Award Abstract # 1738009
Dimensions: Collaborative Research: Elucidating the drivers of mutualism variation in host-symbiont metapopulations

NSF Org: DEB
Division Of Environmental Biology
Recipient: REGENTS OF THE UNIVERSITY OF CALIFORNIA AT RIVERSIDE
Initial Amendment Date: August 2, 2017
Latest Amendment Date: August 2, 2017
Award Number: 1738009
Award Instrument: Standard Grant
Program Manager: Leslie J. Rissler
lrissler@nsf.gov
 (703)292-4628
DEB
 Division Of Environmental Biology
BIO
 Directorate for Biological Sciences
Start Date: October 1, 2017
End Date: September 30, 2022 (Estimated)
Total Intended Award Amount: $892,835.00
Total Awarded Amount to Date: $892,835.00
Funds Obligated to Date: FY 2017 = $892,835.00
History of Investigator:
  • Joel Sachs (Principal Investigator)
    joel.sachs@ucr.edu
Recipient Sponsored Research Office: University of California-Riverside
200 UNIVERSTY OFC BUILDING
RIVERSIDE
CA  US  92521-0001
(951)827-5535
Sponsor Congressional District: 39
Primary Place of Performance: University of California-Riverside
CA  US  92521-0001
Primary Place of Performance
Congressional District:
39
Unique Entity Identifier (UEI): MR5QC5FCAVH5
Parent UEI:
NSF Program(s): Dimensions of Biodiversity
Primary Program Source: 01001718DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s):
Program Element Code(s): 796800
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.074

ABSTRACT

Symbiotic bacteria transform how plants and animals interact with their environment. These bacteria are well known for their ability to enhance host growth and tolerance to stress, but symbioses vary greatly in their effects on host health and fitness. Little is understood about the forces that shape this variation and drive the spread of symbionts that interact, but fail to benefit the host. Here, researchers use the relationship between native California legumes and nitrogen-fixing Bradyrhizobium bacteria to study the drivers of variation in symbioses. The project will employ environmental sampling of interacting plants, bacteria, and soil, genetic approaches, and greenhouse experiments. The research will determine the magnitude of benefits the bacteria provide to the host, what bacterial genes facilitate benefit or exploitation of the host, and how the host responds and defends itself against ineffective symbionts. The project will train undergraduate and graduate students as well as two postdoctoral fellows. The researchers will educate local farmers on plant-microbe interactions, and they will generate and curate a collection of plant and bacterial variants that will be made freely available to other researchers. The project is important because it will provide information on the parameters that influence symbiosis and help guide how microbes can be better deployed to increase productivity of agricultural systems and promote health of humans and the planet.

The maintenance of diversity in microbial symbioses is paradoxical. Conventional theory predicts a lack of variation in symbiont function because host species reward beneficial symbionts and intensely select against ineffective partners. Here, a novel framework is tested to explain the maintenance of symbiont variation. The planned work transcends the dominant theoretical paradigm by investigating ecological, spatiotemporal, and genomic drivers in a metapopulation of rhizobial bacteria and their native legume hosts. Like other hosts, legumes exhibit host control traits: legumes can discriminate against ineffective rhizobia during nodule formation, and can reduce within-nodule growth rates of ineffective rhizobia. Despite the apparent efficiency of host control, ineffective rhizobia are commonly uncovered in natural and agricultural soils. Four aims are proposed to explain the maintenance of symbiont variation in this key model system. Experimental inoculations coupled with genetic and selection analysis are used to investigate i) variation among legume host populations in their capacity to sanction ineffective rhizobia, ii) the spatial and phylogenetic origins of invasions by ineffective rhizobia, and iii) the genomic basis for the evolution of ineffective rhizobia. iv) Inferred invasions of ineffective rhizobia will be recapitulated using experiments that test fitness predictions under realistic conditions. This work challenges conventional mutualism theory and highlights the importance of genetic variation, spatio-temporal dynamics, and fitness tradeoffs.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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(Showing: 1 - 10 of 15)
Forrester, Nicole_J and RebolledaGómez, Maria and Sachs, Joel_L and Ashman, TiaLynn "Polyploid plants obtain greater fitness benefits from a nutrient acquisition mutualism" New Phytologist , v.227 , 2020 https://doi.org/10.1111/nph.16574 Citation Details
Fronk, David C. and Sachs, Joel L. "Symbiotic organs: the nexus of hostmicrobe evolution" Trends in Ecology & Evolution , v.37 , 2022 https://doi.org/10.1016/j.tree.2022.02.014 Citation Details
Gano-Cohen, Kelsey A. and Wendlandt, Camille E. and Al Moussawi, Khadija and Stokes, Peter J. and Quides, Kenjiro W. and Weisberg, Alexandra J. and Chang, Jeff. H. and Sachs, Joel L. "Recurrent mutualism breakdown events in a legume rhizobia metapopulation" Proceedings of the Royal Society B: Biological Sciences , v.287 , 2020 10.1098/rspb.2019.2549 Citation Details
GanoCohen, Kelsey A. and Wendlandt, Camille E. and Stokes, Peter J. and Blanton, Mia A. and Quides, Kenjiro W. and Zomorrodian, Avissa and Adinata, Eunice S. and Sachs, Joel L. and Johnson, ed., Nancy "Interspecific conflict and the evolution of ineffective rhizobia" Ecology Letters , v.22 , 2019 https://doi.org/10.1111/ele.13247 Citation Details
OrtizBarbosa, Gabriel S. and TorresMartínez, Lorena and Manci, Angela and Neal, Sierra and Soubra, Tarek and Khairi, Fizzah and Trinh, Jerry and Cardenas, Paola and Sachs, Joel L. "No disruption of rhizobial symbiosis during early stages of cowpea domestication" Evolution , v.76 , 2022 https://doi.org/10.1111/evo.14424 Citation Details
Ortiz-Barbosa, G. S. and Torres-Martínez, L. and Rothschild, J. and Sachs, J. L. "Lotus japonicus regulates root nodulation and nitrogen fixation dependent on the molecular form of nitrogen fertilizer" Plant and Soil , 2022 https://doi.org/10.1007/s11104-022-05762-1 Citation Details
Porter, Stephanie S. and Sachs, Joel L. "Agriculture and the Disruption of PlantMicrobial Symbiosis" Trends in Ecology & Evolution , v.35 , 2020 10.1016/j.tree.2020.01.006 Citation Details
Quides, Kenjiro W. and Salaheldine, Fathi and Jariwala, Ruchi and Sachs, Joel L. "Dysregulation of hostcontrol causes interspecific conflict over host investment into symbiotic organs" Evolution , v.75 , 2021 https://doi.org/10.1111/evo.14173 Citation Details
Quides, Kenjiro W. and Weisberg, Alexandra J. and Trinh, Jerry and Salaheldine, Fathi and Cardenas, Paola and Lee, Hsu-Han and Jariwala, Ruchi and Chang, Jeff H. and Sachs, Joel L. "Experimental evolution can enhance benefits of rhizobia to novel legume hosts" Proceedings of the Royal Society B: Biological Sciences , v.288 , 2021 https://doi.org/10.1098/rspb.2021.0812 Citation Details
Sachs, Joel L. and Quides, Kenjiro W. and Wendlandt, Camille E. "Legumes versus rhizobia: a model for ongoing conflict in symbiosis" New Phytologist , v.219 , 2018 10.1111/nph.15222 Citation Details
TorresMartínez, Lorena and Porter, Stephanie S. and Wendlandt, Camille and Purcell, Jessica and OrtizBarbosa, Gabriel and Rothschild, Jacob and Lampe, Mathew and Warisha, Farsamin and Le, Tram and Weisberg, Alexandra J. and Chang, Jeff H. and Sachs, Joe "Evolution of specialization in a plantmicrobial mutualism is explained by the oscillation theory of speciation" Evolution , v.75 , 2021 https://doi.org/10.1111/evo.14222 Citation Details
(Showing: 1 - 10 of 15)

