‘shotgun metagenomics’ is applied to the direct sequencing of DNA extracted from a sample without culture or target-specific amplification or capture. In diagnostic metagenomics, this approach is applied to clinical samples in the hope of detecting and characterizing pathogens. Here, I provide a conceptual overview, before reviewing several recent promising proof-of-principle applications of metagenomics in virus discovery, analysis of outbreaks and detection of pathogens in contemporary and historical samples. I also evaluate future prospects for diagnostic metagenomics in the light of relentless improvements in sequencing technologies.

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*Corresponding author: Division of Microbiology and Infection, Warwick Medical School, University of Warwick, Coventry CV4 7AL, UK. E-mail:


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Andersson, P., Klein, M., Lilliebridge, R. A. and Giffard, P. M. (2013). Sequences of multiple bacterial genomes and a Chlamydia trachomatis genotype from direct sequencing of DNA derived from a vaginal swab diagnostic specimen. Clinical Microbiology and Infection 19, E405E408.
Arumugam, M., Raes, J., Pelletier, E., Le Paslier, D., Yamada, T., Mende, D. R., Fernandes, G. R., Tap, J., Bruls, T., Batto, J. M., Bertalan, M., Borruel, N., Casellas, F., Fernandez, L., Gautier, L., Hansen, T., Hattori, M., Hayashi, T., Kleerebezem, M., Kurokawa, K., Leclerc, M., Levenez, F., Manichanh, C., Nielsen, H. B., Nielsen, T., Pons, N., Poulain, J., Qin, J., Sicheritz-Ponten, T., Tims, S., Torrents, D., Ugarte, E., Zoetendal, E. G., Wang, J., Guarner, F., Pedersen, O., de Vos, W. M., Brunak, S., Dore, J., Antolin, M., Artiguenave, F., Blottiere, H. M., Almeida, M., Brechot, C., Cara, C., Chervaux, C., Cultrone, A., Delorme, C., Denariaz, G., Dervyn, R., Foerstner, K. U., Friss, C., van de Guchte, M., Guedon, E., Haimet, F., Huber, W., van Hylckama-Vlieg, J., Jamet, A., Juste, C., Kaci, G., Knol, J., Lakhdari, O., Layec, S., Le Roux, K., Maguin, E., Merieux, A., Melo Minardi, R., M'rini, C., Muller, J., Oozeer, R., Parkhill, J., Renault, P., Rescigno, M., Sanchez, N., Sunagawa, S., Torrejon, A., Turner, K., Vandemeulebrouck, G., Varela, E., Winogradsky, Y., Zeller, G., Weissenbach, J., Ehrlich, S. D. and Bork, P. (2011). Enterotypes of the human gut microbiome. Nature 473, 174180.
Batty, E. M., Wong, T. H., Trebes, A., Argoud, K., Attar, M., Buck, D., Ip, C. L., Golubchik, T., Cule, M., Bowden, R., Manganis, C., Klenerman, P., Barnes, E., Walker, A. S., Wyllie, D. H., Wilson, D. J., Dingle, K. E., Peto, T. E., Crook, D. W. and Piazza, P. (2013). A modified RNA-Seq approach for whole genome sequencing of RNA viruses from faecal and blood samples. PLoS One 8, e66129.
Bos, K. I., Schuenemann, V. J., Golding, G. B., Burbano, H. A., Waglechner, N., Coombes, B. K., McPhee, J. B., DeWitte, S. N., Meyer, M., Schmedes, S., Wood, J., Earn, D. J., Herring, D. A., Bauer, P., Poinar, H. N. and Krause, J. (2011). A draft genome of Yersinia pestis from victims of the Black Death. Nature 478, 506510.
Bouwman, A. S., Kennedy, S. L., Muller, R., Stephens, R. H., Holst, M., Caffell, A. C., Roberts, C. A. and Brown, T. A. (2012). Genotype of a historic strain of Mycobacterium tuberculosis. Proceedings of the National Academy of Sciences USA 109, 1851118516.
