Systems biology approaches towards predictive microbial ecology

Otwell, Anne E.; López García de Lomana, Adrián; Gibbons, Sean M.; Orellana, Mónica V.; Baliga, Nitin S.

doi:10.1111/1462-2920.14378

Title: Systems biology approaches towards predictive microbial ecology

Journal Article · 18 October 2018 · Environmental Microbiology

DOI: https://doi.org/10.1111/1462-2920.14378 · OSTI ID:1777943

Otwell, Anne E. ^[1]; López García de Lomana, Adrián ^[1]; Gibbons, Sean M. ^[2]; Orellana, Mónica V. ^[2]; Baliga, Nitin S. ^[3]

Institute for Systems Biology, Seattle, WA (United States)
Institute for Systems Biology, Seattle, WA (United States); Univ. of Washington, Seattle, WA (United States)
Institute for Systems Biology, Seattle, WA (United States); Univ. of Washington, Seattle, WA (United States) ; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Through complex interspecies interactions, microbial processes drive nutrient cycling and biogeochemistry. However, we still struggle to predict specifically which organisms, communities and biotic and abiotic processes are determining ecosystem function and how environmental changes will alter their roles and stability. While the tools to create such a predictive microbial ecology capability exist, cross-disciplinary integration of high-resolution field measurements, detailed laboratory studies and computation is essential. In this perspective, we emphasize the importance of pursuing a multiscale, systems approach to iteratively link ecological processes measured in the field to testable hypotheses that drive high-throughput laboratory experimentation. Mechanistic understanding of microbial processes gained in controlled lab systems will lead to the development of theory that can be tested back in the field. Using N₂ O production as an example, we review the current status of field and laboratory research and layout a plausible path to the kind of integration that is needed to enable prediction of how N-cycling microbial communities will respond to environmental changes. We advocate for the development of realistic and predictive gene regulatory network models for environmental responses that extend from single-cell resolution to ecosystems, which is essential to understand how microbial communities involved in N₂ O production and consumption will respond to future environmental conditions.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1777943

Journal Information:: Environmental Microbiology, Journal Name: Environmental Microbiology Journal Issue: 12 Vol. 20; ISSN 1462-2912

