Award Abstract # 1542506
DIMENSIONS: COLLABORATIVE RESEARCH: The phylogenetic and functional diversity of extracellular electron transfer across all three domains of life

NSF Org: DEB
Division Of Environmental Biology
Recipient: PRESIDENT AND FELLOWS OF HARVARD COLLEGE
Initial Amendment Date: August 10, 2015
Latest Amendment Date: January 22, 2016
Award Number: 1542506
Award Instrument: Standard Grant
Program Manager: Matthew Kane
mkane@nsf.gov
 (703)292-7186
DEB
 Division Of Environmental Biology
BIO
 Directorate for Biological Sciences
Start Date: January 1, 2016
End Date: December 31, 2020 (Estimated)
Total Intended Award Amount: $599,959.00
Total Awarded Amount to Date: $601,353.00
Funds Obligated to Date: FY 2015 = $599,959.00
FY 2016 = $1,394.00
History of Investigator:
  • Peter Girguis (Principal Investigator)
    pgirguis@oeb.harvard.edu
Recipient Sponsored Research Office: Harvard University
1033 MASSACHUSETTS AVE STE 3
CAMBRIDGE
MA  US  02138-5366
(617)495-5501
Sponsor Congressional District: 05
Primary Place of Performance: Harvard University
26 Oxford street
Cambridge
MA  US  02138-2020
Primary Place of Performance
Congressional District:
05
Unique Entity Identifier (UEI): LN53LCFJFL45
Parent UEI:
NSF Program(s): Dimensions of Biodiversity
Primary Program Source: 01001516DB NSF RESEARCH & RELATED ACTIVIT
01001617DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 7968, 9169, EGCH
Program Element Code(s): 796800
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.074

ABSTRACT

All cells require energy. This fact is somewhat taken for granted in biodiversity studies of plants and animals, but is at the forefront of discovering novel microbial biodiversity. As an electrical charge flows through energy transfer molecules in a cell, it is coupled to the production of ATP molecules (akin to charging the battery that powers the cell) or the production of other compounds that are critical for life function. Until recently, it was thought that all cells require electron energy transfer molecules that are soluble in water, so that they can be brought into the cell. However, scientists discovered that some bacteria are able to use solid metals such as rust (iron oxides) located outside the cell as an energy source. They do so by shuttling electrons from the inside of the cell to the outside of the cell, via energy transfer molecules that deliver electrical charge to metal deposits in the environment. In other words, part of these microbes' energy production pathways have evolved to be outside of the cell. This process, termed extracellular electron transfer (EET), transformed how we think about cellular life and in particular how microbes may impact the global elemental cycles that sustain life on Earth. This research team will conduct the first wide-ranging assessment of the diversity of EET across all three domains of life (Bacteria, Archaea and Eukarya). The project will also broaden public understanding about microbial life through developing interactive museum exhibits that present microbial EET to the public. Project investigators will work with the Encyclopedia of Life to broaden the representation of microbes in their databases and in school curricula. The project is also uniquely poised to strengthen industry and academic pipelines through educational curriculum that engages middle school students in interdisciplinary EET research, and a pedagogical training and lab exchange program that affords students and postdoctoral scholars an opportunity to conduct interdisciplinary research.

