skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Microbiome Engineering: Synthetic Biology of Plant-Associated Microbiomes in Sustainable Agriculture

Abstract

To support an ever-increasing population, modern agriculture faces numerous challenges that pose major threats to global food and energy security. Plant-associated microbes, with their many plant growth-promoting (PGP) traits, have enormous potential in helping to solve these challenges. However, the results of their use in agriculture have been variable, probably because of poor colonization. Phytomicrobiome engineering is an emerging field of synthetic biology that may offer ways to alleviate this limitation. This review highlights recent advances in both bottom-up and top-down approaches to engineering non-model bacteria and microbiomes to promote beneficial plant-microbe interactions, as well as advances in strategies to evaluate these interactions. Biosafety, biosecurity, and biocontainment strategies to address the environmental concerns associated with field use of synthetic microbes are also discussed.

Authors:
; ;
Publication Date:
Research Org.:
Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1647398
Alternate Identifier(s):
OSTI ID: 1807576; OSTI ID: 1813363
Grant/Contract Number:  
SC0018420; AC02-05CH11231; SC0018260; SC0020390
Resource Type:
Published Article
Journal Name:
Trends in Biotechnology
Additional Journal Information:
Journal Name: Trends in Biotechnology Journal Volume: 39 Journal Issue: 3; Journal ID: ISSN 0167-7799
Publisher:
Elsevier
Country of Publication:
Netherlands
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; phytomicrobiome engineering; genome engineering; sustainable agriculture; synthetic microbial community; plant growth promotion; safe genes strategies

Citation Formats

Ke, Jing, Wang, Bing, and Yoshikuni, Yasuo. Microbiome Engineering: Synthetic Biology of Plant-Associated Microbiomes in Sustainable Agriculture. Netherlands: N. p., 2021. Web. https://doi.org/10.1016/j.tibtech.2020.07.008.
Ke, Jing, Wang, Bing, & Yoshikuni, Yasuo. Microbiome Engineering: Synthetic Biology of Plant-Associated Microbiomes in Sustainable Agriculture. Netherlands. https://doi.org/10.1016/j.tibtech.2020.07.008
Ke, Jing, Wang, Bing, and Yoshikuni, Yasuo. Mon . "Microbiome Engineering: Synthetic Biology of Plant-Associated Microbiomes in Sustainable Agriculture". Netherlands. https://doi.org/10.1016/j.tibtech.2020.07.008.
@article{osti_1647398,
title = {Microbiome Engineering: Synthetic Biology of Plant-Associated Microbiomes in Sustainable Agriculture},
author = {Ke, Jing and Wang, Bing and Yoshikuni, Yasuo},
abstractNote = {To support an ever-increasing population, modern agriculture faces numerous challenges that pose major threats to global food and energy security. Plant-associated microbes, with their many plant growth-promoting (PGP) traits, have enormous potential in helping to solve these challenges. However, the results of their use in agriculture have been variable, probably because of poor colonization. Phytomicrobiome engineering is an emerging field of synthetic biology that may offer ways to alleviate this limitation. This review highlights recent advances in both bottom-up and top-down approaches to engineering non-model bacteria and microbiomes to promote beneficial plant-microbe interactions, as well as advances in strategies to evaluate these interactions. Biosafety, biosecurity, and biocontainment strategies to address the environmental concerns associated with field use of synthetic microbes are also discussed.},
doi = {10.1016/j.tibtech.2020.07.008},
journal = {Trends in Biotechnology},
number = 3,
volume = 39,
place = {Netherlands},
year = {2021},
month = {3}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1016/j.tibtech.2020.07.008

Save / Share:

Works referenced in this record:

Minimum Information about a Biosynthetic Gene cluster
journal, August 2015

  • Medema, Marnix H.; Kottmann, Renzo; Yilmaz, Pelin
  • Nature Chemical Biology, Vol. 11, Issue 9
  • DOI: 10.1038/nchembio.1890

Next-generation biocontainment systems for engineered organisms
journal, May 2018

  • Lee, Jeong Wook; Chan, Clement T. Y.; Slomovic, Shimyn
  • Nature Chemical Biology, Vol. 14, Issue 6
  • DOI: 10.1038/s41589-018-0056-x

