Cited by 2,596Gut microbiota and healthOral microbiology and periodontitis researchMicrobial Community Ecology and Physiology

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Multivariable association discovery in population-scale meta-omics studies

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Mallick, Himel, Rahnavard, Ali, McIver, Lauren J., Ma, Siyuan, Zhang, Yancong, Nguyen, Long H., Tickle, Timothy L., Weingart, George, Ren, Boyu, Schwager, Emma H., Chatterjee, Suvo, Thompson, Kelsey N., Wilkinson, Jeremy E., Subramanian, Ayshwarya, Lu, Yiren, Waldron, Levi, Paulson, Joseph N., Franzosa, Eric A., Bravo, Hector Corrada, Huttenhower, Curtis·2021·PLOS Computational Biology

DOI 10.1371/journal.pcbi.1009442PMC PMC8714082

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Abstract

It is challenging to associate features such as human health outcomes, diet, environmental conditions, or other metadata to microbial community measurements, due in part to their quantitative properties. Microbiome multi-omics are typically noisy, sparse (zero-inflated), high-dimensional, extremely non-normal, and often in the form of count or compositional measurements. Here we introduce an optimized combination of novel and established methodology to assess multivariable association of microbial community features with complex metadata in population-scale observational studies. Our approach, MaAsLin 2 (Microbiome Multivariable Associations with Linear Models), uses generalized linear and mixed models to accommodate a wide variety of modern epidemiological studies, including cross-sectional and longitudinal designs, as well as a variety of data types (e.g., counts and relative abundances) with or without covariates and repeated measurements. To construct this method, we conducted a large-scale evaluation of a broad range of scenarios under which straightforward identification of meta-omics associations can be challenging. These simulation studies reveal that MaAsLin 2's linear model preserves statistical power in the presence of repeated measures and multiple covariates, while accounting for the nuances of meta-omics features and controlling false discovery. We also applied MaAsLin 2 to a microbial multi-omics dataset from the Integrative Human Microbiome (HMP2) project which, in addition to reproducing established results, revealed a unique, integrated landscape of inflammatory bowel diseases (IBD) across multiple time points and omics profiles.

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Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
Love, M. I., Huber, W., & Anders, S. (2014) · Genome Biology · doi:10.1186/s13059-014-0550-8 · Cited by 95,106
Fitting Linear Mixed-Effects Models Using lme4
Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015) · Journal of Statistical Software · doi:10.18637/jss.v067.i01 · Cited by 86,835
<tt>edgeR</tt> : a Bioconductor package for differential expression analysis of digital gene expression data
Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp616 · Cited by 41,364
limma powers differential expression analyses for RNA-sequencing and microarray studies
Ritchie, M. E., Phipson, B., Wu, D., Hu, Y., Law, C. W., Shi, W., & Smyth, G. K. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv007 · Cited by 40,458
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
McMurdie, P. J., & Holmes, S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0061217 · Cited by 21,942
Differential expression analysis for sequence count data
Anders, S., & Huber, W. (2010) · Genome Biology · doi:10.1186/gb-2010-11-10-r106 · Cited by 15,581
Data Analysis
Wickham, H. (2016) · Use R! · doi:10.1007/978-3-319-24277-4_9 · Cited by 12,675
Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments
Smyth, G. K. (2004) · Statistical Applications in Genetics and Molecular Biology · doi:10.2202/1544-6115.1027 · Cited by 11,829
Complex heatmaps reveal patterns and correlations in multidimensional genomic data
Gu, Z., Eils, R., & Schlesner, M. (2016) · Bioinformatics · doi:10.1093/bioinformatics/btw313 · Cited by 10,037

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E Ren BS, 2020, sparseDOSSA: Sparse Data Observations for Simulating Synthetic Abundance, R package version 1.12.0.