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

Intellectual Merit: Symbiotic nitrogen fixation is an important beneficial service that rhizobial bacteria provide to legume plants. This association is essential for providing biologically useable nitrogen in natural and agricultural settings and why we use legumes in crop rotations, as well as green manures and cover crops. However, symbiotic nitrogen fixation, along with other microbal-provided beneficial services to plant and animal hosts, are highly varied and unreliable to hosts. For example, the practice of introducing “elite” rhizobial bacteria into soils is often unsuccessful. We characterized genetic and ecological features of services of symbiotic nitrogen-fixation to understand the drivers of symbiosis instability. We used the association between a native species of legume plants and their rhizobial symbionts as a model system to understand why these interactions vary.

We found that rhizobia vary greatly in the magnitude of nitrogen fixed for the native California legume, Acmispon strigosus. Eighty-five rhizobia strains, isolated from across a 750 kilometer transect, were experimentally characterized. These strains were found to vary in the capacity to induce symbiotic nodules on host roots and in their ability to provide fixed nitrogen to hosts, and included strains that offered no benefits at all. Genome sequencing demonstrated that strains that did not induce symbiotic nodules lacked a mobile genetic element that carries clusters of genes necessary for root nodulation and nitrogen fixation. Strains that did induce nodules but did not fix nitrogen had the necessary genes, but they were altered in composition, suggesting adaptation to alternate legume species, and reshuffling of the mobile genetic element.

Evidence showed that symbiosis instability can be driven by competition among rhizobia to infect plants and host specificity. Experimental infections of plants that combined multiple strains of rhizobia consistently provided plants with reduced benefit, compared to infections with the same strains in isolation. Experimental and genomic evidence suggested that rhizobia can associate with multiple plant species, and that providing nitrogen benefits to one species can be associated with the loss of beneficial interactions with other local hosts.

Benefits provided by rhizobia to plants thus depend on the community context. Importantly, we need to consider the variation in host species that the rhizobia can interact with and the presence of other strains that compete for those host plants.

 

Broader impacts: Harnessing capabilities of microbes is crucial for advancing sustainable ways to enhance the health of humans, crops, and livestock. However, this remains a tremendous challenge of the next century. Implementation of bacteria has been limited because of our poor understanding of the forces that shape their services. Our research uncovered the important role of microbial competition and host specificity in driving variation in these services, knowledge that can be applied in any system where microbes are used as bioinoculants or therapies for plants or animals.

The funded research was an important means for developing human resource, It led to training of scientists at all levels, including high school students (2), undergraduates (22), graduate students, (5) and postdoctoral scholars (3; 2 of which are currently in faculty positions). The research training provided high school students and undergraduate students with unique opportunities to work with real world datasets and for experiential learning. Moreover, the learning experiences were opportunities to gain skills in communication and teamwork. Each of these are critical for success in STEM. More than 18 peer reviewed technical publications resulted from the funded research.

 


Last Modified: 12/19/2022
Modified by: Joel L Sachs

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