Linking Associations of Rare Low-Abundance Species to Their Environments by Association Networks
Abstract
Studies of microbial communities by targeted sequencing of rRNA genes lead to recovering numerous rare low-abundance taxa with unknown biological roles. We propose to study associations of such rare organisms with their environments by a computational framework based on transformation of the data into qualitative variables. Namely, we analyze the sparse table of putative species or OTUs (operational taxonomic units) and samples generated in such studies, also known as an OTU table, by collecting statistics on co-occurrences of the species and on shared species richness across samples. Based on the statistics we built two association networks, of the rare putative species and of the samples respectively, using a known computational technique, Association networks (Anets) developed for analysis of qualitative data. Clusters of samples and clusters of OTUs are then integrated and combined with metadata of the study to produce a map of associated putative species in their environments. We tested and validated the framework on two types of microbiomes, of human body sites and that of the Populus tree root systems. We show that in both studies the associations of OTUs can separate samples according to environmental or physiological characteristics of the studied systems.
- Authors:
-
- The Univ. of Texas MD Anderson Cancer Center, Houston, TX (United States). Dept. of Genomic Medicine; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
- The Univ. of Texas MD Anderson Cancer Center, Houston, TX (United States). Dept. of Surgical Oncology; Univ. of Texas School of Public Health, Dallas, TX (United States). Dept. of Epidemiology, Human Genetics and Environmental Sciences
- The Univ. of Texas MD Anderson Cancer Center, Houston, TX (United States). Dept. of Genomic Medicine. Dept. of Surgical Oncology
- The Univ. of Texas MD Anderson Cancer Center, Houston, TX (United States). Dept. of Genomic Medicine
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division; Univ. of Tennessee, Knoxville, TN (United States). Dept. of Microbiology
- Publication Date:
- Research Org.:
- The Univ. of Texas MD Anderson Cancer Center, Houston, TX (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1427603
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Microbiology
- Additional Journal Information:
- Journal Volume: 9; Journal ID: ISSN 1664-302X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; metagenome; microbiome; unsupervised analysis; alpha and beta diversity; sparse data; Anets; qualitative data
Citation Formats
Karpinets, Tatiana V., Gopalakrishnan, Vancheswaran, Wargo, Jennifer, Futreal, Andrew P., Schadt, Christopher W., and Zhang, Jianhua. Linking Associations of Rare Low-Abundance Species to Their Environments by Association Networks. United States: N. p., 2018.
Web. doi:10.3389/fmicb.2018.00297.
Karpinets, Tatiana V., Gopalakrishnan, Vancheswaran, Wargo, Jennifer, Futreal, Andrew P., Schadt, Christopher W., & Zhang, Jianhua. Linking Associations of Rare Low-Abundance Species to Their Environments by Association Networks. United States. https://doi.org/10.3389/fmicb.2018.00297
Karpinets, Tatiana V., Gopalakrishnan, Vancheswaran, Wargo, Jennifer, Futreal, Andrew P., Schadt, Christopher W., and Zhang, Jianhua. Wed .
"Linking Associations of Rare Low-Abundance Species to Their Environments by Association Networks". United States. https://doi.org/10.3389/fmicb.2018.00297. https://www.osti.gov/servlets/purl/1427603.
@article{osti_1427603,
title = {Linking Associations of Rare Low-Abundance Species to Their Environments by Association Networks},
author = {Karpinets, Tatiana V. and Gopalakrishnan, Vancheswaran and Wargo, Jennifer and Futreal, Andrew P. and Schadt, Christopher W. and Zhang, Jianhua},
abstractNote = {Studies of microbial communities by targeted sequencing of rRNA genes lead to recovering numerous rare low-abundance taxa with unknown biological roles. We propose to study associations of such rare organisms with their environments by a computational framework based on transformation of the data into qualitative variables. Namely, we analyze the sparse table of putative species or OTUs (operational taxonomic units) and samples generated in such studies, also known as an OTU table, by collecting statistics on co-occurrences of the species and on shared species richness across samples. Based on the statistics we built two association networks, of the rare putative species and of the samples respectively, using a known computational technique, Association networks (Anets) developed for analysis of qualitative data. Clusters of samples and clusters of OTUs are then integrated and combined with metadata of the study to produce a map of associated putative species in their environments. We tested and validated the framework on two types of microbiomes, of human body sites and that of the Populus tree root systems. We show that in both studies the associations of OTUs can separate samples according to environmental or physiological characteristics of the studied systems.},
doi = {10.3389/fmicb.2018.00297},
journal = {Frontiers in Microbiology},
number = ,
volume = 9,
place = {United States},
year = {Wed Mar 07 00:00:00 EST 2018},
month = {Wed Mar 07 00:00:00 EST 2018}
}
Web of Science
Works referenced in this record:
Error filtering, pair assembly and error correction for next-generation sequencing reads
journal, July 2015
- Edgar, Robert C.; Flyvbjerg, Henrik
- Bioinformatics, Vol. 31, Issue 21
Ecology and exploration of the rare biosphere
journal, March 2015
- Lynch, Michael D. J.; Neufeld, Josh D.
