A novel analysis method for paired-sample microbial ecology experiments

Olesen, Scott W.; Vora, Suhani; Techtmann, Stephen M.; Fortney, Julian L.; Bastidas-Oyanedel, Juan R.; Rodriguez, Jorge; Hazen, Terry C.; Alm, Eric J.; Humbert, Jean -Francois

doi:10.1371/journal.pone.0154804

Title: A novel analysis method for paired-sample microbial ecology experiments

Journal Article · Fri May 06 00:00:00 EDT 2016 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0154804· OSTI ID:1327714

^[1]; Vora, Suhani ^[1]; Techtmann, Stephen M. ^[2]; Fortney, Julian L. ^[3]; Bastidas-Oyanedel, Juan R. ^[4]; Rodriguez, Jorge ^[4]; Hazen, Terry C. ^[3]; Alm, Eric J. ^[1]; Humbert, Jean -Francois ^[5]

Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
Univ. of Tennessee, Knoxville, TN (United States)
Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Masdar Institute of Science and Technology, Abu Dhabi (United Arab Emirates)
INRA (France)

This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Many microbial ecology experiments use sequencing data to measure a community's response to an experimental treatment. In a common experimental design, two units, one control and one experimental, are sampled before and after the treatment is applied to the experimental unit. The four resulting samples contain information about the dynamics of organisms that respond to the treatment, but there are no analytical methods designed to extract exactly this type of information from this configuration of samples. Here we present an analytical method specifically designed to visualize and generate hypotheses about microbial community dynamics in experiments that have paired samples and few or no replicates. The method is based on the Poisson lognormal distribution, long studied in macroecology, which we found accurately models the abundance distribution of taxa counts from 16S rRNA surveys. To demonstrate the method's validity and potential, we analyzed an experiment that measured the effect of crude oil on ocean microbial communities in microcosm. Our method identified known oil degraders as well as two clades, Maricurvus and Rhodobacteraceae, that responded to amendment with oil but do not include known oil degraders. Our approach is sensitive to organisms that increased in abundance only in the experimental unit but less sensitive to organisms that increased in both control and experimental units, thus mitigating the role of "bottle effects".

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC05-00OR22725; AC02-05CH11231

OSTI ID:: 1327714

Alternate ID(s):: OSTI ID: 1480721

Journal Information:: PLoS ONE, Vol. 11, Issue 5; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 5 works

Citation information provided by
Web of Science

References (40)