The RootChip: An Integrated Microfluidic Chip for Plant Science
journal, December 2011

  • Grossmann, Guido; Guo, Woei-Jiun; Ehrhardt, David W.
  • The Plant Cell, Vol. 23, Issue 12
  • DOI: 10.1105/tpc.111.092577

Field Release of a Genetically Modified Pseudomonas fluorescens on Wheat: Establishment, Survival and Dissemination
journal, December 1995

  • De Leij, Frans A. A. M.; Sutton, Emma J.; Whipps, John M.
  • Nature Biotechnology, Vol. 13, Issue 12
  • DOI: 10.1038/nbt1295-1488

Fundamentals of Microbial Community Resistance and Resilience
journal, January 2012


Programming a Human Commensal Bacterium, Bacteroides thetaiotaomicron, to Sense and Respond to Stimuli in the Murine Gut Microbiota
journal, July 2015


Synthetic quorum-sensing circuit to control consortial biofilm formation and dispersal in a microfluidic device
journal, January 2012

  • Hong, Seok Hoon; Hegde, Manjunath; Kim, Jeongyun
  • Nature Communications, Vol. 3, Issue 1
  • DOI: 10.1038/ncomms1616

Generation of a cluster-free Streptomyces albus chassis strains for improved heterologous expression of secondary metabolite clusters
journal, September 2018


Integrative and conjugative elements and their hosts: composition, distribution and organization
journal, July 2017

  • Cury, Jean; Touchon, Marie; Rocha, Eduardo P. C.
  • Nucleic Acids Research, Vol. 45, Issue 15
  • DOI: 10.1093/nar/gkx607

Survival, Colonization and Dispersal of Genetically Modified Pseudomonas fluorescens SBW25 in the Phytosphere of Field Grown Sugar Beet
journal, December 1995

  • Thompson, Ian P.; Lilley, Andrew K.; Ellis, Richard J.
  • Nature Biotechnology, Vol. 13, Issue 12
  • DOI: 10.1038/nbt1295-1493

Refactoring the nitrogen fixation gene cluster from Klebsiella oxytoca
journal, April 2012

  • Temme, K.; Zhao, D.; Voigt, C. A.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 18
  • DOI: 10.1073/pnas.1120788109

Metagenomic engineering of the mammalian gut microbiome in situ
journal, January 2019


The Application of Ecological Theory Toward an Understanding of the Human Microbiome
journal, June 2012


Rational Design of Evolutionarily Stable Microbial Kill Switches
journal, November 2017


Synthetic biology approaches to biological containment: pre-emptively tackling potential risks
journal, November 2016

  • Torres, Leticia; Krüger, Antje; Csibra, Eszter
  • Essays in Biochemistry, Vol. 60, Issue 4
  • DOI: 10.1042/EBC20160013

Exploration of Plant-Microbe Interactions for Sustainable Agriculture in CRISPR Era
journal, August 2019


Actinobacteria phylogenomics, selective isolation from an iron oligotrophic environment and siderophore functional characterization, unveil new desferrioxamine traits
journal, July 2017

  • Cruz-Morales, Pablo; Ramos-Aboites, Hilda E.; Licona-Cassani, Cuauhtémoc
  • FEMS Microbiology Ecology, Vol. 93, Issue 9
  • DOI: 10.1093/femsec/fix086

Establishing Causality: Opportunities of Synthetic Communities for Plant Microbiome Research
journal, August 2017

  • Vorholt, Julia A.; Vogel, Christine; Carlström, Charlotte I.
  • Cell Host & Microbe, Vol. 22, Issue 2
  • DOI: 10.1016/j.chom.2017.07.004

Viral tagging reveals discrete populations in Synechococcus viral genome sequence space
journal, July 2014

  • Deng, Li; Ignacio-Espinoza, J. Cesar; Gregory, Ann C.
  • Nature, Vol. 513, Issue 7517
  • DOI: 10.1038/nature13459

Development of a high efficiency integration system and promoter library for rapid modification of Pseudomonas putida KT2440
journal, December 2017


