Abstract
Recent advances in microbial ecology and synthetic biology have the potential to mitigate damage caused by anthropogenic activities that are deleteriously impacting Earth’s soil ecosystems. Here, we discuss challenges and opportunities for harnessing natural and synthetic soil microbial communities, focusing on plant growth promotion under different scenarios. We explore current needs for microbial solutions in soil ecosystems, how these solutions are being developed and applied, and the potential for new biotechnology breakthroughs to tailor and target microbial products for specific applications. We highlight several scientific and technological advances in soil microbiome engineering, including characterization of microbes that impact soil ecosystems, directing how microbes assemble to interact in soil environments, and the developing suite of gene-engineering approaches. This Review underscores the need for an interdisciplinary approach to understand the composition, dynamics and deployment of beneficial soil microbiomes to drive efforts to mitigate or reverse environmental damage by restoring and protecting healthy soil ecosystems.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Vejan, P., Abdullah, R., Khadiran, T., Ismail, S. & Nasrulhaq Boyce, A. Role of plant growth promoting rhizobacteria in agricultural sustainability—a review. Molecules 21, 573 (2016).
Naylor, D. et al. Soil microbiomes under climate change and implications for carbon cycling. Annu. Rev. Environ. Resour. 45, 29–59 (2020).
Gong, T. et al. An engineered Pseudomonas putida can simultaneously degrade organophosphates, pyrethroids and carbamates. Sci. Total Environ. 628, 1258–1265 (2018).
Rajkumar, M., Ae, N., Prasad, M. N. V. & Freitas, H. Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol. 28, 142–149 (2010).
Bhattacharyya, S. S., Ros, G. H., Furtak, K., Iqbal, H. M. & Parra-Saldívar, R. Soil carbon sequestration—an interplay between soil microbial community and soil organic matter dynamics. Sci. Total Environ. 815, 152928 (2022).
Intergovernmental Panel on Climate Change (ed.). Climate Change 2014: Synthesis Report (Intergovernmental Panel on Climate Change Fifth Assessment Report, 2014).
Jansson, J. K. & Taş, N. The microbial ecology of permafrost. Nat. Rev. Microbiol. 12, 414–425 (2014).
Natali, S. M. et al. Permafrost carbon feedbacks threaten global climate goals. Proc. Natl Acad. Sci. USA 118, e2100163118 (2021).
Abdalla, M. et al. A critical review of the impacts of cover crops on nitrogen leaching, net greenhouse gas balance and crop productivity. Glob. Chang. Biol. 25, 2530–2543 (2019).
Furey, G. N. & Tilman, D. Plant biodiversity and the regeneration of soil fertility. Proc. Natl Acad. Sci. USA 118, e2111321118 (2021).
Cleary, D. W. et al. Long-term antibiotic exposure in soil is associated with changes in microbial community structure and prevalence of class 1 integrons. FEMS Microbiol. Ecol. 92, fiw159 (2016).
Torsvik, V. & Øvreås, L. Microbial diversity and function in soil: from genes to ecosystems. Curr. Opin. Microbiol. 5, 240–245 (2002).
Thompson, L. et al. A communal catalogue reveals Earth’s multiscale 736 microbial diversity. Nature 551, 457–463 (2017).
Jansson, J. K. & Hofmockel, K. S. Soil microbiomes and climate change. Nat. Rev. Microbiol. 18, 35–46 (2020).
Nelson, M. B., Martiny, A. C. & Martiny, J. B. Global biogeography of microbial nitrogen-cycling traits in soil. Proc. Natl Acad. Sci. USA 113, 8033–8040 (2016).
Bodor, A. et al. Challenges of unculturable bacteria: environmental perspectives. Rev. Environ. Sci. Biotechnol. 19, 1–22 (2020).
Bartelme, R. P. et al. Influence of substrate concentration on the culturability of heterotrophic soil microbes isolated by high-throughput dilution-to-extinction cultivation. mSphere 5, e00024-20 (2020).
