DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Linking soil biology and chemistry in biological soil crust using isolate exometabolomics

Journal Article · · Nature Communications
ORCiD logo [1]; ORCiD logo [2];  [3];  [4];  [4]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Climate and Ecosystems Sciences Division
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division; USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Metagenomic sequencing provides a window into microbial community structure and metabolic potential; however, linking these data to exogenous metabolites that microorganisms process and produce (the exometabolome) remains challenging. Previously, we observed strong exometabolite niche partitioning among bacterial isolates from biological soil crust (biocrust). For this study, we examine native biocrust to determine if these patterns are reproduced in the environment. Overall, most soil metabolites display the expected relationship (positive or negative correlation) with four dominant bacteria following a wetting event and across biocrust developmental stages. For metabolites that were previously found to be consumed by an isolate, 70% are negatively correlated with the abundance of the isolate's closest matching environmental relative in situ, whereas for released metabolites, 67% were positively correlated. Our results demonstrate that metabolite profiling, shotgun sequencing and exometabolomics may be successfully integrated to functionally link microbial community structure with environmental chemistry in biocrust.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC02-05CH11231; S10 OD018174
OSTI ID:
1434034
Journal Information:
Nature Communications, Vol. 9, Issue 1; Related Information: © 2017 The Author(s).; ISSN 2041-1723
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 98 works
Citation information provided by
Web of Science

References (111)

