Award Abstract # 1459600
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: BIGELOW LABORATORY FOR OCEAN SCIENCES
Initial Amendment Date: February 18, 2015
Latest Amendment Date: February 18, 2015
Award Number: 1459600
Award Instrument: Standard Grant
Program Manager: David Garrison
OCE
 Division Of Ocean Sciences
GEO
 Directorate For Geosciences
Start Date: March 1, 2015
End Date: February 28, 2018 (Estimated)
Total Intended Award Amount: $522,499.00
Total Awarded Amount to Date: $522,499.00
Funds Obligated to Date: FY 2015 = $522,499.00
History of Investigator:
  • David Emerson (Principal Investigator)
    demerson@bigelow.org
Recipient Sponsored Research Office: Bigelow Laboratory for Ocean Sciences
60 BIGELOW DR
EAST BOOTHBAY
ME  US  04544-5700
(207)315-2567
Sponsor Congressional District: 01
Primary Place of Performance: Bigelow Laboratory for Ocean Sciences
60 Bigelow Drive
East Boothbay
ME  US  04544-0380
Primary Place of Performance
Congressional District:
01
Unique Entity Identifier (UEI): DRTAEZWWJHM8
Parent UEI:
NSF Program(s): Marine Geology and Geophysics,
BIOLOGICAL OCEANOGRAPHY
Primary Program Source: 01001516DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 1389, 1620, 1650, 8811, 9117, 9150
Program Element Code(s): 1620, 1650
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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Emerson, D. "The irony of iron ? biogenic iron oxides as an iron source to the ocean." Frontiers in Microbiology , v.6 , 2016 , p.1518 10.3389/fmicb.2015.01518
David Emerson, Jarrod J. Scott, Anna Leavitt, Emily Fleming, Craig Moyer "In situ estimates of iron-oxidation and accretion rates for iron-oxidizing bacterial mats at L??ihi Seamount." Deep-Sea Research , v.126 , 2017 , p.31 http://dx.doi.org/10.1016/j.dsr.2017.05.011
J.P. Beam, J.J. Scott, S.M. McAllister, C.S. Chan, J. McManus, F.J.R. Meysman, D. Emerson. "Potential for biological rejuvenation of iron oxides in bioturbated marine sediments." ISME J , 2018 https://doi.org/10.1038/s41396-017-0032-6.
Beam, J.P., J.J. Scott, S.M. McAllister, C.S. Chan, J. McManus, F.J.R. Meysman, and D. Emerson. ". A biological source of marine sedimentary iron oxides." bioRxiv , 2017 https://doi.org/10.1101/108621.

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. Iron is a critical element for life that serves as an essential trace element for eukaryotic organisms, while it is common in sediments it is a key limiting nutrient in the upper water column in a third of the global ocean. Understanding biological controls on the iron cycle is thus important to understanding the mechanism behind this nutrient limitation, as well as understanding important sediment biogeochemistry.  Conventional wisdom holds that most of the iron oxidation in sediments is abiological, as a result of the rapid kinetics of chemical iron oxidation in the presence of oxygen.  The central premise of this work was that conventional wisdom is incorrect, iron oxidation is primarily biological, and that microbes play an essential role in iron oxidation, thereby influencing the marine iron-cycle and iron availability to the ocean. Iron-oxidizing microbes are able to support all their growth requirements by extracting energy from the oxidation of iron and fixing carbon dioxide. Our previous work has shown they are important at hydrothermal vents in the ocean, but little was known about their distribution or abundance in sediments. We carried out surveys of marine sediments for the presence of the Zetaproteobacteria a well-known group of iron-oxidizers, followed a seasonal cycle in an intertidal sediment, and conducted laboratory mesocosm experiments to understand the role of hypoxia or low oxygen conditions on iron-cycling in sediments.

 

Intellectual Merit. An initial significant finding was that visible iron oxidation in marine sediments was almost exclusively associated with bioturbating macrofauna, principally polychaete worms in the sampling sties we examined. In bulk sediments with bioturbation, the abundance of Zetaproteobacteria ranged from below detection to around 1% of the population in bulk sediment, whereas in worm burrow walls in these sediments abundances ranged from 0.1% - 15% indicating the partitoning of iron-oxidizers to worm burrow walls. From our own work and analyzing global metagenome data for marine sediments, we estimated Zetaproteobacteria represent an average of 1.05 x 1026 cells (3.83 x1024-1.44 x 1027) in the upper 10 cm of continental shelf sediments, and annual sedimentary biological oxidation of iron—forming iron oxides—could exceed the annual flux of iron oxides from rivers to coastal sediments by up to a factor of ten, primarily due to iron recycling. Following on this work we conducted a seasonal study linking iron geochemistry and microbial population dynamics along with presence of marine worms.  Both dissolved and solid phase iron pools correlated positively with temperature over the season—increases in the sediment temperature resulted in increases in both iron pools. We attribute these increases to the enhanced activity of bioturbating macrofauna in this mudflat, with increased respiration and burrow irrigation at elevated temperature. Building on the above field studies, we conducted controlled laboratory mesocosm experiments to test the effect of declining oxygen—hypoxia—on the iron biogeochemical cycle in bioturbated coastal sediments. In all cases there were dramatic differences in mesocosms with Nereus diversicolor a common marine worm, and those without. