Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Common principles and best practices for engineering microbiomes

Journal Article · · Nature Reviews Microbiology
 [1];  [2];  [3];  [4];  [5];  [6];  [7];  [8];  [9];  [8];  [10];  [11];  [8]
  1. Univ. of Wisconsin-Madison, Madison, WI (United States); Unniversity of Wisconsin-Madison Department of Civil and Environmental Engineering
  2. Univ. of Minnesota, Saint Paul, MN (United States)
  3. Montana State Univ., Bozeman, MT (United States)
  4. Purdue Univ., West Lafayette, IN (United States)
  5. Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  6. Univ. of California, Santa Barbara, CA (United States); DOE Joint Bioenergy Inst., Emeryville, CA (United States)
  7. DOE Joint Bioenergy Inst., Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); DOE Agile BioFoundry, Emeryville, CA (United States); Basque Center for Applied Mathematics, Bilbao (Spain)
  8. Univ. of Wisconsin-Madison, Madison, WI (United States)
  9. Univ. of Michigan, Ann Arbor, MI (United States)
  10. Delft Univ. of Technology, Delft (Netherlands)
  11. Univ. of Wisconsin-Madison, Madison, WI (United States); DOE Great Lakes Bioenergy Research Center, Madison, WI (United States)
Despite broad scientific interest in harnessing the power of Earth’s microbiomes, knowledge gaps hinder their efficient use for addressing urgent societal and environmental challenges. We argue that structuring research and technology developments around a design–build–test–learn (DBTL) cycle will advance microbiome engineering and spur new discoveries of the basic scientific principles governing microbiome function. In this Review, we present key elements of an iterative DBTL cycle for microbiome engineering, focusing on generalizable approaches, including top-down and bottom-up design processes, synthetic and self-assembled construction methods, and emerging tools to analyse microbiome function. These approaches can be used to harness microbiomes for broad applications related to medicine, agriculture, energy and the environment. We also discuss key challenges and opportunities of each approach and synthesize them into best practice guidelines for engineering microbiomes. Here, we anticipate that adoption of a DBTL framework will rapidly advance microbiome-based biotechnologies aimed at improving human and animal health, agriculture and enabling the bioeconomy.
Research Organization:
Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); USDOE Agile BioFoundry, Emeryville, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Sponsoring Organization:
Gordon and Betty Moore Foundation; National Science Foundation (NSF); Natural Sciences and Engineering Research Council of Canada (NSERC); Swiss National Science Foundation; USDOD; USDOE Office of Energy Efficiency and Renewable Energy (EERE), Bioenergy Technologies Office; USDOE Office of Energy Efficiency and Renewable Energy (EERE), Transportation Office. Bioenergy Technologies Office; USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC02-05CH11231; AC05-00OR22725; SC0018409
OSTI ID:
1579360
Alternate ID(s):
OSTI ID: 1823327
Journal Information:
Nature Reviews Microbiology, Journal Name: Nature Reviews Microbiology Journal Issue: 12 Vol. 17; ISSN 1740-1526
Publisher:
Springer NatureCopyright Statement
Country of Publication:
United States
Language:
English

References (177)