Consistent with the objectives of the DIMENSIONS program, this proposal aims to establish the degree to which ribotypes and genotypes relate to function and activity. This is also a grand challenge in environmental microbiology, and our ability to use bioelectrochemical systems to selectively target electroactive communities affords a unique opportunity to selectively isolate and characterize microbes capable of extracellular electron transfer (EET). To these ends, the overarching goal of this proposal is to comprehensively assess and relate the phylogenetic diversity, genetic/genomic diversity, and functional diversity of microorganisms engaged in EET across all three domains of life. The work plan includes: 1) conducting the first broad, systematic assessment of the phylogenetic diversity of EET-enabled microbes in natural habitats; 2) using the results of these data to identify 20 "representative" communities for co-registered metagenomic, metatranscriptomic, and biogeochemical characterization to target differentially expressed transcripts associated with EET and the biogeochemical processes that are mediated by these communities; 3) characterizing the genetic, biochemical and biophysical attributes of cultivated but uncharacterized microbes commonly found on electroactive surfaces; 4) integrating these results to develop a better capacity to predict the physiologies and biogeochemical impacts of electroactive communities in nature; and 5) archiving these data in robust databases to allow others to relate the project's findings to their data. These efforts will provide, for the first time, a comprehensive dataset linking phylogenetic data (16S, 18S) with functional potential (genomics), physiological poise (transcriptomics) and metabolic activity (geochemical measurements) that will have many applications to beyond biodiversity science. For example, the combined 'omics and rate measurements will allow the investigators to constrain the extent to which EET contributes to biogeochemical cycles in nature. The transposon mutagenesis and biophysical studies, in turn, will help researchers understand the means by which common but poorly characterized microbes carry out EET. While the value of each of the proposed efforts is significant, the coordination of these activities enables true integration of these findings to provide a comprehensive perspective on the relationships among phylogenetic, genomic and physiological diversity.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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(Showing: 1 - 10 of 11)
Aude Picard, Amy Gartman, David Clarke, and Peter R. Girguis "Sulfate-reducing bacteria act as organic templates for the formation of iron sulfide minerals with unique characteristics" Geochimica et Cosmochimica Acta , 2017 doi.org/10.1016/j.gca.2017.10.006
Beam, J.P., George, S., Record, N.R., Countway, P.D., Johnston, D.T., Girguis, P.R. and Emerson, D. "Mud, microbes, and macrofauna: seasonal dynamics of the iron biogeochemical cycle in an intertidal mudflat." bioRxiv , 2020 10.1101/2020.05.18.100800
Gartman, A., Picard, A., Olins, H.C., Sarode, N., Clarke, D.R. and Girguis, P.R. "Microbes facilitate mineral deposition in bioelectrochemical systems." ACS Earth and Space Chemistry , 2017 doi: 10.1021/acsearthspacechem.7b00042
Leprich, D.J., Flood, B.E., Schroedl, P.R., Ricci, E., Marlow, J.J., Girguis, P.R., and Bailey, J.V. "Sulfur bacteria promote dissolution of authigenic carbonates at marine methane seeps" The ISME Journal , 2021 10.1038/s41396- 021-00903-3.
Marlow, Jeffrey J and Kumar, Amit and Enalls, Brandon C and Reynard, Linda M and Tuross, Noreen and Stephanopoulos, Gregory and Girguis, Peter "Harnessing a methane-fueled, sediment-free mixed microbial community for utilization of distributed sources of natural gas" Biotechnology and bioengineering , v.115 , 2018 , p.1450--146 10.1002/bit.26576
Nadine, Le Bris and Yucel, Mustafa and Das, Anindita and Sievert, Stefan M and Girguis, Peter R and others "Hydrothermal energy transfer and organic carbon production at the deep seafloor" Frontiers in Marine Science , v.5 , 2018 , p.531 10.3389/fmars.2018.00531
Park, J.O., Liu, N., Holinski, K.M., Emerson, D.F., Qiao, K., Woolston, B.M., Xu, J., Lazar, Z., Islam, M.A., Vidoudez, C. and Girguis, P.R. "Synergistic substrate cofeeding stimulates reductive metabolism." Nature Metabolism , v.1 , 2019 , p.643 10.1038/s42255-019-0077-0
Picard, A., Gartman, A. and Girguis, P.R. "Interactions Between Iron Sulfide Minerals and Organic Carbon: Implications for Biosignature Preservation and Detection." Astrobiology , 2021 10.1089/ast.2020.2276
Picard, A., Gartman, A., Cosmidis, J., Obst, M., Vidoudez, C., Clarke, D.R. and Girguis, P.R. "Authigenic metastable iron sulfide minerals preserve microbial organic carbon in anoxic environments." Chemical Geology. , v.530 , 2020 , p.119343 10.1016/j.chemgeo.2019.119343
Rowe, Annette R and Xu, Shuai and Gardel, Emily and Bose, Arpita and Girguis, Peter and Amend, Jan P and El-Naggar, Mohamed Y "Methane-linked mechanisms of electron uptake from cathodes by Methanosarcina barkeri" mBio , v.10 , 2019 , p.e02448--1 10.1128/mBio.02448-18
Walter, Sunita R Shah and Jaekel, Ulrike and Osterholz, Helena and Fisher, Andrew T and Huber, Julie A and Pearson, Ann and Dittmar, Thorsten and Girguis, Peter R "Microbial decomposition of marine dissolved organic matter in cool oceanic crust" Nature Geoscience , v.11 , 2018 , p.334 10.1038/s41561-018-0109-5
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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.

