Award Abstract # 1749544
CAREER: The consequences of rarity for soil microbiome stability in structure and function

NSF Org: DEB
Division Of Environmental Biology
Recipient: MICHIGAN STATE UNIVERSITY
Initial Amendment Date: May 31, 2018
Latest Amendment Date: January 9, 2024
Award Number: 1749544
Award Instrument: Continuing Grant
Program Manager: Steven Dudgeon
sdudgeon@nsf.gov
 (703)292-2279
DEB
 Division Of Environmental Biology
BIO
 Directorate for Biological Sciences
Start Date: July 1, 2018
End Date: December 31, 2024 (Estimated)
Total Intended Award Amount: $800,000.00
Total Awarded Amount to Date: $832,271.00
Funds Obligated to Date: FY 2018 = $177,537.00
FY 2019 = $622,463.00

FY 2020 = $32,271.00
History of Investigator:
  • Ashley Shade (Principal Investigator)
    shade.ashley@gmail.com
Recipient Sponsored Research Office: Michigan State University
426 AUDITORIUM RD RM 2
EAST LANSING
MI  US  48824-2600
(517)355-5040
Sponsor Congressional District: 07
Primary Place of Performance: Michigan State University
East Lansing
MI  US  48824-1000
Primary Place of Performance
Congressional District:
07
Unique Entity Identifier (UEI): R28EKN92ZTZ9
Parent UEI: VJKZC4D1JN36
NSF Program(s): Ecosystem Science,
Population & Community Ecology,
ECOSYSTEM STUDIES
Primary Program Source: 01002122DB NSF RESEARCH & RELATED ACTIVIT
01001819DB NSF RESEARCH & RELATED ACTIVIT

01002223DB NSF RESEARCH & RELATED ACTIVIT

01001920DB NSF RESEARCH & RELATED ACTIVIT

01002021DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 1182, 1045, 019Z, 1181
Program Element Code(s): 738100, 112800, 118100
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.074

ABSTRACT

Microorganisms are the smallest life forms and yet they have large and critical roles in maintaining the health of ecosystems. Environmental microbial communities provide essential functions, including the cycling of key resources like carbon and nitrogen. In soils, microorganisms form diverse communities with thousands of distinct species, but the role of most of these species is unknown. In particular, it is not clear how microbial species that are not very abundant (rare) contribute to community functions. However, rare microorganisms are thought to be important when environmental conditions fluctuate because they provide functions that help their ecosystem resist change or to recover quickly. This project will investigate the diversity and functions of rare microorganisms in a soil ecosystem impacted by a long-term disturbance, and determine how they contribute to the system's resilience to this disturbance. The research will provide insights into the critical role of microbial diversity for environmental resilience, which has implications for broad national interests in energy and food security, environmental conservation and remediation, and the management of ecosystem services. The project will advance the fields of ecology and ecosystem science by investigating the links between microbial diversity and functions in the environment. It also will benefit society by providing classroom education in quantitative methods and training members of the scientific workforce in leading-edge technologies used in biology and chemistry.

The three aims of this research are to: 1) quantify the contributions of rare microbial taxa to community stability after a long-term environmental disturbance; 2) evaluate the abilities of rare microbial taxa to a) persist given disturbance and b) respond to specific environmental changes that result from the disturbance; and 3) determine the impact of competition between rare and abundant microbial taxa on community stability and functions. The Centralia, Pennsylvania soil ecosystem is the site of a long-burning coal seam fire that will serve a model severe disturbance for this work. For Aims 1 and 2, surface soils will be collected annually from established sites along a fire-impact gradient so that community changes over time due to the influence of fire can be quantified. Soil microbial communities will be assessed using genetic markers of phylogenetic and functional diversity obtained from untargeted DNA and RNA sequencing. Rare microbial taxa will be identified using bioinformatics and their contributions to community stability will be quantified with ecological statistics. For Aim 3, bacteria isolated from field soils will be arrayed into synthetic microbial communities to assess outcomes of competition between rare and abundant microorganisms. Microbial community "goods", which include small, excreted molecules like enzymes and antibiotics, will be measured using sensitive mass spectrometry to determine how competition impacts their production. Together, these efforts will provide insights into the ecological roles of rare microbial taxa, and microbial biodiversity more broadly, for community stability and function.