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Lugli, G. A., Mancabelli, L., Milani, C., Fontana, F., Tarracchini, C., Alessandri, G., van Sinderen, D., Turroni, F., & Ventura, M. (2023) · npj Biofilms and Microbiomes · doi:10.1038/s41522-023-00392-6 · Cited by 36
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Qi, F., Fan, S., Fang, C., Ge, L., Lyu, J., Huang, Z., Zhao, S., Zou, Y., Huang, L.-T., Liu, X., et al. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1125239 · Cited by 40
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Long, X., Wang, H., Lu, Y., Gao, X., Xiao, Y., Zhang, M., Guo, J., Yang, H. J., Zhang, R., Li, Q., et al. (2025) · Cell Metabolism · doi:10.1016/j.cmet.2025.10.017 · Cited by 37
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Mills, M. C., Lee, S., Piperata, B. A., Garabed, R. B., Choi, B., & Lee, J. (2023) · Microbiome · doi:10.1186/s40168-023-01636-5 · Cited by 32
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Samarra, A., Alcañiz, A. J., Martínez-Costa, C., Marina, A., Comas, I., Segata, N., Quijada, N. M., & Collado, M. C. (2025) · Nature Communications · doi:10.1038/s41467-025-61154-w · Cited by 32
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Tee, M. Z., Er, Y. X., Easton, A. V., Yap, N. J., Lee, I. L., Devlin, J. C., Chen, Z., Ng, K. S., Subramanian, P., Angelova, A. G., et al. (2022) · Microbiome · doi:10.1186/s40168-022-01385-x · Cited by 32
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Karl, J. P., Whitney, C. C., Wilson, M. A., Fagnant, H. S., Radcliffe, P. N., Chakraborty, N., Campbell, R., Hoke, A. V., Gautam, A., Hammamieh, R., et al. (2023) · Scientific Reports · doi:10.1038/s41598-023-27463-0 · Cited by 34
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Huang, X., Chen, C., Xie, W., Zhou, C., Tian, X. W., Zhang, Z., Wang, Q., Chang, H., Xiao, W., Zhang, R., et al. (2023) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2023.06.2515 · Cited by 32
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Rosell‐Mases, E., Santiago, A., Corral-Pujol, M., Yáñez, F., Varela, E., Egia‐Mendikute, L., Arpa, B., Cosovanu, C., Panosa, A., Serrano-Gómez, G., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-43652-x · Cited by 33
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Pötgens, S. A., Havelange, V., Lecop, S., Li, F., Neyrinck, A. M., Bindels, F., Neveux, N., Demoulin, J., Moors, I., Kerre, T. C. C., et al. (2024) · Haematologica · doi:10.3324/haematol.2023.284138 · Cited by 33

Authors: Mallick, H., Rahnavard, A., McIver, L. J., Ma, S., Zhang, Y., Nguyen, L. H., Tickle, T. L., Weingart, G., Ren, B., Schwager, E. H., Chatterjee, S., Thompson, K. N., Wilkinson, J. E., Subramanian, A., Lu, Y., Waldron, L., Paulson, J. N., Franzosa, E. A., Bravo, H. C., & Huttenhower, C.
Affiliations: Broad Institute (US)
George Washington University (US)
Harvard University (US)
National Institutes of Health (US)
City University of New York (US)
Genentech (US)
Corresponding author: Huttenhower, Curtis
ORCID: Mallick, Himel
Rahnavard, Ali
McIver, Lauren J.
Ma, Siyuan
Zhang, Yancong
Nguyen, Long H.
Tickle, Timothy L.
Ren, Boyu
Schwager, Emma H.
Chatterjee, Suvo
Thompson, Kelsey N.
Wilkinson, Jeremy E.
Subramanian, Ayshwarya
Waldron, Levi
Paulson, Joseph N.
Franzosa, Eric A.
Huttenhower, Curtis
Venue: PLOS Computational Biology
Publisher: Public Library of Science (PLoS)
Published: 2021-11-16
Volume: 17
Issue: 11
Pages: e1009442
ISSN: 1553-734X (ISSN-L)
1553-7358
DOI: 10.1371/journal.pcbi.1009442
PMC: PMC8714082
OpenAlex: W3211779138
Cited by: 2,596
References: 71
Citations by year: 2026: 564 · 2025: 721 · 2024: 611 · 2023: 378 · 2022: 220 · 2021: 91
FWCI: 107.10
Type: journal article
Language: en
Update notices: new_version (2021-12-28)
Open access: gold
doi.org
Licence: public-domain
creativecommons.org/publicdomain/zero/1.0/ (vor)
Locations: PLoS Computational Biology (publishedVersion, public-domain)
bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, public-domain)
PubMed Central (publishedVersion, public-domain)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: US National Science Foundation, Division of Environmental Biology (DEB 2028280)
national institute of allergy and infectious diseases (U19AI110820)
national human genome research institute (R01HG005220)
national institute of diabetes and digestive and kidney diseases (R24DK110499, U54DK102557)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
Keywords: generalized linear models, mixed models, compositional data, count data, zero-inflated data, repeated measures, false discovery rate control, statistical power, inflammatory bowel disease
MeSH terms: Gastrointestinal Microbiome, Computer Simulation, Humans, Inflammatory Bowel Diseases, Multivariate Analysis, Computational Biology

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