Ferrari, B. C., Binnerup, S. J. & Gillings, M. Microcolony cultivation on a soil substrate membrane system selects for previously uncultured soil bacteria. Appl. Environ. Microbiol. 71, 8714–8720 (2005).
Huang, Y. et al. High-throughput microbial culturomics using automation and machine learning. Nat. Biotechnol. https://doi.org/10.1038/s41587-023-01674-2 (2023).
Schöler, A., Jacquiod, S., Vestergaard, G., Schulz, S. & Schloter, M. Analysis of soil microbial communities based on amplicon sequencing of marker genes. Biol. Fertil. Soils 53, 485–489 (2017).
McArdle, A. J. & Kaforou, M. Sensitivity of shotgun metagenomics to host DNA: abundance estimates depend on bioinformatic tools and contamination is the main issue. Access Microbiol. 2, acmi000104 (2020).
Van der Walt, A. J. et al. Assembling metagenomes, one community at a time. BMC Genomics 18, 521 (2017).
Vandeputte, D. et al. Quantitative microbiome profiling links gut community variation to microbial load. Nature 551, 507–511 (2017).
Carvalhais, L. C., Dennis, P. G., Tyson, G. W. & Schenk, P. M. Application of metatranscriptomics to soil environments. J. Microbiol. Methods 91, 246–251 (2012).
Hestrin, R. et al. Plant-associated fungi support bacterial resilience following water limitation. ISME J. 16, 2752–2762 (2022).
Callister, S. J. et al. Addressing the challenge of soil metaproteome complexity by improving metaproteome depth of coverage through two-dimensional liquid chromatography. Soil Biol. Biochem. 125, 290–299 (2018).
Lin, V. S. Interrogating plant–microbe interactions with chemical tools: click chemistry reagents for metabolic labeling and activity-based probes. Molecules 26, 243 (2021).
Whidbey, C. & Wright, A. T. In Activity-Based Protein Profiling (eds Cravatt, B. F., Hsu, K.-L. & Weerapana, E.) 1–21 (Springer International, 2019).
Shaffer, M. et al. DRAM for distilling microbial metabolism to automate the curation of microbiome function. Nucleic Acids Res. 48, 8883–8900 (2020).
Chowdhury, T. R. et al. Metaphenomic responses of a native prairie soil microbiome to moisture perturbations. mSystems 4, e00061-19 (2019).
Forsberg, E. M. et al. Data processing, multi-omic pathway mapping, and metabolite activity analysis using XCMS Online. Nat. Protoc. 13, 633–651 (2018).
Ahmed, V., Verma, M. K., Gupta, S., Mandhan, V. & Chauhan, N. S. Metagenomic profiling of soil microbes to mine salt stress tolerance genes. Front. Microbiol. 9, 159 (2018).
Alvarez, T. M. et al. Structure and function of a novel cellulase 5 from sugarcane soil metagenome. PLoS ONE 8, e83635 (2013).
Lee, M. H. et al. A new esterase EstD2 isolated from plant rhizosphere soil metagenome. Appl. Microbiol. Biotechnol. 88, 1125–1134 (2010).
Da Rocha, U. N., Andreote, F. D., de Azevedo, J. L., van Elsas, J. D. & van Overbeek, L. S. Cultivation of hitherto-uncultured bacteria belonging to the Verrucomicrobia subdivision 1 from the potato (Solanum tuberosum L.) rhizosphere. J. Soils Sediments 10, 326–339 (2010).
Sharma, S., Anand, G., Singh, N. & Kapoor, R. Arbuscular mycorrhiza augments arsenic tolerance in wheat (Triticum aestivum L.) by strengthening antioxidant defense system and thiol metabolism. Front. Plant Sci. 8, 906 (2017).
Sood, M. et al. Trichoderma: the ‘secrets’ of a multitalented biocontrol agent. Plants 9, 762 (2020).
Abdelfadil, M. R. et al. Clay chips and beads capture in situ barley root microbiota and facilitate in vitro long-term preservation of microbial strains. FEMS Microbiol. Ecol. 98, fiac064 (2022).
