Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-14T17:11:41.276Z Has data issue: false hasContentIssue false

Combining integrated systems-biology approaches with intervention-based experimental design provides a higher-resolution path forward for microbiome research

Published online by Cambridge University Press:  15 July 2019

J. Alfredo Blakeley-Ruiz
Affiliation:
Oak Ridge National Laboratory, Oak Ridge, TN 37830. hettichrl@ornl.gov University of Tennessee–Knoxville, Knoxville, TN 37996. jblakele@vols.utk.edurlydic@utk.eduhbaghdoy@utk.edu
Carlee S. McClintock
Affiliation:
Pain Consultants of East Tennessee, P.L.L.C., Knoxville, TN 37909. cmcclintock@painconsultants.comjchoo@painconsultants.com
Ralph Lydic
Affiliation:
Oak Ridge National Laboratory, Oak Ridge, TN 37830. hettichrl@ornl.gov University of Tennessee–Knoxville, Knoxville, TN 37996. jblakele@vols.utk.edurlydic@utk.eduhbaghdoy@utk.edu
Helen A. Baghdoyan
Affiliation:
Oak Ridge National Laboratory, Oak Ridge, TN 37830. hettichrl@ornl.gov University of Tennessee–Knoxville, Knoxville, TN 37996. jblakele@vols.utk.edurlydic@utk.eduhbaghdoy@utk.edu
James J. Choo
Affiliation:
Pain Consultants of East Tennessee, P.L.L.C., Knoxville, TN 37909. cmcclintock@painconsultants.comjchoo@painconsultants.com
Robert L. Hettich
Affiliation:
Oak Ridge National Laboratory, Oak Ridge, TN 37830. hettichrl@ornl.gov University of Tennessee–Knoxville, Knoxville, TN 37996. jblakele@vols.utk.edurlydic@utk.eduhbaghdoy@utk.edu

Abstract

The Hooks et al. review of microbiota-gut-brain (MGB) literature provides a constructive criticism of the general approaches encompassing MGB research. This commentary extends their review by: (a) highlighting capabilities of advanced systems-biology “-omics” techniques for microbiome research and (b) recommending that combining these high-resolution techniques with intervention-based experimental design may be the path forward for future MGB research.