Briese, T., Paweska, J. T., McMullan, L. K., Hutchison, S. K., Street, C., Palacios, G., Khristova, M. L., Weyer, J., Swanepoel, R., Egholm, M., Nichol, S. T. and Lipkin, W. I. (2009). Genetic detection and characterization of Lujo virus, a new hemorrhagic fever-associated arenavirus from southern Africa. PLoS Pathogens 5, e1000455.
Capobianchi, M. R., Giombini, E. and Rozera, G. (2013). Next-generation sequencing technology in clinical virology. Clinical Microbiology and Infection 19, 1522.
Chan, J. Z., Sergeant, M. J., Lee, O. Y., Minnikin, D. E., Besra, G. S., Pap, I., Spigelman, M., Donoghue, H. D. and Pallen, M. J. (2013). Metagenomic analysis of tuberculosis in a mummy. New England Journal of Medicine 369, 289290.
Christodoulou, D. C., Gorham, J. M., Herman, D. S. and Seidman, J. G. (2011). Construction of normalized RNA-seq libraries for next-generation sequencing using the crab duplex-specific nuclease. Current Protocols in Molecular Biology 94,
Dowd, S. E., Wolcott, R. D., Kennedy, J., Jones, C. and Cox, S. B. (2011). Molecular diagnostics and personalised medicine in wound care: assessment of outcomes. Journal of Wound Care 20, 232, 234–9.
Forney, L. J., Zhou, X. and Brown, C. J. (2004). Molecular microbial ecology: land of the one-eyed king. Current Opinion in Microbiology 7, 210220.
Gram, H. C. (1884). Über die isolierte Färbung der Schizomyceten in Schnitt- und Trockenpräparaten. Fortschritte der Medizin 2, 185189.
Greninger, A. L., Chen, E. C., Sittler, T., Scheinerman, A., Roubinian, N., Yu, G., Kim, E., Pillai, D. R., Guyard, C., Mazzulli, T., Isa, P., Arias, C. F., Hackett, J., Schochetman, G., Miller, S., Tang, P. and Chiu, C. Y. (2010). A metagenomic analysis of pandemic influenza A (2009 H1N1) infection in patients from North America. PLoS One 5, e13381.
Griffing, S. M., Mixson-Hayden, T., Sridaran, S., Alam, M. T., McCollum, A. M., Cabezas, C., Marquino Quezada, W., Barnwell, J. W., De Oliveira, A. M., Lucas, C., Arrospide, N., Escalante, A. A., Bacon, D. J. and Udhayakumar, V. (2011). South American Plasmodium falciparum after the malaria eradication era: clonal population expansion and survival of the fittest hybrids. PLoS One 6, e23486.
Handelsman, J., Rondon, M. R., Brady, S. F., Clardy, J. and Goodman, R. M. (1998). Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chemical Biology 5, R245R249.
Hasman, H., Saputra, D., Sicheritz-Ponten, T., Lund, O., Svendsen, C. A., Frimodt-Moller, N. and Aarestrup, F. M. (2014). Rapid whole-genome sequencing for detection and characterization of microorganisms directly from clinical samples. Journal of Clinical Microbiology 52, 139146.
Karlsson, F. H., Tremaroli, V., Nookaew, I., Bergstrom, G., Behre, C. J., Fagerberg, B., Nielsen, J. and Backhed, F. (2013). Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 498, 99103.