Wen, T., Zhao, M., Yuan, J., Kowalchuk, G. A. & Shen, Q. Root exudates mediate plant defense against foliar pathogens by recruiting beneficial microbes. Soil Ecol. Lett. 3, 42–51 (2021).
Thuita, M. et al. Commercial rhizobial inoculants significantly enhance growth and nitrogen fixation of a promiscuous soybean variety in Kenyan soils. Biol. Fertil. Soils 48, 87–96 (2012).
Alves, B. J., Boddey, R. M. & Urquiaga, S. The success of BNF in soybean in Brazil. Plant Soil 252, 1–9 (2003).
Ghahremani, M. & MacLean, A. M. Home sweet home: how mutualistic microbes modify root development to promote symbiosis. J. Exp. Bot. 72, 2275–2287 (2021).
Vacheron, J. et al. Plant growth-promoting rhizobacteria and root system functioning. Front. Plant Sci. 4, e356 (2013).
Arora, N. K., Egamberdieva, D., Mehnaz, S., Li, W. J. & Mishra, I. Salt tolerant rhizobacteria: for better productivity and remediation of saline soils. Front. Microbiol. 12, 660075 (2021).
Akhtar, S. S. et al. Bacillus licheniformis FMCH001 increases water use efficiency via growth stimulation in both normal and drought conditions. Front. Plant Sci. 11, 297 (2020).
De Souza, R. S. C., Armanhi, J. S. L. & Arruda, P. From microbiome to traits: designing synthetic microbial communities for improved crop resiliency. Front. Plant Sci. 11, 1179 (2020).
Mendoza-Suárez, M., Andersen, S. U., Poole, P. S. & Sánchez-Cañizares, C. Competition, nodule occupancy, and persistence of inoculant strains: key factors in the Rhizobium–legume symbioses. Front. Plant Sci. 12, 690567 (2021).
Kari, A. et al. Monitoring of soil microbial inoculants and their impact on maize (Zea mays L.) rhizosphere using T-RFLP molecular fingerprint method. Appl. Soil Ecol. 138, 233–244 (2019).
Enkerli, J., Widmer, F. & Keller, S. Long-term field persistence of Beauveria brongniartii strains applied as biocontrol agents against European cockchafer larvae in Switzerland. Biol. Control 29, 115–123 (2004).
Fu, L. et al. Inducing the rhizosphere microbiome by biofertilizer application to suppress banana Fusarium wilt disease. Soil Biol. Biochem. 104, 39–48 (2017).
Mawarda, P. C., Le Roux, X., Van Elsas, J. D. & Salles, J. F. Deliberate introduction of invisible invaders: a critical appraisal of the impact of microbial inoculants on soil microbial communities. Soil Biol. Biochem. 148, 107874 (2020).
Xu, H. et al. Rhizobium inoculation drives the shifting of rhizosphere fungal community in a host genotype dependent manner. Front. Microbiol. 10, 3135 (2020).
Zhong, Y. et al. Genotype and Rhizobium inoculation modulate the assembly of soybean rhizobacterial communities. Plant Cell Environ. 42, 2028–2044 (2019).
Hart, M. M., Antunes, P. M. & Abbott, L. K. Unknown risks to soil biodiversity from commercial fungal inoculants. Nat. Ecol. Evol. 1, 115 (2017).
Martignoni, M. M., Garnier, J., Hart, M. M. & Tyson, R. C. Investigating the impact of the mycorrhizal inoculum on the resident fungal community and on plant growth. Ecol. Modell. 438, 109321 (2020).
Chevrette, M. G., Bratburd, J. R., Currie, C. R. & Stubbendieck, R. M. Experimental microbiomes: models not to scale. mSystems 4, e00175-19 (2019).
De Roy, K., Marzorati, M., Van den Abbeele, P., Van de Wiele, T. & Boon, N. Synthetic microbial ecosystems: an exciting tool to understand and apply microbial communities. Environ. Microbiol. 16, 1472–1481 (2014).