Non-cyanobacterial diazotrophs mediate dinitrogen fixation in biological soil crusts during early crust formation journal June 2015
The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter journal February 2002
Analysis of Metabolomics Datasets with High-Performance Computing and Metabolite Atlases journal July 2015
Climate-smart soils journal April 2016
Accurate, multi-kb reads resolve complex populations and detect rare microorganisms journal February 2015
Comparison of methods for extraction of organic N monomers from soil microbial biomass journal February 2015
Revisiting N2 fixation in Guerrero Negro intertidal microbial mats with a functional single-cell approach journal October 2014
Genome-Wide Experimental Determination of Barriers to Horizontal Gene Transfer journal November 2007
Agricultural Management and Labile Carbon Additions Affect Soil Microbial Community Structure and Interact with Carbon and Nitrogen Cycling journal April 2013
Persistence of soil organic matter as an ecosystem property journal October 2011
Contribution of cryptogamic covers to the global cycles of carbon and nitrogen journal June 2012
Diverse, uncultivated bacteria and archaea underlying the cycling of dissolved protein in the ocean journal March 2016
Micron-scale mapping of sulfur cycling across the oxycline of a cyanobacterial mat: a paired nanoSIMS and CARD-FISH approach journal June 2008
The circadian oscillator in Synechococcus elongatus controls metabolite partitioning during diurnal growth journal March 2015
Responses of soil bacterial and fungal communities to extreme desiccation and rewetting journal July 2013
Microbiomes in light of traits: A phylogenetic perspective journal November 2015
Exometabolomics and MSI: deconstructing how cells interact to transform their small molecule environment journal August 2015
OptCom: A Multi-Level Optimization Framework for the Metabolic Modeling and Analysis of Microbial Communities journal February 2012
Proposed minimum reporting standards for chemical analysis: Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI) journal September 2007
Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups journal June 2012
Metabolic Footprinting of Mutant Libraries to Map Metabolite Utilization to Genotype journal October 2012
Phylogenomics of prokaryotic ribosomal proteins journal January 2011
Roles of Bacillus endospores in the environment journal March 2002
Cyanobacterial reuse of extracellular organic carbon in microbial mats journal October 2015
Temperature Drives the Continental-Scale Distribution of Key Microbes in Topsoil Communities journal June 2013
Persistence of soil organic matter as an ecosystem property text January 2011
Microbial regulation of the soil carbon cycle: evidence from gene–enzyme relationships journal May 2016
Nutritional flexibility of oligotrophic and copiotrophic Antarctic bacteria with respect to organic substrates journal January 1989
Molecular-Scale Investigation with ESI-FT-ICR-MS on Fractionation of Dissolved Organic Matter Induced by Adsorption on Iron Oxyhydroxides journal February 2016
Soil fertility is associated with fungal and bacterial richness, whereas pH is associated with community composition in polar soil microbial communities journal November 2014
Nitrogen cycling in desert biological soil crusts across biogeographic regions in the Southwestern United States journal March 2011
Exometabolite niche partitioning among sympatric soil bacteria journal September 2015
A simple, fast, and accurate method of phylogenomic inference journal January 2008
A trait-based approach for modelling microbial litter decomposition journal May 2012
Increasing aridity reduces soil microbial diversity and abundance in global drylands journal December 2015
Dispersing misconceptions and identifying opportunities for the use of 'omics' in soil microbial ecology journal June 2015
Metabolic interactions in microbial communities: untangling the Gordian knot journal October 2015
A Multiscale, Hierarchical Model of Pulse Dynamics in Arid-Land Ecosystems journal November 2014
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system journal October 2016
Integrated metagenomics and network analysis of soil microbial community of the forest timberline journal January 2015
A Multiscale, Hierarchical Model of Pulse Dynamics in Arid-Land Ecosystems journal November 2014
Organic matter transformations in the upper mesopelagic zone of the North Pacific: Chemical composition and linkages to microbial community structure: ORGANIC MATTER IN THE UPPER MESOPELAGIC journal January 2012
Nutritional flexibility of oligotrophic and copiotrophic Antarctic bacteria with respect to organic substrates journal January 1989
Climate–Carbon Cycle Feedback Analysis: Results from the C 4 MIP Model Intercomparison journal July 2006
Phylogenomics of Prokaryotic Ribosomal Proteins journal May 2012
Dynamic substrate preferences predict metabolic properties of a simple microbial consortium journal January 2017
The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes preprint March 2016
Microbial Succession and Flavor Production in the Fermented Dairy Beverage Kefir journal October 2016
METLIN: A Metabolite Mass Spectral Database journal January 2005
Microbiomes in light of traits: A phylogenetic perspective journal November 2015
The Evolution of a Capacity to Build Supra-Cellular Ropes Enabled Filamentous Cyanobacteria to Colonize Highly Erodible Substrates journal November 2009
Contribution of cryptogamic covers to the global cycles of carbon and nitrogen journal June 2012
Untargeted soil metabolomics methods for analysis of extractable organic matter journal January 2015
The generation and maintenance of diversity in microbial communities journal March 2011
Cohesion: a method for quantifying the connectivity of microbial communities journal July 2017
Climate change and physical disturbance cause similar community shifts in biological soil crusts journal September 2015
Exometabolomics and MSI: deconstructing how cells interact to transform their small molecule environment journal August 2015
Climate-smart soils journal April 2016
Analysis of Metabolomics Datasets with High-Performance Computing and Metabolite Atlases journal July 2015
Micron-scale mapping of sulfur cycling across the oxycline of a cyanobacterial mat: a paired nanoSIMS and CARD-FISH approach journal June 2008
Competitive sorption of microbial metabolites on an iron oxide mineral journal November 2015
Accurate, multi-kb reads resolve complex populations and detect rare microorganisms journal February 2015
Comparison of methods for extraction of organic N monomers from soil microbial biomass journal February 2015
Membrane transporter engineering in industrial biotechnology and whole cell biocatalysis journal April 2015
Genome-Wide Experimental Determination of Barriers to Horizontal Gene Transfer journal November 2007
Microbial regulation of the soil carbon cycle: evidence from gene–enzyme relationships journal May 2016
Untargeted soil metabolomics methods for analysis of extractable organic matter journal January 2015
Variation in Dissolved Organic Matter Controls Bacterial Production and Community Composition journal August 2006
Metabolic Footprinting of Mutant Libraries to Map Metabolite Utilization to Genotype journal October 2012
The role of soil microbes in the global carbon cycle: tracking the below-ground microbial processing of plant-derived carbon for manipulating carbon dynamics in agricultural systems: Role of soil microbes in global carbon cycle: carbon tracking & agro-cosystem management journal March 2014
OptCom: A Multi-Level Optimization Framework for the Metabolic Modeling and Analysis of Microbial Communities journal February 2012
Dynamic substrate preferences predict metabolic properties of a simple microbial consortium journal January 2017
Time-Resolved Metabolic Footprinting for Nonlinear Modeling of Bacterial Substrate Utilization journal February 2009
Community genomics in microbial ecology and evolution journal June 2005
Body Shaping under Water Stress: Osmosensing and Osmoregulation of Solute Transport in Bacteria journal May 2002
Cytological Analysis of the Mother Cell Death Process during Sporulation in Bacillus subtilis journal January 2007
Climate change and physical disturbance cause similar community shifts in biological soil crusts journal September 2015
Roles of Bacillus endospores in the environment journal March 2002
The generation and maintenance of diversity in microbial communities journal March 2011
Responses of soil bacterial and fungal communities to extreme desiccation and rewetting journal July 2013
Persistence of soil organic matter as an ecosystem property journal October 2011
Dynamic cyanobacterial response to hydration and dehydration in a desert biological soil crust journal June 2013
A new view of the tree of life journal April 2016
The circadian oscillator in Synechococcus elongatus controls metabolite partitioning during diurnal growth journal March 2015
MetaboLights—an open-access general-purpose repository for metabolomics studies and associated meta-data journal October 2012
Agricultural Management and Labile Carbon Additions Affect Soil Microbial Community Structure and Interact with Carbon and Nitrogen Cycling journal April 2013
Soil fertility is associated with fungal and bacterial richness, whereas pH is associated with community composition in polar soil microbial communities journal November 2014
Exometabolite niche partitioning among sympatric soil bacteria journal September 2015
Structure and Functioning of Dryland Ecosystems in a Changing World text January 2016
The Evolution of a Capacity to Build Supra-Cellular Ropes Enabled Filamentous Cyanobacteria to Colonize Highly Erodible Substrates journal November 2009
Increasing aridity reduces soil microbial diversity and abundance in global drylands journal December 2015
Cyanobacteria track water in desert soils journal September 2001
Cohesion: a method for quantifying the connectivity of microbial communities journal July 2017
Molecular-Scale Investigation with ESI-FT-ICR-MS on Fractionation of Dissolved Organic Matter Induced by Adsorption on Iron Oxyhydroxides journal February 2016
METLIN: A Metabolite Mass Spectral Database journal January 2005
Dispersing misconceptions and identifying opportunities for the use of 'omics' in soil microbial ecology journal June 2015
Phylogenomics of Prokaryotic Ribosomal Proteins journal May 2012
Resistance of Bacillus Endospores to Extreme Terrestrial and Extraterrestrial Environments journal September 2000
Structure and Functioning of Dryland Ecosystems in a Changing World journal November 2016
Proposed minimum reporting standards for chemical analysis: Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI) journal September 2007
MetaboLights—an open-access general-purpose repository for metabolomics studies and associated meta-data journal October 2012
The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes preprint March 2016
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system journal October 2016
Nutrient cross-feeding in the microbial world journal July 2014
What is flux balance analysis? journal March 2010
Metabolic interactions in microbial communities: untangling the Gordian knot journal October 2015
A trait-based approach for modelling microbial litter decomposition journal May 2012
Biological Soil Crusts as an Organizing Principle in Drylands book January 2016
A simple, fast, and accurate method of phylogenomic inference journal January 2008
A new view of the tree of life journal April 2016
Nutrient cross-feeding in the microbial world journal July 2014