Phage combination therapies for bacterial wilt disease in tomato
journal, December 2019


NIH guidelines for research involving recombinant DNA molecules
journal, December 1993


Biosafety and biosecurity in Synthetic Biology: A review
journal, February 2019

  • Gómez-Tatay, Lucía; Hernández-Andreu, José M.
  • Critical Reviews in Environmental Science and Technology, Vol. 49, Issue 17
  • DOI: 10.1080/10643389.2019.1579628

Associations with rhizosphere bacteria can confer an adaptive advantage to plants
journal, May 2015


C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector
journal, June 2016

  • Abudayyeh, Omar O.; Gootenberg, Jonathan S.; Konermann, Silvana
  • Science, Vol. 353, Issue 6299
  • DOI: 10.1126/science.aaf5573

Spatiotemporal control of gene expression with pulse-generating networks
journal, April 2004

  • Basu, S.; Mehreja, R.; Thiberge, S.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 17
  • DOI: 10.1073/pnas.0307571101

COREMIC: a web-tool to search for a niche associated CORE MICrobiome
journal, January 2018

  • Rodrigues, Richard R.; Rodgers, Nyle C.; Wu, Xiaowei
  • PeerJ, Vol. 6
  • DOI: 10.7717/peerj.4395

Multi-chassis engineering for heterologous production of microbial natural products
journal, April 2020


CRAGE enables rapid activation of biosynthetic gene clusters in undomesticated bacteria
journal, October 2019


Microfluidic static droplet array for analyzing microbial communication on a population gradient
journal, January 2015

  • Jeong, Heon-Ho; Jin, Si Hyung; Lee, Byung Jin
  • Lab on a Chip, Vol. 15, Issue 3
  • DOI: 10.1039/C4LC01097C

Elucidating Bacterial Gene Functions in the Plant Microbiome
journal, October 2018


Genome mining identifies cepacin as a plant-protective metabolite of the biopesticidal bacterium Burkholderia ambifaria
journal, March 2019

  • Mullins, Alex J.; Murray, James A. H.; Bull, Matthew J.
  • Nature Microbiology, Vol. 4, Issue 6
  • DOI: 10.1038/s41564-019-0383-z

A Tn7-based broad-range bacterial cloning and expression system
journal, May 2005

  • Choi, Kyoung-Hee; Gaynor, Jared B.; White, Kimberly G.
  • Nature Methods, Vol. 2, Issue 6
  • DOI: 10.1038/nmeth765

A review on the plant microbiome: Ecology, functions, and emerging trends in microbial application
journal, September 2019


Considerations for using bacteriophages for plant disease control
journal, October 2012

  • Jones, Jeffrey B.; Vallad, Gary E.; Iriarte, Fanny B.
  • Bacteriophage, Vol. 2, Issue 4
  • DOI: 10.4161/bact.23857

Engineering Microbiomes to Improve Plant and Animal Health
journal, October 2015


Mini-Tn7 vectors as genetic tools for single copy gene cloning in Acinetobacter baumannii
journal, September 2010

  • Kumar, Ayush; Dalton, Courtney; Cortez-Cordova, Jenny
  • Journal of Microbiological Methods, Vol. 82, Issue 3
  • DOI: 10.1016/j.mimet.2010.07.002

Facilitation of phosphorus uptake in maize plants by mycorrhizosphere bacteria
journal, July 2017


Engineered integrative and conjugative elements for efficient and inducible DNA transfer to undomesticated bacteria
journal, August 2018

  • Brophy, Jennifer A. N.; Triassi, Alexander J.; Adams, Bryn L.
  • Nature Microbiology, Vol. 3, Issue 9
  • DOI: 10.1038/s41564-018-0216-5

Synthetic biology: Recent progress, biosafety and biosecurity concerns, and possible solutions
journal, March 2019


Anti-CRISPR: discovery, mechanism and function
journal, October 2017

  • Pawluk, April; Davidson, Alan R.; Maxwell, Karen L.
  • Nature Reviews Microbiology, Vol. 16, Issue 1
  • DOI: 10.1038/nrmicro.2017.120