Keller, A., Graefen, A., Ball, M., Matzas, M., Boisguerin, V., Maixner, F., Leidinger, P., Backes, C., Khairat, R., Forster, M., Stade, B., Franke, A., Mayer, J., Spangler, J., McLaughlin, S., Shah, M., Lee, C., Harkins, T. T., Sartori, A., Moreno-Estrada, A., Henn, B., Sikora, M., Semino, O., Chiaroni, J., Rootsi, S., Myres, N. M., Cabrera, V. M., Underhill, P. A., Bustamante, C. D., Vigl, E. E., Samadelli, M., Cipollini, G., Haas, J., Katus, H., O'Connor, B. D., Carlson, M. R., Meder, B., Blin, N., Meese, E., Pusch, C. M. and Zink, A. (2012). New insights into the Tyrolean Iceman's origin and phenotype as inferred by whole-genome sequencing. Nature Communications 3, 698.
Khairat, R., Ball, M., Chang, C. C., Bianucci, R., Nerlich, A. G., Trautmann, M., Ismail, S., Shanab, G. M., Karim, A. M., Gad, Y. Z. and Pusch, C. M. (2013). First insights into the metagenome of Egyptian mummies using next-generation sequencing. Journal of Applied Genetics 54, 309325.
Khaireh, B. A., Assefa, A., Guessod, H. H., Basco, L. K., Khaireh, M. A., Pascual, A., Briolant, S., Bouh, S. M., Farah, I. H., Ali, H. M., Abdi, A. I., Aden, M. O., Abdillahi, Z., Ayeh, S. N., Darar, H. Y., Koeck, J. L., Rogier, C., Pradines, B. and Bogreau, H. (2013). Population genetics analysis during the elimination process of Plasmodium falciparum in Djibouti. Malaria Journal 12, 201.
Kinross, J. M., Darzi, A. W. and Nicholson, J. K. (2011). Gut microbiome-host interactions in health and disease. Genome Medicine 3, 14.
Koch, R. (1881). Zur Untersuchung von pathogenen Organismen. Mitteilungen aus dem Kaiserliche Gesundheitsamte 1, 148.
Lagier, J. C., Armougom, F., Million, M., Hugon, P., Pagnier, I., Robert, C., Bittar, F., Fournous, G., Gimenez, G., Maraninchi, M., Trape, J. F., Koonin, E. V., La Scola, B. and Raoult, D. (2012). Microbial culturomics: paradigm shift in the human gut microbiome study. Clinical Microbiology and Infection 18, 11851193.
Le Chatelier, E., Nielsen, T., Qin, J., Prifti, E., Hildebrand, F., Falony, G., Almeida, M., Arumugam, M., Batto, J. M., Kennedy, S., Leonard, P., Li, J., Burgdorf, K., Grarup, N., Jorgensen, T., Brandslund, I., Nielsen, H. B., Juncker, A. S., Bertalan, M., Levenez, F., Pons, N., Rasmussen, S., Sunagawa, S., Tap, J., Tims, S., Zoetendal, E. G., Brunak, S., Clement, K., Dore, J., Kleerebezem, M., Kristiansen, K., Renault, P., Sicheritz-Ponten, T., de Vos, W. M., Zucker, J. D., Raes, J., Hansen, T., Bork, P., Wang, J., Ehrlich, S. D., Pedersen, O., Guedon, E., Delorme, C., Layec, S., Khaci, G., van de Guchte, M., Vandemeulebrouck, G., Jamet, A., Dervyn, R., Sanchez, N., Maguin, E., Haimet, F., Winogradski, Y., Cultrone, A., Leclerc, M., Juste, C., Blottiere, H., Pelletier, E., LePaslier, D., Artiguenave, F., Bruls, T., Weissenbach, J., Turner, K., Parkhill, J., Antolin, M., Manichanh, C., Casellas, F., Boruel, N., Varela, E., Torrejon, A., Guarner, F., Denariaz, G., Derrien, M., van Hylckama Vlieg, J. E., Veiga, P., Oozeer, R., Knol, J., Rescigno, M., Brechot, C., M'Rini, C., Merieux, A. and Yamada, T. (2013). Richness of human gut microbiome correlates with metabolic markers. Nature 500, 541546.
Lecuit, M. and Eloit, M. (2013). The human virome: new tools and concepts. Trends in Microbiology 21, 510515.