Non-parametric multivariate analyses of changes in community structure Clarke, K. R. Austral Ecology, Vol. 18, Issue 1 https://doi.org/10.1111/j.1442-9993.1993.tb00438.x	journal	March 1993
Associations between species and groups of sites: indices and statistical inference Cáceres, Miquel De; Legendre, Pierre Ecology, Vol. 90, Issue 12 https://doi.org/10.1890/08-1823.1	journal	December 2009
Maricurvus nonylphenolicus gen. nov., sp. nov., a nonylphenol-degrading bacterium isolated from seawater Iwaki, Hiroaki; Takada, Kengo; Hasegawa, Yoshie FEMS Microbiology Letters, Vol. 327, Issue 2 https://doi.org/10.1111/j.1574-6968.2011.02471.x	journal	December 2011
Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB DeSantis, T. Z.; Hugenholtz, P.; Larsen, N. Applied and Environmental Microbiology, Vol. 72, Issue 7, p. 5069-5072 https://doi.org/10.1128/AEM.03006-05	journal	July 2006
Hypothesis Testing and Power Calculations for Taxonomic-Based Human Microbiome Data La Rosa, Patricio S.; Brooks, J. Paul; Deych, Elena PLoS ONE, Vol. 7, Issue 12 https://doi.org/10.1371/journal.pone.0052078	journal	December 2012
Development of membrane inlet mass spectrometry for examination of fermentation processes Bastidas-Oyanedel, Juan-Rodrigo; Mohd-Zaki, Zuhaida; Pratt, Steven Talanta, Vol. 83, Issue 2 https://doi.org/10.1016/j.talanta.2010.09.034	journal	December 2010
Multivariate analyses in microbial ecology: Multivariate analyses in microbial ecology Ramette, Alban FEMS Microbiology Ecology, Vol. 62, Issue 2 https://doi.org/10.1111/j.1574-6941.2007.00375.x	journal	November 2007
PyNAST: a flexible tool for aligning sequences to a template alignment Caporaso, J. G.; Bittinger, K.; Bushman, F. D. Bioinformatics, Vol. 26, Issue 2 https://doi.org/10.1093/bioinformatics/btp636	journal	November 2009
DNA-based stable isotope probing coupled with cultivation methods implicates Methylophaga in hydrocarbon degradation Mishamandani, Sara; Gutierrez, Tony; Aitken, Michael D. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00076	journal	January 2014
Effects of crude oil on marine microbial communities in short term outdoor microcosms Jung, Seung Won; Park, Joon Sang; Kown, Oh Youn The Journal of Microbiology, Vol. 48, Issue 5 https://doi.org/10.1007/s12275-010-0199-2	journal	October 2010
Database indexing for production MegaBLAST searches Morgulis, Aleksandr; Coulouris, George; Raytselis, Yan Bioinformatics, Vol. 24, Issue 16 https://doi.org/10.1093/bioinformatics/btn322	journal	June 2008
Species abundance distributions: moving beyond single prediction theories to integration within an ecological framework McGill, Brian J.; Etienne, Rampal S.; Gray, John S. Ecology Letters, Vol. 10, Issue 10 https://doi.org/10.1111/j.1461-0248.2007.01094.x	journal	October 2007
Aestuariicella hydrocarbonica gen. nov., sp. nov., an aliphatic hydrocarbon-degrading bacterium isolated from a sea tidal flat Kim, Kyung Hyun; Baek, Kyunghwa; Jia, Baolei International Journal of Systematic and Evolutionary Microbiology, Vol. 65, Issue 6 https://doi.org/10.1099/ijs.0.000199	journal	June 2015
Estimating prokaryotic diversity and its limits Curtis, T. P.; Sloan, W. T.; Scannell, J. W. Proceedings of the National Academy of Sciences, Vol. 99, Issue 16, p. 10494-10499 https://doi.org/10.1073/pnas.142680199	journal	July 2002
The lognormal distribution is not an appropriate null hypothesis for the species-abundance distribution Williamson, Mark; J. Gaston, Kevin Journal of Animal Ecology, Vol. 74, Issue 3 https://doi.org/10.1111/j.1365-2656.2005.00936.x	journal	May 2005
Compositional data in Community Ecology: the Paradigm or Peril of Proportions? Jackson, Donald A. Ecology, Vol. 78, Issue 3 https://doi.org/10.1890/0012-9658(1997)078[0929:CDICET]2.0.CO;2	journal	April 1997
The Unique Chemistry of Eastern Mediterranean Water Masses Selects for Distinct Microbial Communities by Depth Techtmann, Stephen M.; Fortney, Julian L.; Ayers, Kati A. PLOS ONE, Vol. 10, Issue 3 https://doi.org/10.1371/journal.pone.0120605	journal	March 2015
Transcriptional response of bathypelagic marine bacterioplankton to the Deepwater Horizon oil spill Rivers, Adam R.; Sharma, Shalabh; Tringe, Susannah G. The ISME Journal, Vol. 7, Issue 12 https://doi.org/10.1038/ismej.2013.129	journal	August 2013
Canonical Analysis of Principal Coordinates: a Useful Method of Constrained Ordination for Ecology Anderson, Marti J.; Willis, Trevor J. Ecology, Vol. 84, Issue 2 https://doi.org/10.1890/0012-9658(2003)084[0511:CAOPCA]2.0.CO;2	journal	February 2003
Incorporating 16S Gene Copy Number Information Improves Estimates of Microbial Diversity and Abundance Kembel, Steven W.; Wu, Martin; Eisen, Jonathan A. PLoS Computational Biology, Vol. 8, Issue 10 https://doi.org/10.1371/journal.pcbi.1002743	journal	October 2012
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P. PLoS ONE, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pone.0009490	journal	March 2010
APE: Analyses of Phylogenetics and Evolution in R language Paradis, E.; Claude, J.; Strimmer, K. Bioinformatics, Vol. 20, Issue 2 https://doi.org/10.1093/bioinformatics/btg412	journal	January 2004
Analyzing Spatial Structure of Communities Using the Two‐Dimensional Poisson Lognormal Species Abundance Model Engen, Steinar; Lande, Russell; Walla, Thomas The American Naturalist, Vol. 160, Issue 1 https://doi.org/10.1086/340612	journal	July 2002
The metagenomics RAST server – a public resource for the automatic phylogenetic and functional analysis of metagenomes Meyer, F.; Paarmann, D.; D'Souza, M. BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-386	journal	September 2008
Bias problems in culture-independent analysis of environmental bacterial communities: a representative study on hydrocarbonoclastic bacteria Al-Awadhi, Husain; Dashti, Narjis; Khanafer, Majida SpringerPlus, Vol. 2, Issue 1 https://doi.org/10.1186/2193-1801-2-369	journal	January 2013
A Bayesian framework for the analysis of microarray expression data: regularized t -test and statistical inferences of gene changes Baldi, P.; Long, A. D. Bioinformatics, Vol. 17, Issue 6 https://doi.org/10.1093/bioinformatics/17.6.509	journal	June 2001
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons Haas, B. J.; Gevers, D.; Earl, A. M. Genome Research, Vol. 21, Issue 3 https://doi.org/10.1101/gr.112730.110	journal	January 2011
Patterns of relative species abundance in rainforests and coral reefs Volkov, Igor; Banavar, Jayanth R.; Hubbell, Stephen P. Nature, Vol. 450, Issue 7166 https://doi.org/10.1038/nature06197	journal	November 2007
UPARSE: highly accurate OTU sequences from microbial amplicon reads Edgar, Robert C. Nature Methods, Vol. 10, Issue 10 https://doi.org/10.1038/nmeth.2604	journal	August 2013
Inferring Correlation Networks from Genomic Survey Data Friedman, Jonathan; Alm, Eric J. PLoS Computational Biology, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pcbi.1002687	journal	September 2012
Site-specific molecular analysis of the bacteriota on worn spectacles Fritz, Birgit; März, Melanie; Weis, Severin Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-62186-6	journal	March 2020
Comparative analysis of racial differences in breast tumor microbiome Thyagarajan, Srikantha; Zhang, Yan; Thapa, Santosh Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-71102-x	journal	August 2020
Error filtering, pair assembly and error correction for next-generation sequencing reads Edgar, Robert C.; Flyvbjerg, Henrik Bioinformatics, Vol. 31, Issue 21 https://doi.org/10.1093/bioinformatics/btv401	journal	July 2015
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy Wang, Q.; Garrity, G. M.; Tiedje, J. M. Applied and Environmental Microbiology, Vol. 73, Issue 16 https://doi.org/10.1128/aem.00062-07	journal	June 2007
Distribution-Based Clustering: Using Ecology To Refine the Operational Taxonomic Unit Preheim, Sarah P.; Perrotta, Allison R.; Martin-Platero, Antonio M. Applied and Environmental Microbiology, Vol. 79, Issue 21 https://doi.org/10.1128/aem.00342-13	journal	August 2013
Critical Evaluation of the Volumetric "Bottle Effect" on Microbial Batch Growth Hammes, F.; Vital, M.; Egli, T. Applied and Environmental Microbiology, Vol. 76, Issue 4 https://doi.org/10.1128/aem.01914-09	journal	December 2009
The Expected Frequencies in a Sample of an Animal Population in Which the Abundances of Species are Log-Normally Distributed. Part I Grundy, P. M. Biometrika, Vol. 38, Issue 3/4 https://doi.org/10.2307/2332589	journal	December 1951
On Fitting the Poisson Lognormal Distribution to Species-Abundance Data Bulmer, M. G. Biometrics, Vol. 30, Issue 1 https://doi.org/10.2307/2529621	journal	March 1974
Species Assemblages and Indicator Species: The Need for a Flexible Asymmetrical Approach Dufrene, Marc; Legendre, Pierre Ecological Monographs, Vol. 67, Issue 3 https://doi.org/10.2307/2963459	journal	August 1997