An Engineered Device for Indoleacetic Acid Production under Quorum Sensing Signals Enables Cupriavidus pinatubonensis JMP134 To Stimulate Plant Growth
journal, May 2018

  • Zúñiga, Ana; Fuente, Francisco de la; Federici, Fernán
  • ACS Synthetic Biology, Vol. 7, Issue 6
  • DOI: 10.1021/acssynbio.8b00002

Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome
journal, June 2013

  • Modi, Sheetal R.; Lee, Henry H.; Spina, Catherine S.
  • Nature, Vol. 499, Issue 7457
  • DOI: 10.1038/nature12212

Let the Core Microbiota Be Functional
journal, July 2017


Analysis and cloning of the synthetic pathway of the phytohormone indole-3-acetic acid in the plant-beneficial Bacillus amyloliquefaciens SQR9
journal, September 2015


Phenotypic Landscape of a Bacterial Cell
journal, January 2011


Plant chip for high-throughput phenotyping of Arabidopsis
journal, January 2014

  • Jiang, Huawei; Xu, Zhen; Aluru, Maneesha R.
  • Lab Chip, Vol. 14, Issue 7
  • DOI: 10.1039/C3LC51326B

Autonomous plasmid-like replication of a conjugative transposon
journal, January 2010


Roots Shaping Their Microbiome: Global Hotspots for Microbial Activity
journal, August 2015


Bipartite interactions, antibiotic production and biosynthetic potential of the Arabidopsis leaf microbiome
journal, July 2018

  • Helfrich, Eric J. N.; Vogel, Christine M.; Ueoka, Reiko
  • Nature Microbiology, Vol. 3, Issue 8
  • DOI: 10.1038/s41564-018-0200-0

Genetic Engineering of Bacteriophages Against Infectious Diseases
journal, May 2019


Auxotrophy to Xeno-DNA: an exploration of combinatorial mechanisms for a high-fidelity biosafety system for synthetic biology applications
journal, August 2018

  • Whitford, Christopher M.; Dymek, Saskia; Kerkhoff, Denise
  • Journal of Biological Engineering, Vol. 12, Issue 1
  • DOI: 10.1186/s13036-018-0105-8

High-Yield Production of Herbicidal Thaxtomins and Thaxtomin Analogs in a Nonpathogenic Streptomyces Strain
journal, March 2018

  • Jiang, Guangde; Zhang, Yucheng; Powell, Magan M.
  • Applied and Environmental Microbiology, Vol. 84, Issue 11
  • DOI: 10.1128/AEM.00164-18

Plant host habitat and root exudates shape soil bacterial community structure
journal, August 2008

  • Haichar, Feth el Zahar; Marol, Christine; Berge, Odile
  • The ISME Journal, Vol. 2, Issue 12
  • DOI: 10.1038/ismej.2008.80

Exploiting CRISPR-Cas nucleases to produce sequence-specific antimicrobials
journal, October 2014

  • Bikard, David; Euler, Chad W.; Jiang, Wenyan
  • Nature Biotechnology, Vol. 32, Issue 11
  • DOI: 10.1038/nbt.3043

Emerging Frontiers in Microbiome Engineering
journal, October 2019

  • Inda, María Eugenia; Broset, Esther; Lu, Timothy K.
  • Trends in Immunology, Vol. 40, Issue 10
  • DOI: 10.1016/j.it.2019.08.007

Core microbiomes for sustainable agroecosystems
journal, April 2018


Phytohormones and Beneficial Microbes: Essential Components for Plants to Balance Stress and Fitness
journal, October 2017

  • Egamberdieva, Dilfuza; Wirth, Stephan J.; Alqarawi, Abdulaziz A.
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.02104

Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow
journal, July 2010

  • Wozniak, Rachel A. F.; Waldor, Matthew K.
  • Nature Reviews Microbiology, Vol. 8, Issue 8
  • DOI: 10.1038/nrmicro2382

The Pseudomonas putida T6SS is a plant warden against phytopathogens
journal, January 2017

  • Bernal, Patricia; Allsopp, Luke P.; Filloux, Alain
  • The ISME Journal, Vol. 11, Issue 4
  • DOI: 10.1038/ismej.2016.169