Li, L. and Delwart, E. (2011). From orphan virus to pathogen: the path to the clinical lab. Current Opinion in Virology 1, 282288.
Loman, N. J., Constantinidou, C., Chan, J. Z., Halachev, M., Sergeant, M., Penn, C. W., Robinson, E. R. and Pallen, M. J. (2012). High-throughput bacterial genome sequencing: an embarrassment of choice, a world of opportunity. Nature Reviews Microbiology 10, 599606.
Loman, N. J., Constantinidou, C., Christner, M., Rohde, H., Chan, J. Z., Quick, J., Weir, J. C., Quince, C., Smith, G. P., Betley, J. R., Aepfelbacher, M. and Pallen, M. J. (2013). A culture-independent sequence-based metagenomics approach to the investigation of an outbreak of Shiga-toxigenic Escherichia coli O104:H4. Journal of the American Medical Association 309, 15021510.
Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K. and Knight, R. (2012). Diversity, stability and resilience of the human gut microbiota. Nature 489, 220230.
Maitra, R. D., Kim, J. and Dunbar, W. B. (2012). Recent advances in nanopore sequencing. Electrophoresis 33, 34183428.
McCarthy, C. B., Diambra, L. A. and Rivera Pomar, R. V. (2011). Metagenomic analysis of taxa associated with Lutzomyia longipalpis, vector of visceral leishmaniasis, using an unbiased high-throughput approach. PLoS Neglected Tropical Diseases 5, e1304.
McLean, J. S., Lombardo, M. J., Badger, J. H., Edlund, A., Novotny, M., Yee-Greenbaum, J., Vyahhi, N., Hall, A. P., Yang, Y., Dupont, C. L., Ziegler, M. G., Chitsaz, H., Allen, A. E., Yooseph, S., Tesler, G., Pevzner, P. A., Friedman, R. M., Nealson, K. H., Venter, J. C. and Lasken, R. S. (2013). Candidate phylum TM6 genome recovered from a hospital sink biofilm provides genomic insights into this uncultivated phylum. Proceedings of the National Academy of Sciences USA 110, E2390E2399.
Morgan, X. C. and Huttenhower, C. (2012). Chapter 12: human microbiome analysis. PLoS Computational Biology 8, e1002808.
Nakamura, S., Maeda, N., Miron, I. M., Yoh, M., Izutsu, K., Kataoka, C., Honda, T., Yasunaga, T., Nakaya, T., Kawai, J., Hayashizaki, Y., Horii, T. and Iida, T. (2008). Metagenomic diagnosis of bacterial infections. Emerging Infectious Diseases 14, 17841786.
Nakamura, S., Yang, C. S., Sakon, N., Ueda, M., Tougan, T., Yamashita, A., Goto, N., Takahashi, K., Yasunaga, T., Ikuta, K., Mizutani, T., Okamoto, Y., Tagami, M., Morita, R., Maeda, N., Kawai, J., Hayashizaki, Y., Nagai, Y., Horii, T., Iida, T. and Nakaya, T. (2009). Direct metagenomic detection of viral pathogens in nasal and fecal specimens using an unbiased high-throughput sequencing approach. PLoS One 4, e4219.
Palacios, G., Druce, J., Du, L., Tran, T., Birch, C., Briese, T., Conlan, S., Quan, P. L., Hui, J., Marshall, J., Simons, J. F., Egholm, M., Paddock, C. D., Shieh, W. J., Goldsmith, C. S., Zaki, S. R., Catton, M. and Lipkin, W. I. (2008). A new arenavirus in a cluster of fatal transplant-associated diseases. New England Journal of Medicine 358, 991998.