- Nature Reviews Microbiology, Vol. 13, Issue 4
Microbial diversity in the deep sea and the underexplored "rare biosphere"
journal, July 2006
- Sogin, M. L.; Morrison, H. G.; Huber, J. A.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 32
Where less may be more: how the rare biosphere pulls ecosystems strings
journal, January 2017
- Jousset, Alexandre; Bienhold, Christina; Chatzinotas, Antonis
- The ISME Journal, Vol. 11, Issue 4
Accurate, multi-kb reads resolve complex populations and detect rare microorganisms
journal, February 2015
- Sharon, Itai; Kertesz, Michael; Hug, Laura A.
- Genome Research, Vol. 25, Issue 4
Analyzing large biological datasets with association networks
journal, May 2012
- Karpinets, Tatiana V.; Park, Byung H.; Uberbacher, Edward C.
- Nucleic Acids Research, Vol. 40, Issue 17
At Least 1 in 20 16S rRNA Sequence Records Currently Held in Public Repositories Is Estimated To Contain Substantial Anomalies
journal, December 2005
- Ashelford, K. E.; Chuzhanova, N. A.; Fry, J. C.
- Applied and Environmental Microbiology, Vol. 71, Issue 12
Cluster analysis and display of genome-wide expression patterns
journal, December 1998
- Eisen, M. B.; Spellman, P. T.; Brown, P. O.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 25
Compositional data analysis of the microbiome: fundamentals, tools, and challenges
journal, May 2016
- Tsilimigras, Matthew C. B.; Fodor, Anthony A.
- Annals of Epidemiology, Vol. 26, Issue 5
gCoda: Conditional Dependence Network Inference for Compositional Data
journal, July 2017
- Fang, Huaying; Huang, Chengcheng; Zhao, Hongyu
- Journal of Computational Biology, Vol. 24, Issue 7
Differential abundance analysis for microbial marker-gene surveys
journal, September 2013
- Paulson, Joseph N.; Stine, O. Colin; Bravo, Héctor Corrada
- Nature Methods, Vol. 10, Issue 12
Waste Not, Want Not: Why Rarefying Microbiome Data Is Inadmissible
journal, April 2014
- McMurdie, Paul J.; Holmes, Susan
- PLoS Computational Biology, Vol. 10, Issue 4
VEGAN, a package of R functions for community ecology
journal, April 2003
- Dixon, Philip
- Journal of Vegetation Science, Vol. 14, Issue 6
Inferring Correlation Networks from Genomic Survey Data
journal, September 2012
- Friedman, Jonathan; Alm, Eric J.
- PLoS Computational Biology, Vol. 8, Issue 9
Sparse and Compositionally Robust Inference of Microbial Ecological Networks
journal, May 2015
- Kurtz, Zachary D.; Müller, Christian L.; Miraldi, Emily R.
- PLOS Computational Biology, Vol. 11, Issue 5
The Genus Inocybe in Montana Aspen Stands
journal, July 1997
- Cripps, Cathy L.
- Mycologia, Vol. 89, Issue 4
Dynamics and associations of microbial community types across the human body
journal, April 2014
- Ding, Tao; Schloss, Patrick D.
- Nature, Vol. 509, Issue 7500
Graph Clustering Via a Discrete Uncoupling Process
journal, January 2008
- Van Dongen, Stijn
- SIAM Journal on Matrix Analysis and Applications, Vol. 30, Issue 1
Species abundance distributions and richness estimations in fungal metagenomics - lessons learned from community ecology: COMMUNITY ECOLOGY IN FUNGAL METAGENOMICS
journal, December 2010
- Unterseher, Martin; Jumpponen, Ari; ÖPik, Maarja
- Molecular Ecology, Vol. 20, Issue 2
The Rare Bacterial Biosphere
journal, January 2012
- Pedrós-Alió, Carlos
- Annual Review of Marine Science, Vol. 4, Issue 1
Response of the rare biosphere to environmental stressors in a highly diverse ecosystem (Zodletone spring, OK, USA)
journal, January 2015
- Coveley, Suzanne; Elshahed, Mostafa S.; Youssef, Noha H.