Insecticidal toxins from Photorhabdus bacteria and their potential use in agriculture
journal, March 2007


Phosphate Nutrition: Improving Low-Phosphate Tolerance in Crops
journal, April 2014

  • López-Arredondo, Damar Lizbeth; Leyva-González, Marco Antonio; González-Morales, Sandra Isabel
  • Annual Review of Plant Biology, Vol. 65, Issue 1
  • DOI: 10.1146/annurev-arplant-050213-035949

Engineering banana endosphere microbiome to improve Fusarium wilt resistance in banana
journal, May 2019


Bacillus thuringiensis: a successful insecticide with new environmental features and tidings
journal, February 2017

  • Jouzani, Gholamreza Salehi; Valijanian, Elena; Sharafi, Reza
  • Applied Microbiology and Biotechnology, Vol. 101, Issue 7
  • DOI: 10.1007/s00253-017-8175-y

Genome-wide mapping of mutations at single-nucleotide resolution for protein, metabolic and genome engineering
journal, December 2016

  • Garst, Andrew D.; Bassalo, Marcelo C.; Pines, Gur
  • Nature Biotechnology, Vol. 35, Issue 1, p. 48-55
  • DOI: 10.1038/nbt.3718

Massively parallel screening of synthetic microbial communities
journal, June 2019

  • Kehe, Jared; Kulesa, Anthony; Ortiz, Anthony
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 26
  • DOI: 10.1073/pnas.1900102116

Polyprotein strategy for stoichiometric assembly of nitrogen fixation components for synthetic biology
journal, July 2018

  • Yang, Jianguo; Xie, Xiaqing; Xiang, Nan
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 36
  • DOI: 10.1073/pnas.1804992115

Multilayered genetic safeguards limit growth of microorganisms to defined environments
journal, January 2015

  • Gallagher, Ryan R.; Patel, Jaymin R.; Interiano, Alexander L.
  • Nucleic Acids Research, Vol. 43, Issue 3
  • DOI: 10.1093/nar/gku1378

Plant Growth-Promoting Bacteria: Mechanisms and Applications
journal, January 2012


Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota
journal, July 2018


Systems Biology of Plant-Microbiome Interactions
journal, June 2019

  • Rodriguez, Patricia A.; Rothballer, Michael; Chowdhury, Soumitra Paul
  • Molecular Plant, Vol. 12, Issue 6
  • DOI: 10.1016/j.molp.2019.05.006

Plant pathogens and integrated defence responses to infection
journal, June 2001

  • Dangl, Jeffery L.; Jones, Jonathan D. G.
  • Nature, Vol. 411, Issue 6839
  • DOI: 10.1038/35081161

Computational meta'omics for microbial community studies
journal, January 2013

  • Segata, Nicola; Boernigen, Daniela; Tickle, Timothy L.
  • Molecular Systems Biology, Vol. 9, Issue 1
  • DOI: 10.1038/msb.2013.22

Use of plant colonizing bacteria as chassis for transfer of N2-fixation to cereals
journal, April 2015


Plant-in-chip: Microfluidic system for studying root growth and pathogenic interactions in Arabidopsis
journal, June 2011

  • Parashar, Archana; Pandey, Santosh
  • Applied Physics Letters, Vol. 98, Issue 26
  • DOI: 10.1063/1.3604788

Mutant phenotypes for thousands of bacterial genes of unknown function
journal, May 2018


Control of nitrogen fixation in bacteria that associate with cereals
journal, December 2019


Integrative and Conjugative Elements (ICEs): What They Do and How They Work
journal, November 2015


A microfluidic approach to study the effect of bacterial interactions on antimicrobial susceptibility in polymicrobial cultures
journal, January 2015

  • Mohan, Ritika; Sanpitakseree, Chotitath; Desai, Amit V.
  • RSC Advances, Vol. 5, Issue 44
  • DOI: 10.1039/C5RA04092B

Peptidoglycan from Bacillus cereus Mediates Commensalism with Rhizosphere Bacteria from the Cytophaga-Flavobacterium Group
journal, August 2006