Peterson, J., Garges, S., Giovanni, M., McInnes, P., Wang, L., Schloss, J. A., Bonazzi, V., McEwen, J. E., Wetterstrand, K. A., Deal, C., Baker, C. C., Di Francesco, V., Howcroft, T. K., Karp, R. W., Lunsford, R. D., Wellington, C. R., Belachew, T., Wright, M., Giblin, C., David, H., Mills, M., Salomon, R., Mullins, C., Akolkar, B., Begg, L., Davis, C., Grandison, L., Humble, M., Khalsa, J., Little, A. R., Peavy, H., Pontzer, C., Portnoy, M., Sayre, M. H., Starke-Reed, P., Zakhari, S., Read, J., Watson, B. and Guyer, M. (2009). The NIH Human Microbiome Project. Genome Research 19, 23172323.
Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C., Nielsen, T., Pons, N., Levenez, F., Yamada, T., Mende, D. R., Li, J., Xu, J., Li, S., Li, D., Cao, J., Wang, B., Liang, H., Zheng, H., Xie, Y., Tap, J., Lepage, P., Bertalan, M., Batto, J. M., Hansen, T., Le Paslier, D., Linneberg, A., Nielsen, H. B., Pelletier, E., Renault, P., Sicheritz-Ponten, T., Turner, K., Zhu, H., Yu, C., Li, S., Jian, M., Zhou, Y., Li, Y., Zhang, X., Li, S., Qin, N., Yang, H., Wang, J., Brunak, S., Dore, J., Guarner, F., Kristiansen, K., Pedersen, O., Parkhill, J., Weissenbach, J., Bork, P., Ehrlich, S. D. and Wang, J. (2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 5965.
Qin, J., Li, Y., Cai, Z., Li, S., Zhu, J., Zhang, F., Liang, S., Zhang, W., Guan, Y., Shen, D., Peng, Y., Zhang, D., Jie, Z., Wu, W., Qin, Y., Xue, W., Li, J., Han, L., Lu, D., Wu, P., Dai, Y., Sun, X., Li, Z., Tang, A., Zhong, S., Li, X., Chen, W., Xu, R., Wang, M., Feng, Q., Gong, M., Yu, J., Zhang, Y., Zhang, M., Hansen, T., Sanchez, G., Raes, J., Falony, G., Okuda, S., Almeida, M., LeChatelier, E., Renault, P., Pons, N., Batto, J. M., Zhang, Z., Chen, H., Yang, R., Zheng, W., Li, S., Yang, H., Wang, J., Ehrlich, S. D., Nielsen, R., Pedersen, O., Kristiansen, K. and Wang, J. (2012). A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490, 5560.
Rappe, M. S. and Giovannoni, S. J. (2003). The uncultured microbial majority. Annual Reviews in Microbiology 57, 369394.
Rogers, G. B., Stressmann, F. A., Walker, A. W., Carroll, M. P. and Bruce, K. D. (2010). Lung infections in cystic fibrosis: deriving clinical insight from microbial complexity. Expert Reviews in Molecular Diagnostics 10, 187196.
Schloissnig, S., Arumugam, M., Sunagawa, S., Mitreva, M., Tap, J., Zhu, A., Waller, A., Mende, D. R., Kultima, J. R., Martin, J., Kota, K., Sunyaev, S. R., Weinstock, G. M. and Bork, P. (2013). Genomic variation landscape of the human gut microbiome. Nature 493, 4550.
Schuenemann, V. J., Singh, P., Mendum, T. A., Krause-Kyora, B., Jager, G., Bos, K. I., Herbig, A., Economou, C., Benjak, A., Busso, P., Nebel, A., Boldsen, J. L., Kjellstrom, A., Wu, H., Stewart, G. R., Taylor, G. M., Bauer, P., Lee, O. Y., Wu, H. H., Minnikin, D. E., Besra, G. S., Tucker, K., Roffey, S., Sow, S. O., Cole, S. T., Nieselt, K. and Krause, J. (2013). Genome-wide comparison of medieval and modern Mycobacterium leprae. Science 341, 179183.
