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Award Abstract # 1459252
COLLABORATIVE RESEARCH: The role of iron-oxidizing bacteria in the sedimentary iron cycle: ecological, physiological and biogeochemical implications.

NSF Org: OCE
Division Of Ocean Sciences
Recipient: PRESIDENT AND FELLOWS OF HARVARD COLLEGE
Initial Amendment Date: February 18, 2015
Latest Amendment Date: February 18, 2015
Award Number: 1459252
Award Instrument: Standard Grant
Program Manager: Michael Sieracki
OCE
 Division Of Ocean Sciences
GEO
 Directorate for Geosciences
Start Date: March 1, 2015
End Date: February 28, 2019 (Estimated)
Total Intended Award Amount: $396,186.00
Total Awarded Amount to Date: $396,186.00
Funds Obligated to Date: FY 2015 = $396,186.00
History of Investigator:
  • Peter Girguis (Principal Investigator)
    pgirguis@oeb.harvard.edu
  • David Johnston (Co-Principal Investigator)
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
16 Divinity Avenue
Cambridge
MA  US  02138-2020
Primary Place of Performance
Congressional District:
05
Unique Entity Identifier (UEI): LN53LCFJFL45
Parent UEI:
NSF Program(s): Marine Geology and Geophysics,
BIOLOGICAL OCEANOGRAPHY
Primary Program Source: 01001516DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 1620, 8811, 9150, 1389, 9117, 1650
Program Element Code(s): 162000, 165000
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.050

ABSTRACT

Iron is one of the most abundant elements on Earth and is an essential element for life. Despite its abundance, iron is not always biologically available. For example, in the water column of the ocean, iron is easily oxidized and precipitates or sinks to the sediments. This can result in there being such a deficit of iron in the open ocean that it is often the primary limiting nutrient for the growth of phytoplankton that form the base of the marine food web. Marine sediments can be a major source of iron to the ocean, when it is made biologically available. Interestingly, one group of bacteria, the iron-oxidizing bacteria (FeOB), can use iron directly as an energy source to fuel their growth, and may govern the availability of iron to other parts of the ocean. While this group can be abundant at hydrothermal vents, little is known about their abundance or activity in marine sediments. Are these bacteria playing an important role in controlling the flux of iron from the sediments to the water column? To answer this, sediments on the east and west coasts of the United States will be analyzed to characterize and quantitate the diversity and abundance of FeOB. In addition, a series of laboratory experiments will be aimed at understanding the specific role they play in controlling iron flux from the sediments to the ocean, as well as the technically challenging question of determining the lower limit of oxygen at which they can grow. This work has relevance to our understanding of how biological control of a seemingly minor constituent in seawater, iron, could have implications for productivity of the entire ocean. Notably, a predicted impact of climate change on marine environments is to decrease oxygen levels in the ocean. This could have a profound influence on the sedimentary iron cycle, and possibly lead to greater inputs of iron, which could in turn alleviate iron-limitation in some regions of the ocean, thereby enhancing the rate of CO2-fixation and draw down of CO2 from the atmosphere. This project will provide training for a postdoctoral scientist, graduate students and undergraduates. Public outreach will include a student initiated exhibit, entitled "Iron and the evolution of life on Earth" at the Harvard Museum of Natural History providing a unique opportunity for undergraduate training and outreach.
The central hypothesis of this proposal is that FeOB are more common in marine sedimentary environments than previously recognized, and play a substantive role in governing the iron flux from the sediments into the water column by constraining the release of dissolved iron (dFe) from sediments. A survey of near shore regions in the Gulf of Maine, and a transect along the Monterey Canyon off the coast of California will obtain cores of sedimentary muds and look at the vertical distribution of FeOB and putative Fe-reducing bacteria using sensitive techniques to detect their presence and relative abundance. Sediments will be used in a novel reactor system that will allow for precise control of O2 levels and iron concentration to measure the dynamics of the iron cycle under different oxygen regimens. Pure cultures of FeOB with different O2 affinities will be tested in a bioreactor coupled to a highly sensitive mass spectrometer to determine the lower limits of O2 utilization for different FeOB growing on iron, thus providing mechanistic insight into their activity and distribution in low oxygen environments.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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LeBris, N., Yucel, M., Das, A., Sievert, S.M. and Girguis, P.R. "Hydrothermal energy transfer and organic carbon production at the deep seafloor." Frontiers in Marine Science , v.5 , 2018 10.3389/fmars.2018.00531
Antje Gittel, Johanna Donhauser, Hans Røy, Peter R. Girguis, Bo B. Jørgensen, Kasper U. Kjeldsen "Ubiquitous presence and novel diversityof anaerobic alkane degraders in coldmarine sediments" Frontiers in Microbiology , 2016 10.3389/fmicb.2015.01414
Aude Picard, Amy Gartman, and Girguis, P.R. "What Do We Really Know about the Role of Microorganisms in Iron Sulfide Mineral Formation?" Frontiers in Earth Science. , 2016 10.3389/feart.2016.00068
Aude Picard, Amy Gartman, and Peter R. Girguis "What Do We Really Know about the Role of Microorganisms in Iron Sulfide Mineral Formation?" Frontiers in Earth Science , 2016 10.3389/feart.2016.00068
Gittel, A., Donhauser, J., Røy, H., Girguis, P.R., Jørgensen, B.B. and Kjeldsen, K.U., "Ubiquitous presence and novel diversity of anaerobic alkane degraders in cold marine sediments." Frontiers in Microbiology , v.6 , 2015 , p.1414 10.3389/fmicb.2015.01414
Heather C. Olins, Daniel R. Rogers, Christina Preston, William Ussler III, Douglas Pargett, Scott Jensen, Brent Roman, James M. Birch, Christopher A. Scholin, M. Fauzi Haroon and Peter R. Girguis "Co-registered Geochemistry and Metatranscriptomics Reveal Unexpected Distributions of Microbial Activity within a Hydrothermal Vent Field" Frontiers in Microbiology , 2017 10.3389/fmicb.2017.01042
Heather C. Olins, Daniel R. Rogers, Christina Preston, William Ussler III, Douglas Pargett, Scott Jensen, Brent Roman, James M. Birch, Christopher A. Scholin, M. Fauzi Haroon and Peter R. Girguis. "Co-registered Geochemistry and Metatranscriptomics Reveal Unexpected Distributions of Microbial Activity within a Hydrothermal Vent Field" Frontiers in Microbiology. , 2017 10.3389/fmicb.2017.01042