Dolinšek, J., Goldschmidt, F. & Johnson, D. R. Synthetic microbial ecology and the dynamic interplay between microbial genotypes. FEMS Microbiol. Rev. 40, 961–979 (2016).
Wittebolle, L. et al. Initial community evenness favours functionality under selective stress. Nature 458, 623–626 (2009).
Kehe, J. et al. Massively parallel screening of synthetic microbial communities. Proc. Natl Acad. Sci. USA 116, 12804–12809 (2019).
Herrera Paredes, S. et al. Design of synthetic bacterial communities for predictable plant phenotypes. PLoS Biol. 16, e2003962 (2018).
Lozano, G. L. et al. Introducing THOR, a model microbiome for genetic dissection of community behavior. mBio 10, e02846-18 (2019).
Shayanthan, A., Ordoñez, P. A. C. & Oresnik, I. J. The role of synthetic microbial communities (SynCom) in sustainable agriculture. Front. Agron. 58, 896307 (2022).
Naylor, D. et al. Deconstructing the soil microbiome into reduced-complexity functional modules. mBio 11, e01349-20 (2020).
McClure, R. et al. Development and analysis of a stable, reduced complexity model soil microbiome. Front. Microbiol. 11, 1987 (2020).
McClure, R. et al. Interaction networks are driven by community-responsive phenotypes in a chitin-degrading consortium of soil microbes. mSystems 7, e00372-22 (2022).
Cappellato, M., Baruzzo, G., Patuzzi, I. & Di Camillo, B. Modeling microbial community networks: methods and tools. Curr. Genomics 22, 267–290 (2021).
Matchado, M. S. et al. Network analysis methods for studying microbial communities: a mini review. Comput. Struct. Biotechnol. J. 19, 2687–2698 (2021).
Li, R. et al. Co-occurrence networks depict common selection patterns, not interactions. Soil Sci. Environ. 2, 1 (2023).
Akkaya, Ö. & Arslan, E. Biotransformation of 2,4-dinitrotoluene by the beneficial association of engineered Pseudomonas putida with Arabidopsis thaliana. 3 Biotech 9, 408 (2019).
Xu, J. et al. The structure and function of the global citrus rhizosphere microbiome. Nat. Commun. 9, 4894 (2018).
Pfeiffer, S. et al. Rhizosphere microbiomes of potato cultivated in the High Andes show stable and dynamic core microbiomes with different responses to plant development. FEMS Microbiol. Ecol. 93, fiw242 (2017).
Lee, S.-M., Kong, H. G., Song, G. C. & Ryu, C.-M. Disruption of Firmicutes and Actinobacteria abundance in tomato rhizosphere causes the incidence of bacterial wilt disease. ISME J. 15, 330–347 (2021).
Armanhi, J. S. L., de Souza, R. S. C., Biazotti, B. B., Yassitepe, J. E. D. C. T. & Arruda, P. Modulating drought stress response of maize by a synthetic bacterial community. Front. Microbiol. 12, 747541 (2021).
Armanhi, J. S. L. et al. A community-based culture collection for targeting novel plant growth-promoting bacteria from the sugarcane microbiome. Front. Plant Sci. 8, 2191 (2018).
De Souza, R. S. C., Armanhi, J. S. L., Damasceno, N. D. B., Imperial, J. & Arruda, P. Genome sequences of a plant beneficial synthetic bacterial community reveal genetic features for successful plant colonization. Front. Microbiol. 10, 1779 (2019).
Wang, C. et al. Functional assembly of root‐associated microbial consortia improves nutrient efficiency and yield in soybean. J. Integr. Plant Biol. 63, 1021–1035 (2021).
Liu, H. et al. Effective colonisation by a bacterial synthetic community promotes plant growth and alters soil microbial community. J. Sustain. Agric. Environ. 1, 30–42 (2022).
Bankhead, S. B., Landa, B. B., Lutton, E., Weller, D. M. & Gardener, B. B. M. Minimal changes in rhizobacterial population structure following root colonization by wild type and transgenic biocontrol strains. FEMS Microbiol. Ecol. 49, 307–318 (2004).