- PeerJ, Vol. 3
The Multiple Forms of the Interspecific Abundance-Distribution Relationship
journal, June 1996
- Gaston, Kevin J.
- Oikos, Vol. 76, Issue 2
The Contribution of Rare Species to Community Phylogenetic Diversity across a Global Network of Forest Plots
journal, July 2012
- Mi, Xiangcheng; Swenson, Nathan G.; Valencia, Renato
- The American Naturalist, Vol. 180, Issue 1
Exact sequence variants should replace operational taxonomic units in marker-gene data analysis
journal, July 2017
- Callahan, Benjamin J.; McMurdie, Paul J.; Holmes, Susan P.
- The ISME Journal, Vol. 11, Issue 12
Reducing the Effects of PCR Amplification and Sequencing Artifacts on 16S rRNA-Based Studies
journal, December 2011
- Schloss, Patrick D.; Gevers, Dirk; Westcott, Sarah L.
- PLoS ONE, Vol. 6, Issue 12
VEGAN, a package of R functions for community ecology
journal, January 2003
- Dixon, Philip
- Journal of Vegetation Science, Vol. 14, Issue 6
Systems Analysis of Gut Microbiome Influence on Metabolic Disease in HIV-Positive and High-Risk Populations
journal, June 2021
- Armstrong, Abigail J. S.; Quinn, Kevin; Fouquier, Jennifer
- mSystems, Vol. 6, Issue 3
Where less may be more: how the rare biosphere pulls ecosystems strings
text, January 2017
- Jousset, Alexandre; Rillig, Matthias C.; Bienhold, Christina
- Freie Universität Berlin
Waste Not, Want Not: Why Rarefying Microbiome Data is Inadmissible
text, January 2013
- McMurdie, Paul J.; Holmes, Susan
- arXiv
Sparse and compositionally robust inference of microbial ecological networks
text, January 2014
- Kurtz, Zachary D.; Mueller, Christian L.; Miraldi, Emily R.
- arXiv
Compositional data analysis of the microbiome: fundamentals, tools, and challenges
journal, May 2016
- Tsilimigras, Matthew C. B.; Fodor, Anthony A.
- Annals of Epidemiology, Vol. 26, Issue 5
The Unified Neutral Theory of Biodiversity and Biogeography at Age Ten
journal, July 2011
- Rosindell, James; Hubbell, Stephen P.; Etienne, Rampal S.
- Trends in Ecology & Evolution, Vol. 26, Issue 7
The human microbiome: there is much left to do
journal, June 2022
- Ley, Ruth
- Nature, Vol. 606, Issue 7914
Emergence of structural and dynamical properties of ecological mutualistic networks
journal, August 2013
- Suweis, Samir; Simini, Filippo; Banavar, Jayanth R.
- Nature, Vol. 500, Issue 7463
Differential abundance analysis for microbial marker-gene surveys
journal, September 2013
- Paulson, Joseph N.; Stine, O. Colin; Bravo, Héctor Corrada
- Nature Methods, Vol. 10, Issue 12
DADA2: High-resolution sample inference from Illumina amplicon data
journal, May 2016
- Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J.
- Nature Methods, Vol. 13, Issue 7
QIIME allows analysis of high-throughput community sequencing data
journal, April 2010
- Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
- Nature Methods, Vol. 7, Issue 5
Microbial diversity in the deep sea and the underexplored "rare biosphere"
journal, July 2006
- Sogin, M. L.; Morrison, H. G.; Huber, J. A.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 32
The nested assembly of plant-animal mutualistic networks
journal, July 2003
- Bascompte, J.; Jordano, P.; Melian, C. J.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 16
The Contribution of Rare Species to Community Phylogenetic Diversity across a Global Network of Forest Plots
journal, July 2012
- Mi, Xiangcheng; Swenson, Nathan G.; Valencia, Renato
- The American Naturalist, Vol. 180, Issue 1
gCoda: Conditional Dependence Network Inference for Compositional Data
journal, July 2017
- Fang, Huaying; Huang, Chengcheng; Zhao, Hongyu
- Journal of Computational Biology, Vol. 24, Issue 7
Cytoscape 2.8: new features for data integration and network visualization
journal, December 2010
- Smoot, M. E.; Ono, K.; Ruscheinski, J.
