Ecosystem consequences of introducing plant growth promoting rhizobacteria to managed systems and potential legacy effects
Abstract
The rapidly growing industry of crop biostimulants leverages the application of plant growth promoting rhizobacteria (PGPR) to promote plant growth and health. However, introducing nonnative rhizobacteria may impact other aspects of ecosystem functioning and have legacy effects; these potential consequences are largely unexplored. Nontarget consequences of PGPR may include changes in resident microbiomes, nutrient cycling, pollinator services, functioning of other herbivores, disease suppression, and organic matter persistence. Importantly, we lack knowledge of whether these ecosystem effects may manifest in adjacent ecosystems. The introduced PGPR can leave a functional legacy whether they persist in the community or not. Legacy effects include shifts in resident microbiomes and their temporal dynamics, horizontal transfer of genes from the PGPR to resident taxa, and changes in resident functional groups and interaction networks. Ecosystem functions may be affected by legacies PGPR leave following niche construction, such as when PGPR alter soil pH that in turn alters biogeochemical cycling rates. Here, we highlight new research directions to elucidate how introduced PGPR impact resident microbiomes and ecosystem functions and their capacity for legacy effects.
- Authors:
-
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1870242
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Journal Article: Accepted Manuscript
- Journal Name:
- New Phytologist
- Additional Journal Information:
- Journal Volume: 234; Journal Issue: 6; Journal ID: ISSN 0028-646X
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; agroecology; biostimulant; invasion ecology; microbiome; plant growth promoting bacteria; plant-microbe interactions
Citation Formats
Moore, Jessica A. M., Abraham, Paul E., Michener, Joshua K., Muchero, Wellington, and Cregger, Melissa A. Ecosystem consequences of introducing plant growth promoting rhizobacteria to managed systems and potential legacy effects. United States: N. p., 2022.
Web. doi:10.1111/nph.18010.
Moore, Jessica A. M., Abraham, Paul E., Michener, Joshua K., Muchero, Wellington, & Cregger, Melissa A. Ecosystem consequences of introducing plant growth promoting rhizobacteria to managed systems and potential legacy effects. United States. https://doi.org/10.1111/nph.18010
Moore, Jessica A. M., Abraham, Paul E., Michener, Joshua K., Muchero, Wellington, and Cregger, Melissa A. 2022.
"Ecosystem consequences of introducing plant growth promoting rhizobacteria to managed systems and potential legacy effects". United States. https://doi.org/10.1111/nph.18010. https://www.osti.gov/servlets/purl/1870242.
@article{osti_1870242,
title = {Ecosystem consequences of introducing plant growth promoting rhizobacteria to managed systems and potential legacy effects},
author = {Moore, Jessica A. M. and Abraham, Paul E. and Michener, Joshua K. and Muchero, Wellington and Cregger, Melissa A.},
abstractNote = {The rapidly growing industry of crop biostimulants leverages the application of plant growth promoting rhizobacteria (PGPR) to promote plant growth and health. However, introducing nonnative rhizobacteria may impact other aspects of ecosystem functioning and have legacy effects; these potential consequences are largely unexplored. Nontarget consequences of PGPR may include changes in resident microbiomes, nutrient cycling, pollinator services, functioning of other herbivores, disease suppression, and organic matter persistence. Importantly, we lack knowledge of whether these ecosystem effects may manifest in adjacent ecosystems. The introduced PGPR can leave a functional legacy whether they persist in the community or not. Legacy effects include shifts in resident microbiomes and their temporal dynamics, horizontal transfer of genes from the PGPR to resident taxa, and changes in resident functional groups and interaction networks. Ecosystem functions may be affected by legacies PGPR leave following niche construction, such as when PGPR alter soil pH that in turn alters biogeochemical cycling rates. Here, we highlight new research directions to elucidate how introduced PGPR impact resident microbiomes and ecosystem functions and their capacity for legacy effects.},
doi = {10.1111/nph.18010},
url = {https://www.osti.gov/biblio/1870242},
journal = {New Phytologist},
issn = {0028-646X},
number = 6,
volume = 234,
place = {United States},
year = {Mon Jan 31 00:00:00 EST 2022},
month = {Mon Jan 31 00:00:00 EST 2022}
}
Works referenced in this record:
Controlling the Implementation of Transgenic Microbes: Are We Ready for What Synthetic Biology Has to Offer?
journal, May 2020
- Stirling, Finn; Silver, Pamela A.