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

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Year-Round Shotgun Metagenomes Reveal Stable Microbial Communities in Agricultural Soils and Novel Ammonia Oxidizers Responding to Fertilization Orellana, Luis H.; Chee-Sanford, Joanne C.; Sanford, Robert A. Applied and Environmental Microbiology, Vol. 84, Issue 2 https://doi.org/10.1128/AEM.01646-17	journal	November 2017
Insights into the Effect of Soil pH on N2O and N2 Emissions and Denitrifier Community Size and Activity Cuhel, J.; Simek, M.; Laughlin, R. J. Applied and Environmental Microbiology, Vol. 76, Issue 6 https://doi.org/10.1128/AEM.02484-09	journal	January 2010
Transcriptome of a Nitrosomonas europaea Mutant with a Disrupted Nitrite Reductase Gene (nirK) Cho, C. M. -H.; Yan, T.; Liu, X. Applied and Environmental Microbiology, Vol. 72, Issue 6 https://doi.org/10.1128/AEM.02958-05	journal	June 2006
High-Throughput Metagenomic Technologies for Complex Microbial Community Analysis: Open and Closed Formats Zhou, Jizhong; He, Zhili; Yang, Yunfeng mBio, Vol. 6, Issue 1 https://doi.org/10.1128/mBio.02288-14	journal	January 2015
Genome-Scale, Constraint-Based Modeling of Nitrogen Oxide Fluxes during Coculture of Nitrosomonas europaea and Nitrobacter winogradskyi Mellbye, Brett L.; Giguere, Andrew T.; Murthy, Ganti S. mSystems, Vol. 3, Issue 3 https://doi.org/10.1128/mSystems.00170-17	journal	March 2018
Nitrogen Cycle of the Open Ocean: From Genes to Ecosystems Zehr, Jonathan P.; Kudela, Raphael M. Annual Review of Marine Science, Vol. 3, Issue 1 https://doi.org/10.1146/annurev-marine-120709-142819	journal	January 2011
Establishment and metabolic analysis of a model microbial community for understanding trophic and electron accepting interactions of subsurface anaerobic environments Miller, Lance D.; Mosher, Jennifer J.; Venkateswaran, Amudhan BMC Microbiology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2180-10-149	journal	January 2010
Transcriptional program for nitrogen starvation-induced lipid accumulation in Chlamydomonas reinhardtii López García de Lomana, Adrián; Schäuble, Sascha; Valenzuela, Jacob Biotechnology for Biofuels, Vol. 8, Issue 1 https://doi.org/10.1186/s13068-015-0391-z	journal	December 2015
Predominant but Previously-overlooked Prokaryotic Drivers of Reductive Nitrogen Transformation in Paddy Soils, Revealed by Metatranscriptomics Masuda, Yoko; Itoh, Hideomi; Shiratori, Yutaka Microbes and environments, Vol. 32, Issue 2 https://doi.org/10.1264/jsme2.ME16179	journal	January 2017
Nitrogen substrate–dependent nitrous oxide cycling in salt marsh sediments Ji, Qixing; Babbin, Andrew R.; Peng, Xuefeng Journal of Marine Research, Vol. 73, Issue 3 https://doi.org/10.1357/002224015815848820	journal	May 2015
Inference of Gene Regulatory Network Based on Local Bayesian Networks Liu, Fei; Zhang, Shao-Wu; Guo, Wei-Feng PLOS Computational Biology, Vol. 12, Issue 8 https://doi.org/10.1371/journal.pcbi.1005024	journal	August 2016
Two dynamic regimes in the human gut microbiome Gibbons, Sean M.; Kearney, Sean M.; Smillie, Chris S. PLOS Computational Biology, Vol. 13, Issue 2 https://doi.org/10.1371/journal.pcbi.1005364	journal	February 2017
Combining inferred regulatory and reconstructed metabolic networks enhances phenotype prediction in yeast Wang, Zhuo; Danziger, Samuel A.; Heavner, Benjamin D. PLOS Computational Biology, Vol. 13, Issue 5 https://doi.org/10.1371/journal.pcbi.1005489	journal	May 2017
Identifying Keystone Species in the Human Gut Microbiome from Metagenomic Timeseries Using Sparse Linear Regression Fisher, Charles K.; Mehta, Pankaj PLoS ONE, Vol. 9, Issue 7 https://doi.org/10.1371/journal.pone.0102451	journal	July 2014
Intergenomic Comparisons Highlight Modularity of the Denitrification Pathway and Underpin the Importance of Community Structure for N2O Emissions Graf, Daniel R. H.; Jones, Christopher M.; Hallin, Sara PLoS ONE, Vol. 9, Issue 12 https://doi.org/10.1371/journal.pone.0114118	journal	December 2014
From the Ground Up: Global Nitrous Oxide Sources are Constrained by Stable Isotope Values Snider, David M.; Venkiteswaran, Jason J.; Schiff, Sherry L. PLOS ONE, Vol. 10, Issue 3 https://doi.org/10.1371/journal.pone.0118954	journal	March 2015
A system‐level model for the microbial regulatory genome Brooks, Aaron N.; Reiss, David J.; Allard, Antoine Molecular Systems Biology, Vol. 10, Issue 7 https://doi.org/10.15252/msb.20145160	journal	July 2014
Mechanism for microbial population collapse in a fluctuating resource environment Turkarslan, Serdar; Raman, Arjun V.; Thompson, Anne W. Molecular Systems Biology, Vol. 13, Issue 3 https://doi.org/10.15252/msb.20167058	journal	March 2017
Deciphering microbial interactions in synthetic human gut microbiome communities Venturelli, Ophelia S.; Carr, Alex V.; Fisher, Garth Molecular Systems Biology, Vol. 14, Issue 6 https://doi.org/10.15252/msb.20178157	journal	June 2018
DAYCENT National-Scale Simulations of Nitrous Oxide Emissions from Cropped Soils in the United States Del Grosso, S. J.; Parton, W. J.; Mosier, A. R. Journal of Environment Quality, Vol. 35, Issue 4 https://doi.org/10.2134/jeq2005.0160	journal	January 2006
Community composition of ammonia-oxidizing archaea from surface and anoxic depths of oceanic oxygen minimum zones Peng, Xuefeng; Jayakumar, Amal; Ward, Bess B. Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00177	journal	January 2013
Deciphering microbial interactions and detecting keystone species with co-occurrence networks Berry, David; Widder, Stefanie Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00219	journal	May 2014
Genome-Wide Discovery of Putative sRNAs in Paracoccus denitrificans Expressed under Nitrous Oxide Emitting Conditions Gaimster, Hannah; Chalklen, Lisa; Alston, Mark Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01806	journal	November 2016
Community Composition of Nitrous Oxide Consuming Bacteria in the Oxygen Minimum Zone of the Eastern Tropical South Pacific Sun, Xin; Jayakumar, Amal; Ward, Bess B. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01183	journal	June 2017
Mechanisms of Chromium and Uranium Toxicity in Pseudomonas stutzeri RCH2 Grown under Anaerobic Nitrate-Reducing Conditions Thorgersen, Michael P.; Lancaster, W. Andrew; Ge, Xiaoxuan Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01529	journal	August 2017
Niche Partitioning of the N Cycling Microbial Community of an Offshore Oxygen Deficient Zone Fuchsman, Clara A.; Devol, Allan H.; Saunders, Jaclyn K. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02384	journal	December 2017
Exploring the Denitrification Proteome of Paracoccus denitrificans PD1222 Olaya-Abril, Alfonso; Hidalgo-Carrillo, Jesús; Luque-Almagro, Víctor M. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01137	journal	May 2018
Top-down estimates of European CH ₄ and N ₂ O emissions based on four different inverse models Bergamaschi, P.; Corazza, M.; Karstens, U. Atmospheric Chemistry and Physics, Vol. 15, Issue 2 https://doi.org/10.5194/acp-15-715-2015	journal	January 2015
Constraining a complex biogeochemical model for CO ₂ and N ₂ O emission simulations from various land uses by model–data fusion Houska, Tobias; Kraus, David; Kiese, Ralf Biogeosciences, Vol. 14, Issue 14 https://doi.org/10.5194/bg-14-3487-2017	journal	January 2017
Production of oceanic nitrous oxide by ammonia-oxidizing archaea Löscher, C. R.; Kock, A.; Könneke, M. Biogeosciences, Vol. 9, Issue 7 https://doi.org/10.5194/bg-9-2419-2012	journal	January 2012
Metagenomic analysis of nitrogen and methane cycling in the Arabian Sea oxygen minimum zone Lüke, Claudia; Speth, Daan R.; Kox, Martine A. R. PeerJ, Vol. 4 https://doi.org/10.7717/peerj.1924	journal	January 2016

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