Type
Open Peer Commentary
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bravo, J. A., Forsythe, P., Chew, M. V., Escaravage, E., Savignac, H. M., Dinan, T. G., Bienenstock, J. & Cryan, J. F. (2011) Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proceedings of the National Academy of Sciences USA 108(38):16050–55. Available at: https://doi.org/10.1073/pnas.1102999108.Google Scholar
Brown, C. T., Xiong, W., Olm, M. R., Thomas, B. C., Baker, R., Firek, B., Morowitz, M. J., Hettich, R. L. & Banfield, J. F. (2018) Hospitalized premature infants are colonized by related bacterial strains with distinct proteomic profiles. mBio 9:e0044118.Google Scholar
Caspi, R., Billington, R., Fulcher, C. A., Keseler, I. M., Kothari, A., Krummenacker, M., Latendresse, M., Midford, P. E., Ong, Q., Ong, W. K., Paley, S., Subhraveti, P. & Karp, P. D. (2018) The MetaCyc database of metabolic pathways and enzymes. Nucleic Acids Research 46(D1):D63339. Available at: https://doi.org/10.1093/nar/gkx935.Google Scholar
David, L. A., Maurice, C. F., Carmody, R. N., Gootenberg, D. B., Button, J. E., Wolfe, B. E., Ling, A. V., Devlin, A. S., Varma, Y., Fischbach, M. A., Biddinger, S. B., Dutton, R. J. & Turnbaugh, P. J. (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505(7484):559–63. Available at: https://doi.org/10.1038/nature12820.Google Scholar
Erickson, A. R., Cantarel, B. L., Lamendella, R., Darzi, Y., Mongodin, E. F., Pan, C., Shah, M., Halfvarson, J., Tysk, C., Henrissat, B., Raes, J., Verberkmoes, N. C., Fraser, C. M., Hettich, R. L. & Jansson, J. K. (2012) Integrated metagenomics/metaproteomics reveals human host-microbiota signatures of Crohn's disease. PLoS ONE 7(11):e49138. Available at: https://doi.org/10.1371/journal.pone.0049138.Google Scholar
Halfvarson, J., Brislawn, C. J., Lamendella, R., Vázquez-Baeza, Y., Walters, W. A., Bramer, L. M., D'Amato, M., Bonfiglio, F., McDonald, D., Gonzalez, A., McClure, E. E., Dunklegarger, M. F., Knight, R. & Jansson, J. K. (2017) Dynamics of the human gut microbiome in inflammatory bowel disease. Nature Microbiology 2:17004. Available at: https://doi.org/10.1038/nmicrobiol.2017.4.Google Scholar
Heijtz, R. D., Wang, S., Anuar, F., Qian, Y., Björkholm, B., Samuelsson, A., Hibberd, M. L., Forssberg, H. & Pettersson, S. (2011) Normal gut microbiota modulates brain development and behavior. Proceedings of the National Academy of Sciences of the USA 108(7):3047–52.Google Scholar
Hsiao, E. Y., McBride, S. W., Hsien, S., Sharon, G., Hyde, E. R., McCue, T., Codelli, J. A., Chow, J., Reisman, S. E., Petrosino, J. F., Patterson, P. H. & Mazmanian, S. K. (2013) Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155:1451–63. Available at: https://doi.org/10.1016/j.cell.2013.11.024.Google Scholar
Human Microbiome Project Consortium (2012) Structure, function and diversity of the healthy human microbiome. Nature 486(7402):207–14. Available at: https://doi.org/10.1038/nature11234.Google Scholar
Jorth, P., Turner, K. H., Gumus, P., Nizam, N., Buduneli, N. & Whiteley, M. (2014) Metatranscriptomics of the human oral microbiome during health and disease. mBio 5(2):e01012-14.Google Scholar
Kanehisa, M., Sato, Y., Kawashima, M., Furumichi, M. & Tanabe, M. (2016) KEGG as a reference resource for gene and protein annotation. Nucleic Acids Research 44(D1):D45762. Available at: https://doi.org/10.1093/nar/gkv1070.Google Scholar
Kang, D. D., Froula, J., Egan, R. & Wange, Z. (2015) MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ 3:e1165. Available at: https://doi.org/10.7717/peerj.1165.Google Scholar
Karu, N., Deng, L., Slae, M., Guo, A. C., Sajed, T., Huynh, H., Wine, E. & Wishart, D. S. (2018) A review on human fecal metabolomics: Methods, applications and the human fecal metabolome database. Analytica Chimica Acta 1030:124. Available at: https://doi.org/10.1016/j.aca.2018.05.031.Google Scholar
Knight, R., Vrbanac, A., Taylor, B. C., Aksenov, A., Callewaert, C., Debelius, J., Gonzalez, A., Kosciolek, T., McCall, L.-I., McDonald, D., Melnik, A. V., Morton, J. T., Navas, J., Quinn, R. A., Sanders, J. G., Swafford, A. D., Thompson, L. R., Tripathi, A., Xu, Z. Z., Zaneveld, J. R., Zhu, Q., Caporaso, J. G. & Dorrestein, P. C. (2018) Best practices for analysing microbiomes. Nature Reviews Microbiology 16(7):410–22. Available at: https://doi.org/10.1038/s41579-018-0029-9.Google Scholar
Song, S. J., Lauber, C., Costello, E. K., Lozupone, C. A., Humphrey, G., Berg-Lyons, D., Caporaso, J. G., Knights, D., Clemente, J. C., Nakielny, S., Gordon, J. I., Fierer, N. & Knight, R. (2013) Cohabiting family members share microbiota with one another and with their dogs. eLife 2:e00458. Available at: https://doi.org/10.7554/eLife.00458.Google Scholar
Stewart, C. J., Ajami, N. J., O'Brien, J. L., Hutchinson, D. S., Smith, D. P., Wong, M. C., Ross, M. C., Lloyd, R. E., Doddapaneni, H. V., Metcalf, G. A., Muzny, D., Gibbs, R. A., Vatanen, T., Huttenhower, C., Xavier, R. J., Rewers, M., Hagopian, W., Toppari, J., Ziegler, A.-G., She, J.-X., Akolkar, B., Lernmark, A., Hyoty, H., Vehik, K., Krischer, J. P. & Petrosino, J. F. (2018) Temporal development of the gut microbiome in early childhood from the TEDDY study. Nature 562(7728):583–88. Available at: https://doi.org/10.1038/s41586-018-0617-x.Google Scholar
Sudo, N., Chida, Y., Aiba, Y., Sonoda, J., Oyama, N., Yu, X.-N., Kubo, C. & Koga, Y. (2004) Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. Journal of Physiology 558(1):263–75. Available at: https://doi.org/10.1113/jphysiol.2004.063388.Google Scholar
Sze, M. A. & Schloss, P. D. (2016) Looking for a signal in the noise: Revisiting obesity and the microbiome. mBio 7:e01018-16. Available at: https://doi.org/10.1128/mBio.01018-16.Google Scholar
Xiong, W., Brown, C. T., Morowitz, M. J., Banfield, J. F. & Hettich, R. L. (2017) Genome-resolved metaproteomic characterization of preterm infant gut microbiota development reveals species-specific metabolic shifts and variabilities during early life. Microbiome 5:72. Available at: https://doi.org/10.1186/s40168-017-0290-6.Google Scholar
Yatsunenko, T., Rey, F. E., Manary, M. J., Trehan, I., Dominguez-Bello, M. G., Contreras, M., Magris, M., Hidalgo, G., Baldassano, R. N., Anokhin, A. P., Heath, A. C., Warner, B., Reeder, J., Kuczynski, J., Caporaso, J. G., Lozupone, C. A., Lauber, C., Clemente, J. C., Knights, D., Knight, R. & Gordon, J. I. (2012) Human gut microbiome viewed across age and geography. Nature 486(7402):222–27. Available at: https://doi.org/10.1038/nature11053.Google Scholar