Characterization of TAP Ambr 250 disposable bioreactors, as a reliable scale-down model for biologics process development: Characterization and Application of Ambr 250 in Clone Selection and Process Development journal February 2017
Microbial Resource Management: The Road To Go for Environmental Biotechnology journal April 2007
Microbial community engineering for biopolymer production from glycerol journal June 2011
Co-cultivation of the anaerobic fungus Anaeromyces robustus with Methanobacterium bryantii enhances transcription of carbohydrate active enzymes journal May 2019
Mathematical modelling of anaerobic digestion processes: applications and future needs journal August 2015
Engineering the rhizosphere: Expressing a bias journal March 1996
The effect of liquid upward velocity and hydraulic retention time on granulation in UASB reactors treating wastewater with a high sulphate content journal January 1993
The essential role of hydrodynamic shear force in the formation of biofilm and granular sludge journal April 2002
Diversity and dynamics of microbial communities in engineered environments and their implications for process stability journal June 2003
Mechanistic modelling of in vitro fermentation and methane production by rumen microbiota journal October 2016
Design and operations of the Kaldnes moving bed biofilm reactors journal May 2006
Leveraging knowledge engineering and machine learning for microbial bio-manufacturing journal July 2018
An integrative review of granular sludge for the biological removal of nutrients and recalcitrant organic matter from wastewater journal March 2018
Engineering Cellular Metabolism journal March 2016
Metabolic Resource Allocation in Individual Microbes Determines Ecosystem Interactions and Spatial Dynamics journal May 2014
Manipulation of the Quorum Sensing Signal AI-2 Affects the Antibiotic-Treated Gut Microbiota journal March 2015
Engineering Modular Viral Scaffolds for Targeted Bacterial Population Editing journal September 2015
Global Rebalancing of Cellular Resources by Pleiotropic Point Mutations Illustrates a Multi-scale Mechanism of Adaptive Evolution journal April 2016
Inferring Metabolic Mechanisms of Interaction within a Defined Gut Microbiota journal September 2018
Metabolism Links Bacterial Biofilms and Colon Carcinogenesis journal June 2015
Biological insights through omics data integration journal June 2019
Harnessing microbial activities for environmental cleanup journal June 2006
Microbial communities involved in enhanced biological phosphorus removal from wastewater—a model system in environmental biotechnology journal June 2012
Modular Assembly of Polysaccharide-Degrading Marine Microbial Communities journal May 2019
Domestication of Industrial Microbes journal May 2019
Microfluidic Organ-on-a-Chip Models of Human Intestine journal January 2018
Synthetic Ecology of Microbes: Mathematical Models and Applications journal February 2016
Towards Engineering Biological Systems in a Broader Context journal February 2016
The soil microbiome — from metagenomics to metaphenomics journal June 2018
A review of computational tools for design and reconstruction of metabolic pathways journal December 2017
Manipulating Bacterial Communities by in situ Microbiome Engineering journal April 2016
Engineering Microbiomes to Improve Plant and Animal Health journal October 2015
Spatial, Temporal, and Phylogenetic Scales of Microbial Ecology journal August 2019
A conceptual ecosystem model of microbial communities in enhanced biological phosphorus removal plants journal September 2010
Impact of cell cluster size on apparent half-saturation coefficients for oxygen in nitrifying sludge and biofilms journal December 2016
Biomass segregation between biofilm and flocs improves the control of nitrite-oxidizing bacteria in mainstream partial nitritation and anammox processes journal May 2019
Elementary metabolite units (EMU): A novel framework for modeling isotopic distributions journal January 2007
13C-metabolic flux analysis of co-cultures: A novel approach journal September 2015
“Replica-Extraction-Transfer” Nanostructure-Initiator Mass Spectrometry Imaging of Acoustically Printed Bacteria journal October 2013
Mass Spectrometry Imaging of Complex Microbial Communities journal December 2016
Intermittent Aeration Suppresses Nitrite-Oxidizing Bacteria in Membrane-Aerated Biofilms: A Model-Based Explanation journal May 2017
A Versatile Microfluidic Device for Automating Synthetic Biology journal June 2015
A Droplet Microfluidic Platform for Automating Genetic Engineering journal February 2016
The Experiment Data Depot: A Web-Based Software Tool for Biological Experimental Data Storage, Sharing, and Visualization journal September 2017
Segregation of Biomass in Cyclic Anaerobic/Aerobic Granular Sludge Allows the Enrichment of Anaerobic Ammonium Oxidizing Bacteria at Low Temperatures journal September 2011
Domestic Wastewater Treatment as a Net Energy Producer–Can This be Achieved? journal September 2011
Navigating Wastewater Energy Recovery Strategies: A Life Cycle Comparison of Anaerobic Membrane Bioreactor and Conventional Treatment Systems with Anaerobic Digestion journal May 2014
High-Efficiency Multiplex Genome Editing of Streptomyces Species Using an Engineered CRISPR/Cas System journal November 2014
Anaerobic microbial metabolism can proceed close to thermodynamic limits journal January 2002
Microbiology: Create a global microbiome effort journal October 2015
GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes journal May 2007
Genome-scale dynamic modeling of the competition between Rhodoferax and Geobacter in anoxic subsurface environments journal July 2010
Functionally relevant diversity of closely related Nitrospira in activated sludge journal August 2014
Selection on soil microbiomes reveals reproducible impacts on plant function journal October 2014
Dynamics in microbial communities: unraveling mechanisms to identify principles journal December 2014