Cited By (3)

Generalized Hotelling's test for paired compositional data with application to human microbiome studies Zhao, Ni; Zhan, Xiang; Guthrie, Katherine A. Genetic Epidemiology, Vol. 42, Issue 5 https://doi.org/10.1002/gepi.22127	journal	May 2018
Profiling Living Bacteria Informs Preparation of Fecal Microbiota Transplantations Chu, Nathaniel D.; Smith, Mark B.; Perrotta, Allison R. PLOS ONE, Vol. 12, Issue 1 https://doi.org/10.1371/journal.pone.0170922	journal	January 2017
Oil Hydrocarbon Degradation by Caspian Sea Microbial Communities Miller, John I.; Techtmann, Stephen; Fortney, Julian Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00995	journal	May 2019

Similar Records

Macroecological distributions of gene variants highlight the functional organization of soil microbial systems

Journal Article · Mon Sep 27 00:00:00 EDT 2021 · The ISME Journal · OSTI ID:1327714

Escalas, Arthur; Paula, Fabiana S.; Guilhaumon, François; +7 more

Carbon Amendments Alter Microbial Community Structure and Net Mercury Methylation Potential in Sediments

Journal Article · Thu Feb 01 00:00:00 EST 2018 · Applied and Environmental Microbiology · OSTI ID:1327714

Christensen, Geoff A.; Somenahally, Anil C.; Moberly, James G.; +11 more

The Utility of Macroecological Rules for Microbial Biogeography

Journal Article · Thu Apr 01 00:00:00 EDT 2021 · Frontiers in Ecology and Evolution · OSTI ID:1327714

Dickey, Jonathan R.; Swenie, Rachel A.; Turner, Sophia C.; +6 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
oils
microbial ecology
probability distribution
community ecology
crude oil
oceans
sequence databases
sequence alignment

Title: A novel analysis method for paired-sample microbial ecology experiments

Citation Formats

References (40)

Cited By (3)

Similar Records

Related Subjects