Award Abstract # 1831582
Dimensions: Collaborative Research: the role of microbial biodiversity in controlling nitrous oxide emissions from soils

NSF Org: DEB
Division Of Environmental Biology
Recipient: GEORGIA TECH RESEARCH CORP
Initial Amendment Date: July 31, 2018
Latest Amendment Date: July 31, 2018
Award Number: 1831582
Award Instrument: Standard Grant
Program Manager: Kendra McLauchlan
kmclauch@nsf.gov
 (703)292-2217
DEB
 Division Of Environmental Biology
BIO
 Directorate for Biological Sciences
Start Date: August 1, 2018
End Date: July 31, 2024 (Estimated)
Total Intended Award Amount: $698,234.00
Total Awarded Amount to Date: $698,234.00
Funds Obligated to Date: FY 2018 = $698,234.00
History of Investigator:
  • Konstantinos Konstantinidis (Principal Investigator)
    kostas@ce.gatech.edu
Recipient Sponsored Research Office: Georgia Tech Research Corporation
926 DALNEY ST NW
ATLANTA
GA  US  30318-6395
(404)894-4819
Sponsor Congressional District: 05
Primary Place of Performance: Georgia Institute of Technology
225 North Avenue, NW
Atlanta
GA  US  30332-0002
Primary Place of Performance
Congressional District:
05
Unique Entity Identifier (UEI): EMW9FC8J3HN4
Parent UEI: EMW9FC8J3HN4
NSF Program(s): Dimensions of Biodiversity
Primary Program Source: 01001819DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 7968, 9251
Program Element Code(s): 796800
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.074

ABSTRACT

Despite the vast amount of microbial biodiversity on Earth, the links among the number of microbial species, their genetic diversity, and ecosystem function remain poorly understood. Soils play an important role in sustaining human health. Therefore, it is particularly important to understand the function of the large number of bacterial species in the soil. To provide new insights into the relationship between microbial species and soil function, this project will focus on the reduction of a potent greenhouse gas called nitrous oxide. The reduction of nitrous oxide is a key function of soil microbes. This reduction step determines how much of this greenhouse gas is emitted to the atmosphere from the soil. The recent discovery of a new set of genes, organisms, and pathways that reduce nitrous oxide provides an opportunity to make progress on understanding this function. This project will train undergraduate students and graduate students, including individuals from under-represented groups from Puerto Rico. The training would include workshops, research opportunities, and a Research Experience for Undergraduates program at three institutions. The project also provides outreach opportunities to the general public through established K to Gray programs. Finally, the research from this study will provide society benefits in two ways. First, it will provide a mechanistic understanding of the controls on the production of an important greenhouse gas (nitrous oxide). Second, it will help understand an important loss pathway of nitrogen, the single most limiting nutrient on Earth.

This project will test the hypothesis that the amount of taxonomic and genetic diversity in the nitrous oxide reductase gene is necessary for specialization due to different substrate and environmental conditions in the soil. The ultimate goal is to predict both nitrous oxide reduction rates and nitrous oxide emissions from the genetic and phylogenetic diversity of soil microbes. The proposal will focus on two study sites- one in Illinois and one in Puerto Rico- and measure the abundances and activities of nitrous oxide-reducing taxa and genes in the soils. Simultaneous measurements of nitrous oxide emission rates in a variety of environmental conditions such as temperature, moisture, and nutrient levels, will allow the biotic and abiotic drivers of this reaction to be separated. The predicted rates of nitrous oxide consumption from a multivariate statistical analysis will be tested with independently measured rates by isotope-based methodology. This will allow assessment of the robust model of the microbial and environmental controls of the fate of nitrous oxide.