All known life is electrical life. All living organisms use the movement of electrons within each cell to generate energy, build new biomolecules, and send signals.

Typically, for energy generation, organisms will take electrons away from electron-rich compounds (such as sugars, as we humans do) and pass them through their biochemical apparatus to electron-poor compounds (such as oxygen).  The movement of electrons through these pathways drives the re-generation of ATP (our energy currency) as well as the synthesis of biological "building bocks" to make new biomolecules (these are called reducing equivalents, and NAPH is an example of a reducing equivalent). Until recently, it was thought that all cells ?from single-cell microbes to the largest plants and animals- require these compounds to be brought into the cell.  However, about 30 years ago scientists discovered that some bacteria are able to use solid compounds such as rust (iron oxides) located outside the cell as the electron acceptor. They do so by shuttling electrons from the inside of the cell to the outside of the cell, via biomolecules that deliver electrical charge to the solid compounds in the environment. In other words, these microbes "breathe" rust, and part of these microbes? energy production pathways evolved to be outside of the cell.

This process, termed extracellular electron transfer (EET), transformed how we think about cellular life and in particular how microbes may impact global biogeochemical cycles that keep our biosphere healthy. As one example, EET enables microbes to chemically alter minerals, including toxic elements such as Uranium, for energy generation without bringing those substances into the cell. This has profound implications for the mobility of such toxins in both natural and human-built ecosystems. To date, however, we have studied the biochemistry, physiology and ecology of EET in just a few cultured microbes in natural and human-made habitats. By applying a multi-faceted and interdisciplinary approach, our team will conduct the first wide-ranging assessment of the diversity of EET across all three domains of life. Specifically, the overarching goal of this proposal is to comprehensively assess and relate the phylogenetic diversity, genetic/genomic diversity, and functional diversity of microorganisms engaged in EET across all three domains of life. By virtue of our experimental design and project plan, this project will provide, for the first time, experiments that linking microbial identity (phylogenetic analyses) with their genomic capacity (metagenomics) and their metabolic/EET rates (transcriptomics, genetics, and metabolic rate measurements). While the value of each of the proposed efforts is significant, the coordination of these activities enables true integration of these findings and will yield the first comprehensive knowledge base for EET that can be used to identify new organisms that are capable of EET across all domains of life. Equally important, this research has caught the attention of companies across a diversity of sectors. Companies engaged in biofuel generation, soil remediation, wastewater treatment, and synthetic biology have used our research as a basis for further research, and potenitally to advance their product lines.

In addition to the technical objectives, this project promoted the progress of science and support education and diversity. We broadened public understanding about microbial life through developing interactive museum exhibits that presents microbial EET to the public. We contributed to the Encyclopedia of Life to broaden the representation of microbes in their databases and school curricula. We developed a cross-university STEM program that uses "microbial fuel cells" to teach students about physics, chemistry, and biology through EET experiments. Further, our project strengthened industry and academic pipelines through educational curricula that engaged middle school and college-level students in EET research, and a pedagogical training and lab exchange program that afforded our students and postdocs an opportunity to conduct interdisciplinary research. 


Last Modified: 05/15/2021
Modified by: Peter Girguis

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