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)
Guittar, John and Koffel, Thomas and Shade, Ashley and Klausmeier, Christopher A and Litchman, Elena "Resource competition and host feedbacks underlie regime shifts in gut microbiota" The American Naturalist , 2021 https://doi.org/10.1086/714527 Citation Details
Vandepol, Natalie S and Shade, Ashley "Is everything everywhere? A hands-on activity to engage undergraduates with key concepts in quantitative microbial biogeography" Journal of Microbiology & Biology Education , 2024 https://doi.org/10.1128/jmbe.00170-23 Citation Details
Tobin, Tammy C and Shade, Ashley "A town on fire! Integrating 16S rRNA gene amplicon analyses into an undergraduate microbiology lecture class" FEMS Microbiology Letters , v.365 , 2018 10.1093/femsle/fny104 Citation Details
Stehling, Eliana Guedes and Furlan, João_Pedro Rueda and Lopes, Ralf and Chodkowski, John and Stopnisek, Nejc and Savazzi, Eduardo Angelino and Shade, Ashley "The relationship between water quality and the microbial virulome and resistome in urban streams in Brazil" Environmental Pollution , v.348 , 2024 https://doi.org/10.1016/j.envpol.2024.123849 Citation Details
Sorensen, Jackson W. and Shade, Ashley "Dormancy dynamics and dispersal contribute to soil microbiome resilience" Philosophical Transactions of the Royal Society B: Biological Sciences , v.375 , 2020 10.1098/rstb.2019.0255 Citation Details
Sorensen, Jackson W. and Dunivin, Taylor K. and Tobin, Tammy C. and Shade, Ashley "Ecological selection for small microbial genomes along a temperate-to-thermal soil gradient" Nature Microbiology , v.4 , 2019 10.1038/s41564-018-0276-6 Citation Details
Shade, Ashley K. and Dunivin, Taylor K. and Choi, Jinlyung C. and Teal, Tracy S. and Howe, Adina and Greene, Casey "Strategies for Building Computing Skills To Support Microbiome Analysis: a Five-Year Perspective from the EDAMAME Workshop" mSystems , v.4 , 2019 10.1128/mSystems.00297-19 Citation Details
Shade, Ashley and Dunn, Robert R. and Blowes, Shane A. and Keil, Petr and Bohannan, Brendan J.M. and Herrmann, Martina and Küsel, Kirsten and Lennon, Jay T. and Sanders, Nathan J. and Storch, David and Chase, Jonathan "Macroecology to Unite All Life, Large and Small" Trends in Ecology & Evolution , v.33 , 2018 10.1016/j.tree.2018.08.005 Citation Details
Shade, Ashley "Microbiome rescue: directing resilience of environmental microbial communities" Current Opinion in Microbiology , v.72 , 2023 https://doi.org/10.1016/j.mib.2022.102263 Citation Details
Kearns, Patrick J. and Shade, Ashley "Trait-based patterns of microbial dynamics in dormancy potential and heterotrophic strategy: case studies of resource-based and post-press succession" The ISME Journal , v.12 , 2018 10.1038/s41396-018-0194-x Citation Details
Jurburg, Stephanie D and Blowes, Shane A and Shade, Ashley and Eisenhauer, Nico and Chase, Jonathan M "Synthesis of recovery patterns in microbial communities across environments" Microbiome , v.12 , 2024 https://doi.org/10.1186/s40168-024-01802-3 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.

Overview
Soils contain tens of thousands of different microbial populations, and these microbes provide critical functions to ecosystems, including supporting plant health, making nutrients available, and modulating the exchange of gases with the atmosphere. Thus, these communities are front-line players in determining how ecosystems respond to stress. It is of societal importance to understand how soil microbial communities respond to stress so that we can manage them to be resilient and stable in the critical functions they provide. To better understand soil microbial responses to a large and unnatural stress, this award leveraged the ongoing underground coal seam fire in Centralia, Pennsylvania, USA, that ignited accidentally in 1962. The Centralia heat gradient enabled a long-term investigation of soil microbial community responses to and recovery from stress.


Intellectual Merit
This award advanced the understanding of how complex microbial communities respond to and recover from environmental stress. Soil microbial communities shifted starkly in their compositions in response to the heat and recovered gradually as the soils cooled. The communities in heated soils had traits and likely functions adapted to the stress, including relatively smaller genomes and specialized metabolisms. Together, experimental and field results showed that bacterial populations sensitive to the heat later re-established in the soil by dispersal or by persisting in an inactive state, likely to gain protection during the stress. Experimental results showed that interactions among different bacterial populations can also influence how a community responds to stress: a population’s functions can change depending on which other populations were present and whether their interactions were positive or negative. In addition, this award supported the targeted investigation of how several microbial genes responded to heat stress, including arsenic and antibiotic resistance genes, which encode functions relevant to human and animal health and can be exchanged among different microbial populations. Generally, these genes changed with stress intensity, which was attributed to concordant changes in the microbial populations present rather than gene exchange.  


This award has broadly advanced ecological understanding of the consequences of microbial biodiversity for community stress response and ecosystem functions. It has highlighted the importance and consequences of microbial inactivation and re-activation to support community transitions during stress and their eventual resilience towards a recovered state. It has also advanced the understanding of how reservoirs of inactive microbial biodiversity can accumulate during and after a disturbance, with consequences for a community’s recovery potential. These specific findings have provoked new directions of research.


This work resulted in 23 peer-reviewed scientific papers, three doctoral dissertations, and over a thousand publicly available data products actively used by scientists (e.g., for gene and pathway mining), including DNA sequences, metabolite profiles, code for computational data analysis, and a public reference database of soil bacterial genomes linked to plasmids. Significant results were communicated via 21 posters and talks at approximately 19 scientific conferences and 18 invited university or institutional seminars. The media covered the award’s research results at least six times.  

Broader Impacts
This award benefited society by advancing understanding of the mechanisms that support resilient soil microbial communities, with broad relevance for understanding how to predict and manage soil health in natural and agricultural ecosystems. It further advanced societal goals of open and reproducible science by making data and educational products publicly available. The scientific community is using the rich sequencing data generated as part of this award to discover microbial pathways that may be useful for developing new products or drugs.  


It also produced several educational products established at Michigan State University and MSU’s Kellogg Biological Station. These efforts included a five-year, annually-delivered training workshop on big data analysis and computing that reached 132 domestic and international learners. It also produced publicly available learning materials for the microbiology and ecology undergraduate classroom, including team-based active learning exercises, video lectures, and specific learning objectives aligned to content and assessments.


The award supported the scientific workforce training of three Ph.D. students, one MSc. student, four post-doctoral scholars, three teaching fellows, one technician, over 30 undergraduate researchers, and two visiting international scholars. These project personnel developed quantitative skills in data analysis, computing, ecology, microbiology, molecular biology, soil science, experimental design, and responsible conduct of research, including societal values of open and reproducible science. All graduate students contributing to this award’s work are currently employed in science-relevant public or private sector positions. It supported a Ph.D. internship in the private sector with a start-up company and allowed the PI to engage in science communication training at Michigan State.   


Last Modified: 02/19/2025
Modified by: Ashley L Shade

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