- Molecular Cell, Vol. 78, Issue 4
Plant nodulation inducers enhance horizontal gene transfer of Azorhizobium caulinodans symbiosis island
journal, November 2016
- Ling, Jun; Wang, Hui; Wu, Ping
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 48
Efficiency of probiotic traits in plant inoculation is determined by environmental constrains
journal, September 2020
- da Costa, Pedro Beschoren; van Elsas, Jan Dirk; Mallon, Cyrus
- Soil Biology and Biochemistry, Vol. 148
Environmental Filtering, Niche Construction, and Trait Variability: The Missing Discussion
journal, December 2017
- Thakur, Madhav P.; Wright, Alexandra J.
- Trends in Ecology & Evolution, Vol. 32, Issue 12
Plant growth promoting rhizobacteria increase the efficiency of fertilisers while reducing nitrogen loss
journal, March 2019
- Paungfoo-Lonhienne, Chanyarat; Redding, Matthew; Pratt, Chris
- Journal of Environmental Management, Vol. 233
Microbial Inoculants: Silver Bullet or Microbial Jurassic Park?
journal, April 2021
- Jack, Chandra N.; Petipas, Renee H.; Cheeke, Tanya E.
- Trends in Microbiology, Vol. 29, Issue 4
Nodulating strains of Rhizobium loti arise through chromosomal symbiotic gene transfer in the environment.
journal, September 1995
- Sullivan, J. T.; Patrick, H. N.; Lowther, W. L.
- Proceedings of the National Academy of Sciences, Vol. 92, Issue 19
Transient invaders can induce shifts between alternative stable states of microbial communities
journal, February 2020
- Amor, Daniel R.; Ratzke, Christoph; Gore, Jeff
- Science Advances, Vol. 6, Issue 8
Specific recruitment of soil bacteria and fungi decomposers following a biostimulant application increased crop residues mineralization
journal, December 2018
- Hellequin, Eve; Monard, Cécile; Quaiser, Achim
- PLOS ONE, Vol. 13, Issue 12
Horizontal gene transfer overrides mutation in Escherichia coli colonizing the mammalian gut
journal, August 2019
- Frazão, Nelson; Sousa, Ana; Lässig, Michael
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 36
Stoichiometrically coupled carbon and nitrogen cycling in the MIcrobial-MIneral Carbon Stabilization model version 1.0 (MIMICS-CN v1.0)
journal, January 2020
- Kyker-Snowman, Emily; Wieder, William R.; Frey, Serita D.
- Geoscientific Model Development, Vol. 13, Issue 9
Population densities of indigenous Acidobacteria change in the presence of plant growth promoting rhizobacteria (PGPR) in rhizosphere
journal, April 2017
- Kalam, Sadaf; Das, Subha Narayan; Basu, Anirban
- Journal of Basic Microbiology, Vol. 57, Issue 5
Building the microbiome in health and disease: niche construction and social conflict in bacteria
journal, August 2015
- McNally, Luke; Brown, Sam P.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 370, Issue 1675
Co-inoculation of Glomus intraradices and Trichoderma atroviride acts as a biostimulant to promote growth, yield and nutrient uptake of vegetable crops
journal, September 2014
- Colla, Giuseppe; Rouphael, Youssef; Di Mattia, Elena
- Journal of the Science of Food and Agriculture, Vol. 95, Issue 8
Tracking microbial evolution in the human gut using Hi-C reveals extensive horizontal gene transfer, persistence and adaptation
journal, December 2019
- Yaffe, Eitan; Relman, David A.
- Nature Microbiology, Vol. 5, Issue 2
Widespread transfer of mobile antibiotic resistance genes within individual gut microbiomes revealed through bacterial Hi-C
journal, September 2020
- Kent, Alyssa G.; Vill, Albert C.; Shi, Qiaojuan
- Nature Communications, Vol. 11, Issue 1
Induced Systemic Resistance by Beneficial Microbes
journal, August 2014
- Pieterse, Corné M. J.; Zamioudis, Christos; Berendsen, Roeland L.
- Annual Review of Phytopathology, Vol. 52, Issue 1
Rapid evolution of adaptive niche construction in experimental microbial populations
journal, September 2014
- Callahan, Benjamin J.; Fukami, Tadashi; Fisher, Daniel S.
- Evolution, Vol. 68, Issue 11
Selection on soil microbiomes reveals reproducible impacts on plant function
journal, October 2014
- Panke-Buisse, Kevin; Poole, Angela C.; Goodrich, Julia K.