Van Geel, M., De Beenhouwer, M., Lievens, B. & Honnay, O. Crop-specific and single-species mycorrhizal inoculation is the best approach to improve crop growth in controlled environments. Agron. Sustain. Dev. 36, 37 (2016).
Vestberg, M. The effect of vesicular–arbuscular mycorrhizal inoculation on the growth and root colonization of ten strawberry cultivars. Agric. Food Sci. 1, 527–535 (1992).
Felici, C. et al. Single and co-inoculation of Bacillus subtilis and Azospirillum brasilense on Lycopersicon esculentum: effects on plant growth and rhizosphere microbial community. Appl. Soil Ecol. 40, 260–270 (2008).
Berendsen, R. L. et al. Disease-induced assemblage of a plant-beneficial bacterial consortium. ISME J. 12, 1496–1507 (2018).
Gerrits, G. M. et al. Synthesis on the effectiveness of soil translocation for plant community restoration. J. Appl. Ecol. 60, 714–724 (2023).
Pantoja Angles, A., Valle-Pérez, A. U., Hauser, C. & Mahfouz, M. M. Microbial biocontainment systems for clinical, agricultural, and industrial applications. Front. Bioeng. Biotechnol. 10, 830200 (2022).
De Lorenzo, V. & Danchin, A. Synthetic biology: discovering new worlds and new words. EMBO Rep. 9, 822–827 (2008).
Temme, K., Zhao, D. & Voigt, C. A. Refactoring the nitrogen fixation gene cluster from Klebsiella oxytoca. Proc. Natl Acad. Sci. USA 109, 7085–7090 (2012).
Del Valle, I. et al. Soil organic matter attenuates the efficacy of flavonoid-based plant–microbe communication. Sci. Adv. 6, eaax8254 (2020).
Shulse, C. N. et al. Engineered root bacteria release plant-available phosphate from phytate. Appl. Environ. Microbiol. 85, e01210-19 (2019).
Del Valle, I. et al. Translating new synthetic biology advances for biosensing into the earth and environmental sciences. Front. Microbiol. 11, 618373 (2020).
Wen, A. et al. Enabling biological nitrogen fixation for cereal crops in fertilized fields. ACS Synth. Biol. 10, 3264–3277 (2021).
Egbert, R. G. et al. A versatile platform strain for high-fidelity multiplex genome editing. Nucleic Acids Res. 47, 3244–3256 (2019).
Sridhar, S., Ajo-Franklin, C. M. & Masiello, C. A. A framework for the systematic selection of biosensor chassis for environmental synthetic biology. ACS Synth. Biol. 11, 2909–2916 (2022).
Nikel, P. I., Chavarria, M., Danchin, A. & de Lorenzo, V. From dirt to industrial applications: Pseudomonas putida as a synthetic biology chassis for hosting harsh biochemical reactions. Curr. Opin. Chem. Biol. 34, 20–29 (2016).
Vo, P. L. H. et al. CRISPR RNA-guided integrases for high-efficiency, multiplexed bacterial genome engineering. Nat. Biotechnol. 39, 480–489 (2021).
Huang, P.-H. et al. M-TUBE enables large-volume bacterial gene delivery using a high-throughput microfluidic electroporation platform. PLoS Biol. 20, e3001727 (2022).
Shih, S. C. C. et al. A versatile microfluidic device for automating synthetic biology. ACS Synth. Biol. 4, 1151–1164 (2015).
Riley, L. A., Ji, L., Schmitz, R. J., Westpheling, J. & Guss, A. M. Rational development of transformation in Clostridium thermocellum ATCC 27405 via complete methylome analysis and evasion of native restriction-modification systems. J. Ind. Microbiol. Biotechnol. 46, 1435–1443 (2019).
Tourancheau, A., Mead, E. A., Zhang, X.-S. & Fang, G. Discovering multiple types of DNA methylation from bacteria and microbiome using nanopore sequencing. Nat. Methods 18, 491–498 (2021).