Microbial dark matter ecogenomics reveals complex synergistic networks in a methanogenic bioreactor journal January 2015
Linking metabolite production to taxonomic identity in environmental samples by (MA)LDI-FISH journal July 2015
Segregating metabolic processes into different microbial cells accelerates the consumption of inhibitory substrates journal January 2016
Coupled RNA-SIP and metatranscriptomics of active chemolithoautotrophic communities at a deep-sea hydrothermal vent journal February 2016
Rapid evolution of microbe-mediated protection against pathogens in a worm host journal March 2016
Identification of syntrophic acetate-oxidizing bacteria in anaerobic digesters by combined protein-based stable isotope probing and metagenomics journal April 2016
DNA-SIP based genome-centric metagenomics identifies key long-chain fatty acid-degrading populations in anaerobic digesters with different feeding frequencies journal September 2017
Build your own soil: exploring microfluidics to create microbial habitat structures journal November 2017
A synthetic Escherichia coli predator–prey ecosystem journal January 2008
Metabolic networks in motion: 13 C‐based flux analysis journal January 2006
Clathrate nanostructures for mass spectrometry journal October 2007
The Human Microbiome Project journal October 2007
Genome evolution and adaptation in a long-term experiment with Escherichia coli journal October 2009
Insights into the phylogeny and coding potential of microbial dark matter journal July 2013
Single cell activity reveals direct electron transfer in methanotrophic consortia journal September 2015
Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria journal October 2015
Culturing of ‘unculturable’ human microbiota reveals novel taxa and extensive sporulation journal May 2016
What is flux balance analysis? journal March 2010
Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes journal May 2013
Distributing a metabolic pathway among a microbial consortium enhances production of natural products journal January 2015
Engineered bacteria can function in the mammalian gut long-term as live diagnostics of inflammation journal May 2017
Single-cell genome sequencing at ultra-high-throughput with microfluidic droplet barcoding journal May 2017
Cultivation and sequencing of rumen microbiome members from the Hungate1000 Collection journal March 2018
KBase: The United States Department of Energy Systems Biology Knowledgebase journal July 2018
Microbial metabolic exchange—the chemotype-to-phenotype link journal December 2011
A microfluidics-based in vitro model of the gastrointestinal human–microbe interface journal May 2016
Microbial interactions lead to rapid micro-scale successions on model marine particles journal June 2016
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system journal October 2016
Metabolic network analysis reveals microbial community interactions in anammox granules journal May 2017
Culture of previously uncultured members of the human gut microbiota by culturomics journal November 2016
A protocol for generating a high-quality genome-scale metabolic reconstruction journal January 2010
Scaling by shrinking: empowering single-cell 'omics' with microfluidic devices journal April 2017
Advancing microbial sciences by individual-based modelling journal June 2016
Spatial structure, cooperation and competition in biofilms journal July 2016
Quorum sensing signal–response systems in Gram-negative bacteria journal August 2016
The microbial nitrogen-cycling network journal February 2018
Marine microorganisms make a meal of oil journal March 2006
Microbial interactions: from networks to models journal July 2012
An interspecies malate–pyruvate shuttle reconciles redox imbalance in an anaerobic microbial community journal January 2019
Linking soil biology and chemistry in biological soil crust using isolate exometabolomics journal January 2018
A machine learning approach to predict metabolic pathway dynamics from time-series multiomics data journal May 2018
Function and functional redundancy in microbial systems journal April 2018
Engineered integrative and conjugative elements for efficient and inducible DNA transfer to undomesticated bacteria journal August 2018
Interspecies cross-feeding orchestrates carbon degradation in the rumen ecosystem journal October 2018
An automated Raman-based platform for the sorting of live cells by functional properties journal March 2019
CRISPR-based genomic tools for the manipulation of genetically intractable microorganisms journal March 2018
The social network of microorganisms — how auxotrophies shape complex communities journal March 2018
Keystone taxa as drivers of microbiome structure and functioning journal May 2018
Can we predict keystones? journal December 2018
Mutant phenotypes for thousands of bacterial genes of unknown function journal May 2018
A human gut bacterial genome and culture collection for improved metagenomic analyses journal February 2019
Next-generation biocontainment systems for engineered organisms journal May 2018
Metagenomic engineering of the mammalian gut microbiome in situ journal January 2019
EcoFABs: advancing microbiome science through standardized fabricated ecosystems journal June 2019
Multicellular microorganisms: laboratory versus nature journal May 2004
A new model for electron flow during anaerobic digestion: direct interspecies electron transfer to Methanosaeta for the reduction of carbon dioxide to methane journal January 2014
Droplet microfluidics for microbiology: techniques, applications and challenges journal January 2016
On-chip integration of droplet microfluidics and nanostructure-initiator mass spectrometry for enzyme screening journal January 2017
On the origin and robustness of power-law species-area relationships in ecology journal June 2006
Artificial selection of simulated microbial ecosystems journal May 2007
Large-scale reconstruction and phylogenetic analysis of metabolic environments journal September 2008