This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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(Showing: 1 - 10 of 23)
Bertagnolli, Anthony D. and Konstantinidis, Konstantinos T. and Stewart, Frank J. "Nondenitrifier nitrous oxide reductases dominate marine biomes" Environmental Microbiology Reports , v.12 , 2020 https://doi.org/10.1111/1758-2229.12879 Citation Details
Conrad, Roth E and Brink, Catherine E and Viver, Tomeu and Rodriguez-R, Luis M and Aldeguer-Riquelme, Borja and Hatt, Janet K and Venter, Stephanus N and Rossello-Mora, Ramon and Amann, Rudolf and Konstantinidis, Konstantinos T "Microbial species and intraspecies units exist and are maintained by ecological cohesiveness coupled to high homologous recombination" Nature Communications , v.15 , 2024 https://doi.org/10.1038/s41467-024-53787-0 Citation Details
Conrad, Roth_E and Viver, Tomeu and Gago, Juan_F and Hatt, Janet_K and Venter, Stephanus_N and Rossello-Mora, Ramon and Konstantinidis, Konstantinos_T "Toward quantifying the adaptive role of bacterial pangenomes during environmental perturbations" The ISME Journal , v.16 , 2021 https://doi.org/10.1038/s41396-021-01149-9 Citation Details
Durán-Viseras, Ana and Lindner, Blake G and Hatt, Janet K and Lai, Amanda and Wallace, Robert and Ginn, Olivia and Brown, Joe and Konstantinidis, Konstantinos T "Metagenomic insights into the impact of litter from poultry Concentrated Animal Feeding Operations (CAFOs) to adjacent soil and water microbial communities" Science of The Total Environment , v.920 , 2024 https://doi.org/10.1016/j.scitotenv.2024.170772 Citation Details
He, Guang and Chen, Gao and Xie, Yongchao and Swift, Cynthia M. and Ramirez, Diana and Cha, Gyuhyon and Konstantinidis, Konstantinos T. and Radosevich, Mark and Löffler, Frank E. "Sustained bacterial N2O reduction at acidic pH" Nature Communications , v.15 , 2024 https://doi.org/10.1038/s41467-024-48236-x Citation Details
Karthikeyan, Smruthi and Orellana, Luis H. and Johnston, Eric R. and Hatt, Janet K. and Löffler, Frank E. and Ayala-del-Río, Héctor L. and González, Grizelle and Konstantinidis, Konstantinos T. "Metagenomic Characterization of Soil Microbial Communities in the Luquillo Experimental Forest (Puerto Rico) and Implications for Nitrogen Cycling" Applied and Environmental Microbiology , v.87 , 2021 https://doi.org/10.1128/AEM.00546-21 Citation Details
Konstantinidis, Konstantinos T and Viver, Tomeu and Conrad, Roth E and Venter, Stephanus N and Rossello-Mora, Ramon "Solar salterns as model systems to study the units of bacterial diversity that matter for ecosystem functioning" Current Opinion in Biotechnology , v.73 , 2022 https://doi.org/10.1016/j.copbio.2021.07.028 Citation Details
Lindner, Blake G. and Suttner, Brittany and Zhu, Kevin J. and Conrad, Roth E. and Rodriguez-R, Luis M. and Hatt, Janet K. and Brown, Joe and Konstantinidis, Konstantinos T. "Toward shotgun metagenomic approaches for microbial source tracking sewage spills based on laboratory mesocosms" Water Research , v.210 , 2022 https://doi.org/10.1016/j.watres.2021.117993 Citation Details
Meziti, A. and Nikouli, E. and Hatt, J. K. and Konstantinidis, K. T. and Kormas, K. A. "Time series metagenomic sampling of the Thermopyles, Greece, geothermal springs reveals stable microbial communities dominated by novel sulfuroxidizing chemoautotrophs" Environmental Microbiology , 2020 https://doi.org/10.1111/1462-2920.15373 Citation Details
Orellana, Luis H. and Hatt, Janet K. and Iyer, Ramsunder and Chourey, Karuna and Hettich, Robert L. and Spain, Jim C. and Yang, Wendy H. and Chee-Sanford, Joanne C. and Sanford, Robert A. and Löffler, Frank E. and Konstantinidis, Konstantinos T. "Comparing DNA, RNA and protein levels for measuring microbial dynamics in soil microcosms amended with nitrogen fertilizer" Scientific Reports , v.9 , 2019 https://doi.org/10.1038/s41598-019-53679-0 Citation Details
Ramírez-Fernández, Lia and Orellana, Luis H. and Johnston, Eric R. and Konstantinidis, Konstantinos T. and Orlando, Julieta "Diversity of microbial communities and genes involved in nitrous oxide emissions in Antarctic soils impacted by marine animals as revealed by metagenomics and 100 metagenome-assembled genomes" Science of The Total Environment , v.788 , 2021 https://doi.org/10.1016/j.scitotenv.2021.147693 Citation Details
(Showing: 1 - 10 of 23)

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.