Yim, S. S. et al. Multiplex transcriptional characterizations across diverse bacterial species using cell‐free systems. Mol. Syst. Biol. 15, e8875 (2019).
Elmore, J. R. et al. High-throughput genetic engineering of nonmodel and undomesticated bacteria via iterative site-specific genome integration. Sci. Adv. 9, eade1285 (2023).
Younger, D., Berger, S., Baker, D. & Klavins, E. High-throughput characterization of protein–protein interactions by reprogramming yeast mating. Proc. Natl Acad. Sci. USA 114, 12166–12171 (2017).
Nielsen, A. A. et al. Genetic circuit design automation. Science 352, aac7341 (2016).
Yeh, A. H.-W. et al. De novo design of luciferases using deep learning. Nature 614, 774–780 (2023).
Madani, A. et al. Large language models generate functional protein sequences across diverse families. Nat. Biotechnol. 41, 1099–1106 (2023).
Yu, D. et al. An efficient recombination system for chromosome engineering in Escherichia coli. Proc. Natl Acad. Sci. USA 97, 5978–5983 (2000).
Garst, A. D. et al. Genome-wide mapping of mutations at single-nucleotide resolution for protein, metabolic and genome engineering. Nat. Biotechnol. 35, 48–55 (2017).
Brophy, J. A. N. et al. Engineered integrative and conjugative elements for efficient and inducible DNA transfer to undomesticated bacteria. Nat. Microbiol. 3, 1043–1053 (2018).
Wang, G. et al. CRAGE enables rapid activation of biosynthetic gene clusters in undomesticated bacteria. Nat. Microbiol. 4, 2498–2510 (2019).
Rottinghaus, A. G., Vo, S. & Moon, T. S. Computational design of CRISPR guide RNAs to enable strain-specific control of microbial consortia. Proc. Natl Acad. Sci. USA 120, e2213154120 (2023).
Ronda, C., Chen, S. P., Cabral, V., Yaung, S. J. & Wang, H. H. Metagenomic engineering of the mammalian gut microbiome in situ. Nat. Methods 16, 167–170 (2019).
Rubin, B. E. et al. Species- and site-specific genome editing in complex bacterial communities. Nat. Microbiol. 7, 34–47 (2021).
Singh, J. S., Abhilash, P. C., Singh, H. B., Singh, R. P. & Singh, D. P. Genetically engineered bacteria: an emerging tool for environmental remediation and future research perspectives. Gene 480, 1–9 (2011).
Pant, G. et al. Biological approaches practised using genetically engineered microbes for a sustainable environment: a review. J. Hazard. Mater. 405, 124631 (2021).
Liu, L., Bilal, M., Duan, X. & Iqbal, H. M. N. Mitigation of environmental pollution by genetically engineered bacteria—current challenges and future perspectives. Sci. Total Environ. 667, 444–454 (2019).
Ronchel, M. C. & Ramos, J. L. Dual system to reinforce biological containment of recombinant bacteria designed for rhizoremediation. Appl. Environ. Microbiol. 67, 2649–2656 (2001).
Asin-Garcia, E. et al. Phosphite synthetic auxotrophy as an effective biocontainment strategy for the industrial chassis Pseudomonas putida. Microb. Cell Factories 21, 156 (2022).
Mandell, D. J. et al. Biocontainment of genetically modified organisms by synthetic protein design. Nature 518, 55–60 (2015).
Chan, C. T. Y., Lee, J. W., Cameron, D. E., Bashor, C. J. & Collins, J. J. ‘Deadman’ and ‘Passcode’ microbial kill switches for bacterial containment. Nat. Chem. Biol. 12, 82–86 (2016).
Rottinghaus, A. G., Ferreiro, A., Fishbein, S. R. S., Dantas, G. & Moon, T. S. Genetically stable CRISPR-based kill switches for engineered microbes. Nat. Commun. 13, 672 (2022).