  • Peterson, S. B.; Dunn, A. K.; Klimowicz, A. K.
  • Applied and Environmental Microbiology, Vol. 72, Issue 8
  • DOI: 10.1128/AEM.02928-05

Engineered bacteriophage targeting gene networks as adjuvants for antibiotic therapy
journal, March 2009

  • Lu, T. K.; Collins, J. J.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 12
  • DOI: 10.1073/pnas.0800442106

Multi-functional genome-wide CRISPR system for high throughput genotype–phenotype mapping
journal, December 2019


The Hidden World within Plants: Ecological and Evolutionary Considerations for Defining Functioning of Microbial Endophytes
journal, July 2015

  • Hardoim, Pablo R.; van Overbeek, Leonard S.; Berg, Gabriele
  • Microbiology and Molecular Biology Reviews, Vol. 79, Issue 3
  • DOI: 10.1128/MMBR.00050-14

Improving phosphorus use efficiency: a complex trait with emerging opportunities
journal, February 2017

  • Heuer, Sigrid; Gaxiola, Roberto; Schilling, Rhiannon
  • The Plant Journal, Vol. 90, Issue 5
  • DOI: 10.1111/tpj.13423

Simplified and representative bacterial community of maize roots
journal, March 2017

  • Niu, Ben; Paulson, Joseph Nathaniel; Zheng, Xiaoqi
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 12
  • DOI: 10.1073/pnas.1616148114

Optimized inducible shRNA and CRISPR/Cas9 platforms for in vitro studies of human development using hPSCs
journal, November 2016

  • Bertero, Alessandro; Pawlowski, Matthias; Ortmann, Daniel
  • Development, Vol. 143, Issue 23
  • DOI: 10.1242/dev.138081

Bacteria isolated from roots and rhizosphere of Vitis vinifera retard water losses, induce abscisic acid accumulation and synthesis of defense-related terpenes in in vitro cultured grapevine
journal, November 2013

  • Salomon, María Victoria; Bottini, Rubén; de Souza Filho, Gonçalo Apolinário
  • Physiologia Plantarum, Vol. 151, Issue 4
  • DOI: 10.1111/ppl.12117

Recoding the metagenome: microbiome engineering in situ
journal, August 2019


Biological nitrogen fixation in maize: optimizing nitrogenase expression in a root-associated diazotroph
journal, April 2020

  • Bloch, Sarah E.; Clark, Rosemary; Gottlieb, Shayin S.
  • Journal of Experimental Botany, Vol. 71, Issue 15
  • DOI: 10.1093/jxb/eraa176

Multiplexed site-specific genome engineering for overproducing bioactive secondary metabolites in actinomycetes
journal, March 2017


New Applications for Phage Integrases
journal, July 2014

  • Fogg, Paul C. M.; Colloms, Sean; Rosser, Susan
  • Journal of Molecular Biology, Vol. 426, Issue 15
  • DOI: 10.1016/j.jmb.2014.05.014

Direct Pathway Cloning (DiPaC) to unlock natural product biosynthetic potential
journal, May 2018


Quantification of cellular penetrative forces using lab-on-a-chip technology and finite element modeling
journal, April 2013

  • Sanati Nezhad, A.; Naghavi, M.; Packirisamy, M.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 20
  • DOI: 10.1073/pnas.1221677110

Rational development of transformation in Clostridium thermocellum ATCC 27405 via complete methylome analysis and evasion of native restriction–modification systems
journal, July 2019

  • Riley, Lauren A.; Ji, Lexiang; Schmitz, Robert J.
  • Journal of Industrial Microbiology & Biotechnology, Vol. 46, Issue 9-10
  • DOI: 10.1007/s10295-019-02218-x

Broad host range plasmids can invade an unexpectedly diverse fraction of a soil bacterial community
journal, October 2014


Building-in biosafety for synthetic biology
journal, July 2013


Functional optimization of gene clusters by combinatorial design and assembly
journal, November 2014

  • Smanski, Michael J.; Bhatia, Swapnil; Zhao, Dehua
  • Nature Biotechnology, Vol. 32, Issue 12, p. 1241-1249
  • DOI: 10.1038/nbt.3063