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.

Iron is the fourth most abundant element in the crust. It has been a key element in humankind's evolution (we would not exist without iron, as it is necessary for many of our key enzymes) and civilization (iron was so important to us that we call it out by name as the Iron Age: when humans started fashioning tools out of Iron). 

Iron is equally critical to the rest of our biosphere. As in humans, Iron is important for the nearly all life on Earth. The oxygen in our atmosphere is made in large part by marine bacteria and alga, who depend on Iron to make the enzymes necessary for photosynthesis. Indeed, oxygen production on Earth is governed by the limited availability of Iron to these marine microorganisms, so it?s fair to say that Iron controls the amount of oxygen in our atmosphere.

Iron's relationship with oxygen is, however, a bit more complicated. Iron exists in two predominant forms on Earth: Iron(II), or "Iron two", and Iron(III), or "Iron three". Iron(II) was very common on early Earth, and remains common today in those parts of our world devoid of oxygen.  Deep sea hydrothermal vents, acidic hot springs, and even deep sea sediments and deep terrestrial soils all harbor Iron(II). Iron(III) is very common wherever oxygen is present, which nearly all of the surface and deep ocean, nearly every river and lake, and nearly all the surface soils on all the continents.  Notably, Iron(III) forms when Iron(II) encounters oxygen. More specifically, this fast and spontaneous reaction between Iron(II) and oxygen forms Iron(III) oxides, which are commonly known as "rust".  

Humans typically don't think highly of rust. We associate it with the decay of our bridges, cars, and other objects. Rust is also problematic for the many organisms that need Iron for their enzymes. Iron(III) is not readily accessible to most organisms, so they have evolved different mechanisms to acquire scarce Iron(II) from the environment, or to convert Iron(III) back into Iron(II) for the biosynthesis of new enzymes.

The situation, however, is most dire for those microbes that make a living on Iron(II). On early Earth, before there was lots of oxygen in our atmosphere, there was an abundance of Iron (II) that microbes could use as a "fuel" source. As the oxygen in Earth's atmosphere continued to rise, these so-called "iron oxidizing bacteria" had to find ways to use the Iron(II) before is spontaneously reacted with oxygen to form Iron (III).  

Today, we find these bacteria to be most abundant in areas where oxygen is sparse, such as the aforementioned vents, hot springs, and sediments. However, we also find them in areas where there is seemingly plenty of oxygen, and we do not yet know how they manage to "make a living". This project was aimed at understanding how iron-oxidizing bacteria (which we will call FeOB for short, as the letters "Fe" represent Iron on the periodic table of elements) compete with these spontaneous processes. We hypothesized that FeOB might somehow manage to control the oxygen in their environment, allowing them to better compete for Iron(II). We conducted a broad series of studies that revealed that they do, indeed, manage to influence the oxygen concentration around their Iron sources. They do this by forming a layer of polysaccharides, which is kind of like the mucus in the human nose. It covers the Iron(II) minerals and somehow keeps oxygen from accessing them. Also, FeOBs seems to use some tricks like changing the pH (activity) so that they can access Iron in ways that other organisms can't.

These studies were important for helping us understand how these organisms make a living on a well-oxygenated Earth. Equally important, these organisms do play a role in rusting away the many buildings, cars and other structures that we make out of Iron. This research might help our industry counterparts think broadly about how to minimize the role of these microbes in rusting away infrastructure.  Finally, this project gave us a chance to train many early career scientists in microbiology, statistics, public communication, engineering, and writing. Some of the students from this project are going on to pursue careers in industry, while others are considering medicine, environmental law, and academics.

 

 

 

 


Last Modified: 06/26/2019
Modified by: Peter Girguis

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