Park, S. et al. Construction of Bacillus thuringiensis simulant strains suitable for environmental release. Appl. Environ. Microbiol. 83, e00126-17 (2017).
Jaderlund, L., Hellman, M., Sundh, I., Bailey, M. J. & Jansson, J. K. Use of a novel nonantibiotic triple marker gene cassette to monitor high survival of Pseudomonas fluorescens SBW25 on winter wheat in the field. FEMS Microbiol. Ecol. 63, 156–168 (2008).
Yee, M. O. et al. Specialized plant growth chamber designs to study complex rhizosphere interactions. Front. Microbiol. 12, 625752 (2021).
Zengler, K. et al. EcoFABs: advancing microbiome science through standardized fabricated ecosystems. Nat. Methods 16, 567–571 (2019).
Aufrecht, J. et al. Hotspots of root-exuded amino acids are created within a rhizosphere-on-a-chip. Lab Chip 22, 954–963 (2022).
Handakumbura, P. P., Rivas Ubach, A. & Battu, A. K. Visualizing the hidden half: plant–microbe interactions in the rhizosphere. mSystems 6, e0076521 (2021).
Del Valle, I., Gao, X., Ghezzehei, T. A., Silberg, J. J. & Masiello, C. A. Artificial soils reveal individual factor controls on microbial processes. mSystems 7, e0030122 (2022).
Tian, B., Pei, Y., Huang, W., Ding, J. & Siemann, E. Increasing flavonoid concentrations in root exudates enhance associations between arbuscular mycorrhizal fungi and an invasive plant. ISME J. 15, 1919–1930 (2021).
Hu, L. et al. Root exudate metabolites drive plant–soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat. Commun. 9, 2738 (2018).
Geddes, B. A. et al. Engineering transkingdom signalling in plants to control gene expression in rhizosphere bacteria. Nat. Commun. 10, 3430 (2019).
Haskett, T. L. et al. Engineered plant control of associative nitrogen fixation. Proc. Natl Acad. Sci. USA 119, e2117465119 (2022).
Kaeppler, S. M. et al. Variation among maize inbred lines and detection of quantitative trait loci for growth at low phosphorus and responsiveness to arbuscular mycorrhizal fungi. Crop Sci. 40, 358–364 (2000).
Tosi, M., Mitter, E. K., Gaiero, J. & Dunfield, K. It takes three to tango: the importance of microbes, host plant, and soil management to elucidate manipulation strategies for the plant microbiome. Can. J. Microbiol. 66, 413–433 (2020).
Acknowledgements
This work was supported by the US Department of Energy (DOE) Office of Biological and Environmental Research as part of the Genomic Science Program and is a contribution of the Pacific Northwest National Laboratory (PNNL) Secure Biosystems Design Science Focus Area entitled ‘Persistence Control of Engineered Functions in Complex Soil Microbiomes’. PNNL is a multiprogram national laboratory operated by Battelle Memorial Institute for the DOE under contract DE-AC05-76RL01830.
Author information
Authors and Affiliations
Contributions
All authors contributed equally to the writing and formulation of figures.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Peer review
Peer review information
Nature Biotechnology thanks Giles Oldroyd, Paul Bodelier, and Marnix Medema for their contribution to the peer review of this work.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Jansson, J.K., McClure, R. & Egbert, R.G. Soil microbiome engineering for sustainability in a changing environment. Nat Biotechnol 41, 1716–1728 (2023). https://doi.org/10.1038/s41587-023-01932-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41587-023-01932-3
This article is cited by
-
Soil microbiome characterization and its future directions with biosensing
Journal of Biological Engineering (2024)
-
Natural plant disease suppressiveness in soils extends to insect pest control
Microbiome (2024)
-
Viability of enhancing methanotrophy in terrestrial ecosystems exposed to low concentrations of methane
Communications Earth & Environment (2024)
-
Superiority of native soil core microbiomes in supporting plant growth
Nature Communications (2024)
-
Advances in understanding plant-pathogen interactions: insights from tomato as a model system
VirusDisease (2024)