EcoFABs: advancing microbiome science through standardized fabricated ecosystems
journal, June 2019


Sequencing and beyond: integrating molecular 'omics' for microbial community profiling
journal, April 2015

  • Franzosa, Eric A.; Hsu, Tiffany; Sirota-Madi, Alexandra
  • Nature Reviews Microbiology, Vol. 13, Issue 6
  • DOI: 10.1038/nrmicro3451

Impact of Field Release of Genetically Modified Pseudomonas fluorescens on Indigenous Microbial Populations of Wheat.
journal, January 1995


Rapid Quantification of Mutant Fitness in Diverse Bacteria by Sequencing Randomly Bar-Coded Transposons
journal, May 2015

  • Wetmore, Kelly M.; Price, Morgan N.; Waters, Robert J.
  • mBio, Vol. 6, Issue 3, Article No. e00306-15
  • DOI: 10.1128/mBio.00306-15

Phage-Based Applications in Synthetic Biology
journal, September 2018


Long-term manure exposure increases soil bacterial community potential for plasmid uptake: Manure increases community plasmid uptake
journal, January 2014

  • Musovic, Sanin; Klümper, Uli; Dechesne, Arnaud
  • Environmental Microbiology Reports, Vol. 6, Issue 2
  • DOI: 10.1111/1758-2229.12138

Knockdown of Mythimna separata chitinase genes via bacterial expression and oral delivery of RNAi effectors
journal, February 2017


Programming gene and engineered-cell therapies with synthetic biology
journal, February 2018


Engineered Root Bacteria Release Plant-Available Phosphate from Phytate
journal, July 2019

  • Shulse, Christine N.; Chovatia, Mansi; Agosto, Carolyn
  • Applied and Environmental Microbiology, Vol. 85, Issue 18
  • DOI: 10.1128/AEM.01210-19

'Deadman' and 'Passcode' microbial kill switches for bacterial containment
journal, December 2015

  • Chan, Clement T. Y.; Lee, Jeong Wook; Cameron, D. Ewen
  • Nature Chemical Biology, Vol. 12, Issue 2
  • DOI: 10.1038/nchembio.1979

Broad host range plasmids
journal, September 2013


The chromosomal accommodation and domestication of mobile genetic elements
journal, December 2014

  • Touchon, Marie; Bobay, Louis-Marie; Rocha, Eduardo PC
  • Current Opinion in Microbiology, Vol. 22
  • DOI: 10.1016/j.mib.2014.09.010

Root nodule symbiosis in Lotus japonicus drives the establishment of distinctive rhizosphere, root, and nodule bacterial communities
journal, November 2016

  • Zgadzaj, Rafal; Garrido-Oter, Ruben; Jensen, Dorthe Bodker
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 49
  • DOI: 10.1073/pnas.1616564113

Recombinant plasmids carrying nitrogen fixation genes from Rhizobium japonicum
journal, May 1981


Programmed population control by cell–cell communication and regulated killing
journal, April 2004

  • You, Lingchong; Cox, Robert Sidney; Weiss, Ron
  • Nature, Vol. 428, Issue 6985, p. 868-871
  • DOI: 10.1038/nature02491

Transposon-aided capture (TRACA) of plasmids resident in the human gut mobile metagenome
journal, November 2006

  • Jones, Brian V.; Marchesi, Julian R.
  • Nature Methods, Vol. 4, Issue 1
  • DOI: 10.1038/nmeth964

The impact of failure: unsuccessful bacterial invasions steer the soil microbial community away from the invader’s niche
journal, January 2018


The structural biology of type IV secretion systems
journal, October 2009

  • Fronzes, Rémi; Christie, Peter J.; Waksman, Gabriel
  • Nature Reviews Microbiology, Vol. 7, Issue 10
  • DOI: 10.1038/nrmicro2218

Exploration of the Biosynthetic Potential of the Populus Microbiome
journal, October 2018


DNA watermarks in non-coding regulatory sequences
journal, January 2009

  • Heider, Dominik; Pyka, Martin; Barnekow, Angelika
  • BMC Research Notes, Vol. 2, Issue 1
  • DOI: 10.1186/1756-0500-2-125