- Bioinformatics, Vol. 27, Issue 3
Error filtering, pair assembly and error correction for next-generation sequencing reads
journal, July 2015
- Edgar, Robert C.; Flyvbjerg, Henrik
- Bioinformatics, Vol. 31, Issue 21
Analyzing large biological datasets with association networks
journal, May 2012
- Karpinets, Tatiana V.; Park, Byung H.; Uberbacher, Edward C.
- Nucleic Acids Research, Vol. 40, Issue 17
The Human Microbiome Project strategy for comprehensive sampling of the human microbiome and why it matters
journal, November 2012
- Aagaard, Kjersti; Petrosino, Joseph; Keitel, Wendy
- The FASEB Journal, Vol. 27, Issue 3
Accurate, multi-kb reads resolve complex populations and detect rare microorganisms
journal, February 2015
- Sharon, Itai; Kertesz, Michael; Hug, Laura A.
- Genome Research, Vol. 25, Issue 4
VEGAN, a package of R functions for community ecology
journal, April 2003
- Dixon, Philip
- Journal of Vegetation Science, Vol. 14, Issue 6
Assessing and Improving Methods Used in Operational Taxonomic Unit-Based Approaches for 16S rRNA Gene Sequence Analysis
journal, March 2011
- Schloss, Patrick D.; Westcott, Sarah L.
- Applied and Environmental Microbiology, Vol. 77, Issue 10
At Least 1 in 20 16S rRNA Sequence Records Currently Held in Public Repositories Is Estimated To Contain Substantial Anomalies
journal, December 2005
- Ashelford, K. E.; Chuzhanova, N. A.; Fry, J. C.
- Applied and Environmental Microbiology, Vol. 71, Issue 12
Graph Clustering Via a Discrete Uncoupling Process
journal, January 2008
- Van Dongen, Stijn
- SIAM Journal on Matrix Analysis and Applications, Vol. 30, Issue 1
Microbial Co-occurrence Relationships in the Human Microbiome
journal, July 2012
- Faust, Karoline; Sathirapongsasuti, J. Fah; Izard, Jacques
- PLoS Computational Biology, Vol. 8, Issue 7
Inferring Correlation Networks from Genomic Survey Data
journal, September 2012
- Friedman, Jonathan; Alm, Eric J.
- PLoS Computational Biology, Vol. 8, Issue 9
Fine-Scale Bacterial Beta Diversity within a Complex Ecosystem (Zodletone Spring, OK, USA): The Role of the Rare Biosphere
journal, August 2010
- Youssef, Noha H.; Couger, M. B.; Elshahed, Mostafa S.
- PLoS ONE, Vol. 5, Issue 8
Reducing the Effects of PCR Amplification and Sequencing Artifacts on 16S rRNA-Based Studies
journal, December 2011
- Schloss, Patrick D.; Gevers, Dirk; Westcott, Sarah L.
- PLoS ONE, Vol. 6, Issue 12
Dirichlet Multinomial Mixtures: Generative Models for Microbial Metagenomics
journal, February 2012
- Holmes, Ian; Harris, Keith; Quince, Christopher
- PLoS ONE, Vol. 7, Issue 2
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
journal, April 2013
- McMurdie, Paul J.; Holmes, Susan
- PLoS ONE, Vol. 8, Issue 4
A Multifactor Analysis of Fungal and Bacterial Community Structure in the Root Microbiome of Mature Populus deltoides Trees
journal, October 2013
- Shakya, Migun; Gottel, Neil; Castro, Hector
- PLoS ONE, Vol. 8, Issue 10
The Genus Inocybe in Montana Aspen Stands
journal, July 1997
- Cripps, Cathy L.
- Mycologia, Vol. 89, Issue 4
Waste Not, Want Not: Why Rarefying Microbiome Data is Inadmissible
text, January 2013
- McMurdie, Paul J.; Holmes, Susan
- arXiv
Sparse and compositionally robust inference of microbial ecological networks
text, January 2014
- Kurtz, Zachary D.; Mueller, Christian L.; Miraldi, Emily R.
- arXiv
Works referencing / citing this record:
Understanding the Mechanisms Behind the Response to Environmental Perturbation in Microbial Mats: A Metagenomic-Network Based Approach
journal, November 2018
- De Anda, Valerie; Zapata-Peñasco, Icoquih; Blaz, Jazmín
- Frontiers in Microbiology, Vol. 9