- The ISME Journal, Vol. 9, Issue 4
Plant biostimulants: innovative tool for enhancing plant nutrition in organic farming
journal, January 2018
- De Pascale, S.; Rouphael, Y.; Colla, G.
- European Journal of Horticultural Science, Vol. 82, Issue 6
The impact of interactions on invasion and colonization resistance in microbial communities
journal, January 2021
- Kurkjian, Helen M.; Akbari, M. Javad; Momeni, Babak
- PLOS Computational Biology, Vol. 17, Issue 1
Post-Antibiotic Gut Mucosal Microbiome Reconstitution Is Impaired by Probiotics and Improved by Autologous FMT
journal, September 2018
- Suez, Jotham; Zmora, Niv; Zilberman-Schapira, Gili
- Cell, Vol. 174, Issue 6
Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health
journal, September 2015
- Wei, Zhong; Yang, Tianjie; Friman, Ville-Petri
- Nature Communications, Vol. 6, Issue 1
Biotic Interactions Are More Important than Propagule Pressure in Microbial Community Invasions
journal, October 2020
- Albright, Michaeline B. N.; Sevanto, Sanna; Gallegos-Graves, La Verne
- mBio, Vol. 11, Issue 5
The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter?
journal, February 2013
- Cotrufo, M. Francesca; Wallenstein, Matthew D.; Boot, Claudia M.
- Global Change Biology, Vol. 19, Issue 4
Recording mobile DNA in the gut microbiota using an Escherichia coli CRISPR-Cas spacer acquisition platform
journal, January 2020
- Munck, Christian; Sheth, Ravi U.; Freedberg, Daniel E.
- Nature Communications, Vol. 11, Issue 1
Bio-fertilizer application induces soil suppressiveness against Fusarium wilt disease by reshaping the soil microbiome
journal, November 2017
- Xiong, Wu; Guo, Sai; Jousset, Alexandre
- Soil Biology and Biochemistry, Vol. 114
Insight Into the Role of PGPR in Sustainable Agriculture and Environment
journal, June 2021
- Mohanty, Pratikhya; Singh, Puneet Kumar; Chakraborty, Debosmita
- Frontiers in Sustainable Food Systems, Vol. 5
Engineering rhizobacteria for sustainable agriculture
journal, November 2020
- Haskett, Timothy L.; Tkacz, Andrzej; Poole, Philip S.
- The ISME Journal, Vol. 15, Issue 4
Getting the ecology into interactions between plants and the plant growth-promoting bacterium Pseudomonas fluorescens
journal, January 2013
- Hol, W. H. Gera; Bezemer, T. Martijn; Biere, Arjen
- Frontiers in Plant Science, Vol. 4
Effects of phosphorus-mobilizing bacteria on tomato growth and soil microbial activity
journal, December 2017
- Nassal, Dinah; Spohn, Marie; Eltlbany, Namis
- Plant and Soil, Vol. 427, Issue 1-2
Microbiome Engineering: Synthetic Biology of Plant-Associated Microbiomes in Sustainable Agriculture
journal, March 2021
- Ke, Jing; Wang, Bing; Yoshikuni, Yasuo
- Trends in Biotechnology, Vol. 39, Issue 3
Plant Defense by VOC-Induced Microbial Priming
journal, March 2019
- Liu, Hongwei; Brettell, Laura E.
- Trends in Plant Science, Vol. 24, Issue 3
PGPR Mediated Alterations in Root Traits: Way Toward Sustainable Crop Production
journal, January 2021
- Grover, Minakshi; Bodhankar, Shrey; Sharma, Abha
- Frontiers in Sustainable Food Systems, Vol. 4
Biostimulants in agriculture
journal, August 2015
- Brown, Patrick; Saa, Sebastian
- Frontiers in Plant Science, Vol. 6
Plant Growth‐Promoting Rhizobacteria (PGPR) Reduce Evaporation and Increase Soil Water Retention
journal, May 2018
- Zheng, Wenjuan; Zeng, Saiqi; Bais, Harsh
- Water Resources Research, Vol. 54, Issue 5
A Plant Growth-Promoting Microbial Soil Amendment Dynamically Alters the Strawberry Root Bacterial Microbiome
journal, November 2019
- Deng, Siwen; Wipf, Heidi M. -L.; Pierroz, Grady
- Scientific Reports, Vol. 9, Issue 1
The impact of failure: unsuccessful bacterial invasions steer the soil microbial community away from the invader’s niche
journal, January 2018
- Mallon, C. A.; Le Roux, X.; van Doorn, G. S.
- The ISME Journal, Vol. 12, Issue 3