Defined spatial structure stabilizes a synthetic multispecies bacterial community journal November 2008
Rapid evolution of stability and productivity at the origin of a microbial mutualism journal January 2010
Bacterial community structures are unique and resilient in full-scale bioenergy systems journal February 2011
3D printing of microscopic bacterial communities journal October 2013
Programmable bacteria detect and record an environmental signal in the mammalian gut journal March 2014
Metaproteomics reveals differential modes of metabolic coupling among ubiquitous oxygen minimum zone microbes journal July 2014
Syntrophic exchange in synthetic microbial communities journal April 2014
Artificial ecosystem selection journal July 2000
Novel pathways for fuels and lubricants from biomass optimized using life-cycle greenhouse gas assessment journal June 2015
Biogeography of a human oral microbiome at the micron scale journal January 2016
Visualizing in situ translational activity for identifying and sorting slow-growing archaeal−bacterial consortia journal June 2016
Cas9-mediated genome editing in the methanogenic archaeon Methanosarcina acetivorans journal March 2017
Printed droplet microfluidics for on demand dispensing of picoliter droplets and cells journal July 2017
Massively parallel screening of synthetic microbial communities journal June 2019
Proteomics and pulse azidohomoalanine labeling of newly synthesized proteins: what are the potential applications? journal July 2018
MiDAS: the field guide to the microbes of activated sludge journal January 2015
The nature of laboratory domestication changes in freshly isolated Escherichia coli strains : Laboratory domestication of journal July 2013
In situ visualization of newly synthesized proteins in environmental microbes using amino acid tagging and click chemistry : Visualizing new proteins in microbes by click chemistry journal April 2014
Raman-FISH: combining stable-isotope Raman spectroscopy and fluorescence in situ hybridization for the single cell analysis of identity and function journal August 2007
NanoSIMS for biological applications: Current practices and analyses journal June 2018
3D printing of bacteria into functional complex materials journal December 2017
Diversity and Productivity in a Long-Term Grassland Experiment journal October 2001
The Microbial Engines That Drive Earth's Biogeochemical Cycles journal May 2008
The Competitive Exclusion Principle journal April 1960
A unified initiative to harness Earth's microbiomes journal October 2015
Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction journal February 2016
Gut bacteria selectively promoted by dietary fibers alleviate type 2 diabetes journal March 2018
Energetics of syntrophic cooperation in methanogenic degradation. journal January 1997
A Model for Designing Adaptive Laboratory Evolution Experiments journal February 2017
High-Throughput Single-Cell Cultivation on Microfluidic Streak Plates journal February 2016
Extracellular Polysaccharides of Rhodococcus rhodochrous S-2 Stimulate the Degradation of Aromatic Components in Crude Oil by Indigenous Marine Bacteria journal May 2002
Particle-Based Multidimensional Multispecies Biofilm Model journal May 2004
It Is All about Metabolic Fluxes journal December 2003
Need for Laboratory Ecosystems To Unravel the Structures and Functions of Soil Microbial Communities Mediated by Chemistry journal July 2018
Introducing THOR, a Model Microbiome for Genetic Dissection of Community Behavior journal March 2019
Machine Learning Reveals Missing Edges and Putative Interaction Mechanisms in Microbial Ecosystem Networks journal October 2018
Metatranscriptomic and Thermodynamic Insights into Medium-Chain Fatty Acid Production Using an Anaerobic Microbiome journal November 2018
Metabolic Imaging at the Single-Cell Scale: Recent Advances in Mass Spectrometry Imaging journal June 2019
Harnessing Nature's Anaerobes for Biotechnology and Bioprocessing journal June 2019
I N V IVO M EASUREMENT OF F LUXES THROUGH M ETABOLIC P ATHWAYS : The Missing Link in Functional Genomics and Pharmaceutical Research journal July 2003
Robo-Lector – a novel platform for automated high-throughput cultivations in microtiter plates with high information content journal January 2009
What do cells actually want? journal May 2016
A Peptide-Based Method for 13C Metabolic Flux Analysis in Microbial Communities journal September 2014
An Integrated Approach to Reconstructing Genome-Scale Transcriptional Regulatory Networks journal February 2015
Deciphering microbial interactions in synthetic human gut microbiome communities journal June 2018
Ensemble Modeling of Metabolic Networks journal December 2008
Robo-Lector - a novel platform for automated high-throughput cultivations in microtiter plates with high information content text January 2009
Activated Sludge Model No.2d, ASM2D journal January 1999
The SHARON®-Anammox® process for treatment of ammonium rich wastewater journal July 2001
Granular biomass capable of partial nitritation and anammox journal September 2008
Granular biomass capable of partial nitritation and anammox journal February 2009
Fluctuations of Animal Populations and a Measure of Community Stability journal July 1955
Biodiversity: Population Versus Ecosystem Stability journal July 1995
Fundamentals of Microbial Community Resistance and Resilience journal January 2012
Connecting the dots: linking nitrogen cycle gene expression to nitrogen fluxes in marine sediment mesocosms journal August 2014
Application of Machine Learning in Microbiology journal April 2019
The Design of FluxML: A Universal Modeling Language for 13C Metabolic Flux Analysis journal May 2019
Microbial interactions lead to rapid micro-scale successions on model marine particles text January 2016
3D printing of bacteria into functional complex materials text January 2017
Modular Assembly of Polysaccharide-Degrading Marine Microbial Communities text January 2019
Spatial structure, cooperation and competition in biofilms text January 2016