Cited By (20)

Biocrust science and global change journal May 2019
Characteristics of Wetting-Induced Bacteriophage Blooms in Biological Soil Crust journal December 2019
Defining trait-based microbial strategies with consequences for soil carbon cycling under climate change journal September 2019
Bio‐priming seeds with cyanobacteria: effects on native plant growth and soil properties journal November 2019
Root renovation: how an improved understanding of basic root biology could inform the development of elite crops that foster sustainable soil health journal January 2019
Characteristics of Wetting-Induced Bacteriophage Blooms in Biological Soil Crust journal December 2019
Spatial segregation of the biological soil crust microbiome around its foundational cyanobacterium, Microcoleus vaginatus, and the formation of a nitrogen-fixing cyanosphere journal April 2019
Evaluation of an untargeted nano-liquid chromatography-mass spectrometry approach to expand coverage of low molecular weight dissolved organic matter in Arctic soil journal April 2019
Costless metabolic secretions as drivers of interspecies interactions in microbial ecosystems journal January 2019
Assessing the influence of soil abiotic and biotic factors on Nostoc commune inoculation success journal August 2019
Microbial Group Dynamics in Plant Rhizospheres and Their Implications on Nutrient Cycling journal July 2018
Populations of Populus angustifolia have evolved distinct metabolic profiles that influence their surrounding soil journal February 2020
Revisiting microbe-metabolite interactions: doing better than random text January 2019
The known and the unknown in soil microbial ecology journal January 2019
Biofilms 2018: a Diversity of Microbes and Mechanisms journal February 2019
Learning representations of microbe–metabolite interactions journal November 2019
Microbial Group Dynamics in Plant Rhizospheres and Their Implications on Nutrient Cycling journal July 2018
The Ecology of Subaerial Biofilms in Dry and Inhospitable Terrestrial Environments journal September 2019
Costless metabolic secretions as drivers of interspecies interactions in microbial ecosystems journal January 2019
Common principles and best practices for engineering microbiomes journal September 2019