How the insect pathogen bacteria Bacillus thuringiensis and Xenorhabdus/Photorhabdus occupy their hosts
journal, June 2012

  • Nielsen-LeRoux, Christina; Gaudriault, Sophie; Ramarao, Nalini
  • Current Opinion in Microbiology, Vol. 15, Issue 3
  • DOI: 10.1016/j.mib.2012.04.006

A microfluidic device and computational platform for high-throughput live imaging of gene expression
journal, September 2012

  • Busch, Wolfgang; Moore, Brad T.; Martsberger, Bradley
  • Nature Methods, Vol. 9, Issue 11
  • DOI: 10.1038/nmeth.2185

Bacteriocin production augments niche competition by enterococci in the mammalian gastrointestinal tract
journal, October 2015

  • Kommineni, Sushma; Bretl, Daniel J.; Lam, Vy
  • Nature, Vol. 526, Issue 7575
  • DOI: 10.1038/nature15524

Live imaging of root–bacteria interactions in a microfluidics setup
journal, March 2017

  • Massalha, Hassan; Korenblum, Elisa; Malitsky, Sergey
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 17
  • DOI: 10.1073/pnas.1618584114

Novel rhizobox design to assess rhizosphere characteristics at high spatial resolution
journal, November 2001

  • Wenzel, Walter W.; Wieshammer, Gottfried; Fitz, Walter J.
  • Plant and Soil, Vol. 237, Issue 1, p. 37-45
  • DOI: 10.1023/A:1013395122730

Metagenomic mining of regulatory elements enables programmable species-selective gene expression
journal, March 2018

  • Johns, Nathan I.; Gomes, Antonio L. C.; Yim, Sung Sun
  • Nature Methods, Vol. 15, Issue 5
  • DOI: 10.1038/nmeth.4633

Antibiotic resistance in Pseudomonas aeruginosa – Mechanisms, epidemiology and evolution
journal, May 2019


Single-copy chromosomal integration systems for Francisella tularensis
journal, April 2009

  • LoVullo, Eric D.; Molins-Schneekloth, Claudia R.; Schweizer, Herbert P.
  • Microbiology, Vol. 155, Issue 4
  • DOI: 10.1099/mic.0.022491-0

Discovery of Reactive Microbiota-Derived Metabolites that Inhibit Host Proteases
journal, January 2017


Characterization of a Bacteroides Mobilizable Transposon, NBU2, Which Carries a Functional Lincomycin Resistance Gene
journal, June 2000


Plant-microbe partnerships in 2020
journal, July 2016

  • Mitter, Birgit; Pfaffenbichler, Nikolaus; Sessitsch, Angela
  • Microbial Biotechnology, Vol. 9, Issue 5
  • DOI: 10.1111/1751-7915.12382

Uncoupling virulence and biocontrol
journal, May 2019


Genome-wide identification of bacterial plant colonization genes
journal, September 2017


3D printing of microscopic bacterial communities
journal, October 2013

  • Connell, J. L.; Ritschdorff, E. T.; Whiteley, M.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 46
  • DOI: 10.1073/pnas.1309729110

Tn-seq: high-throughput parallel sequencing for fitness and genetic interaction studies in microorganisms
journal, September 2009

  • van Opijnen, Tim; Bodi, Kip L.; Camilli, Andrew
  • Nature Methods, Vol. 6, Issue 10
  • DOI: 10.1038/nmeth.1377

Anti-CRISPR-Associated Proteins Are Crucial Repressors of Anti-CRISPR Transcription
journal, September 2019


Evaluation of a novel tool for sampling root exudates from soil-grown plants compared to conventional techniques
journal, March 2013


Discovery and Characterization of Cas9 Inhibitors Disseminated across Seven Bacterial Phyla
journal, February 2019


Streamlined Genetic Manipulation of Diverse Bacteroides and Parabacteroides Isolates from the Human Gut Microbiota
journal, August 2019


Microfluidic platforms for plant cells studies
journal, January 2014


Manipulating Bacterial Communities by in situ Microbiome Engineering
journal, April 2016