Cited By (16)

Gut Microbiome and Common Variable Immunodeficiency: Few Certainties and Many Outstanding Questions journal August 2021
Modulation of the Root Microbiome by Plant Molecules: The Basis for Targeted Disease Suppression and Plant Growth Promotion journal January 2020
Additional file 10 of Exploring the key microbial changes in the rhizosphere that affect the occurrence of tobacco root-knot nematodes dataset January 2020
Additional file 1 of Exploring the key microbial changes in the rhizosphere that affect the occurrence of tobacco root-knot nematodes dataset January 2020
Additional file 2 of Exploring the key microbial changes in the rhizosphere that affect the occurrence of tobacco root-knot nematodes dataset January 2020
Additional file 3 of Exploring the key microbial changes in the rhizosphere that affect the occurrence of tobacco root-knot nematodes dataset January 2020
Additional file 4 of Exploring the key microbial changes in the rhizosphere that affect the occurrence of tobacco root-knot nematodes image January 2020
Additional file 5 of Exploring the key microbial changes in the rhizosphere that affect the occurrence of tobacco root-knot nematodes dataset January 2020
Additional file 6 of Exploring the key microbial changes in the rhizosphere that affect the occurrence of tobacco root-knot nematodes dataset January 2020
Additional file 7 of Exploring the key microbial changes in the rhizosphere that affect the occurrence of tobacco root-knot nematodes dataset January 2020
Additional file 8 of Exploring the key microbial changes in the rhizosphere that affect the occurrence of tobacco root-knot nematodes dataset January 2020
Additional file 9 of Exploring the key microbial changes in the rhizosphere that affect the occurrence of tobacco root-knot nematodes dataset January 2020
Additional file 2 of Efficient management of the nitritation-anammox microbiome through intermittent aeration: absence of the NOB guild and expansion and diversity of the NOx reducing guild suggests a highly reticulated nitrogen cycle dataset January 2022
Additional file 3 of Efficient management of the nitritation-anammox microbiome through intermittent aeration: absence of the NOB guild and expansion and diversity of the NOx reducing guild suggests a highly reticulated nitrogen cycle dataset January 2022
Polarization of microbial communities between competitive and cooperative metabolism journal January 2021
Exploring the key microbial changes in the rhizosphere that affect the occurrence of tobacco root-knot nematodes journal April 2020

Similar Records

Integrating Systems and Synthetic Biology to Understand and Engineer Microbiomes
Journal Article · Sun Mar 28 20:00:00 EDT 2021 · Annual Review of Biomedical Engineering · OSTI ID:1774955

Soil microbiome engineering for sustainability in a changing environment
Journal Article · Sun Oct 29 20:00:00 EDT 2023 · Nature Biotechnology · OSTI ID:2323330

Related Subjects