Segata, N., Waldron, L., Ballarini, A., Narasimhan, V., Jousson, O. and Huttenhower, C. (2012). Metagenomic microbial community profiling using unique clade-specific marker genes. Nature Methods 9, 811814.
Seth-Smith, H. M., Harris, S. R., Skilton, R. J., Radebe, F. M., Golparian, D., Shipitsyna, E., Duy, P. T., Scott, P., Cutcliffe, L. T., O'Neill, C., Parmar, S., Pitt, R., Baker, S., Ison, C. A., Marsh, P., Jalal, H., Lewis, D. A., Unemo, M., Clarke, I. N., Parkhill, J. and Thomson, N. R. (2013). Whole-genome sequences of Chlamydia trachomatis directly from clinical samples without culture. Genome Research 23, 855866.
Smits, S. L. and Osterhaus, A. D. (2013). Virus discovery: one step beyond. Current Opinion in Virology doi: 10.1016/j.coviro.2013.03.007. [Epub ahead of print].
Temperton, B. and Giovannoni, S. J. (2012). Metagenomics: microbial diversity through a scratched lens. Current Opinion in Microbiology 15, 605612.
Towner, J. S., Sealy, T. K., Khristova, M. L., Albarino, C. G., Conlan, S., Reeder, S. A., Quan, P. L., Lipkin, W. I., Downing, R., Tappero, J. W., Okware, S., Lutwama, J., Bakamutumaho, B., Kayiwa, J., Comer, J. A., Rollin, P. E., Ksiazek, T. G. and Nichol, S. T. (2008). Newly discovered ebola virus associated with hemorrhagic fever outbreak in Uganda. PLoS Pathogens 4, e1000212.
Turnbaugh, P. J., Ley, R. E., Hamady, M., Fraser-Liggett, C. M., Knight, R. and Gordon, J. I. (2007). The human microbiome project. Nature 449, 804810.
Venter, J. C., Remington, K., Heidelberg, J. F., Halpern, A. L., Rusch, D., Eisen, J. A., Wu, D., Paulsen, I., Nelson, K. E., Nelson, W., Fouts, D. E., Levy, S., Knap, A. H., Lomas, M. W., Nealson, K., White, O., Peterson, J., Hoffman, J., Parsons, R., Baden-Tillson, H., Pfannkoch, C., Rogers, Y. H. and Smith, H. O. (2004). Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 6674.
Victoria, J. G., Kapoor, A., Li, L., Blinkova, O., Slikas, B., Wang, C., Naeem, A., Zaidi, S. and Delwart, E. (2009). Metagenomic analyses of viruses in stool samples from children with acute flaccid paralysis. Journal of Virology 83, 46424651.
Weinstock, G. M. (2012). Genomic approaches to studying the human microbiota. Nature 489, 250256.
Wong, T. H., Dearlove, B. L., Hedge, J., Giess, A. P., Piazza, P., Trebes, A., Paul, J., Smit, E., Smith, E. G., Sutton, J. K., Wilcox, M. H., Dingle, K. E., Peto, T. E., Crook, D. W., Wilson, D. J. and Wyllie, D. H. (2013). Whole genome sequencing and de novo assembly identifies Sydney-like variant noroviruses and recombinants during the winter 2012/2013 outbreak in England. Virology Journal 10, 335.
Wooley, J. C., Godzik, A. and Friedberg, I. (2010). A primer on metagenomics. PLoS Computational Biology 6, e1000667.
Yang, J., Yang, F., Ren, L., Xiong, Z., Wu, Z., Dong, J., Sun, L., Zhang, T., Hu, Y., Du, J., Wang, J. and Jin, Q. (2011). Unbiased parallel detection of viral pathogens in clinical samples by use of a metagenomic approach. Journal of Clinical Microbiology 49, 34633469.


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Diagnostic metagenomics: potential applications to bacterial, viral and parasitic infections

  • M. J. PALLEN (a1)


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