Natural microbial communities, especially soil microbiomes, are highly diverse and encompass hundreds, if not thousands, of distinct bacterial and archaeal species, each of which encodes a couple hundred species-specific genes together with distinct alleles of shared genes. The basis for this astonishing microbial biodiversity and its relevance for ecosystem function remain poorly understood. Predicting ecosystem function from the resident gene/genotype sequence diversity remains a particularly challenging issue for soil microbiology. Advancing this issue is a cornerstone for (more reliably) modeling ecosystem processes and the biochemical contributions of microbial species. To provide new insights into these topics, a key soil ecosystem process was studied: nitrous oxide (N2O) reduction to dinitrogen (N2). N2O emissions from both managed and natural lands contribute to climate change and stratospheric ozone destruction. A great diversity of bacterial species, each encoding distinct alleles of the N2O reductase gene (nosZ), are considered keystone populations controlling N2O reduction to environmentally benign N2. However, the biotic and abiotic controls over N2O reduction activity are poorly understood limiting management practices that would enhance soil N2O reduction as a greenhouse gas emission mitigation approach. 

Our work determined the abundance and taxonomic diversity of N2O-reducing bacterial species (phylogenetic diversity), as well as the activity of diverse nosZ gene alleles (genetic diversity) under different prevailing environmental conditions, in two key ecosystems, the Luquillo tropical forest in Puerto Rico and agricultural fields in Midwest US (Illinois). Our studies showed that low pH, in the Luquillo forest, selects for distinct (Sun et al., ISME Comms. 2024) and functional (He et al., Nature Comms. 2024) N2O-reducing microbiomes, and how environmental parameters, most notably low pH and N2O concentration, affect the rate of N2O-reduction. This discovery is particularly important because it was previously thought that microbial N2O-reduction is not possible at acidic pH. Further, we answered important, long-lasting questions about microbial diversity as part of this project such as what constitutes a species or a strain (Rodriguez-R et al., Nat. Comm. 2021), what mechanisms maintain the species- and intra-species units observed (Conrad et al., Nat. Comm. 2024), how many strains make up a natural population (Viver et al., Nat. Comm. 2024), what fraction of the species pangenome may be functionally important under fluctuating environmental conditions (Conrad et al., ISME 2021), and more [pangenome defined as all nonredundant genes carried by all strains of a species]. Briefly, these studies confirmed earlier observations by the PI that the immense microbial diversity is organized in discrete species-like clusters with the intra-species diversity encompassing genomes showing commonly, but not always, >95-96 genome-average nucleotide identity (ANI) whereas ANI between closely related species is <90%, revealing natural gap of values (genomes) between species at 85-95% ANI. As part of this project, we observed a similar ANI gap within species at 99.5% ANI, which can be used to define intra-species units such as genomovars and strains more reliably and robustly than the current practice. Rampant and unbiased (not selection-driven) homologous recombination across the genome, coupled to high ecological cohesiveness, appear to underlie these species and intra-species units (Conrad et al., Nat. Comm. 2024). However, only a small fraction of the immense gene and strain diversity within species (e.g., 2-3% of total) was found to be ecologically important when conditions changed in-situ; the rest appear to represent mostly ephemeral diversity (Conrad et al., ISME 2021). We anticipate that these studies will have a major impact on microbial sciences, as species and strains have been ill-defined to date, and ultimately impact modeling and tracking of microbial diversity. 

Finally, we built a great team of young researchers and students who were trained at demanding, cross-disciplinary areas of research. Our graduates have been highly successful in landing jobs in industry or academia; for instance, several of them are Assistant Professors currently at Institutions like the California Institute of Technology, the University of Puerto Rico, the University of Innsbruck, Austria and the Max Planck Institute, Germany. We delivered highly successful workshops (based on students’ exit interviews) in Puerto Rico (Adjuntas), Atlanta GA, and elsewhere in the world (e.g., EMBL in Germany, Microbiokosmos in Greece) for training graduate (Master’s) and undergraduate students in cutting-edge microbiome research. We provided these students with hands-on bioinformatics exercises with genomic and metagenomic data from this project, and discussed career opportunities in the microbiome field. Therefore, our work has provided new insights into the organization of microbial diversity on the planet and advanced understanding of N2O emissions, a potent greenhouse gas and a pollutant of the atmosphere. Our work has also contributed significantly toward building the future workforce. 

 


Last Modified: 11/16/2024
Modified by: Konstantinos T Konstantinidis

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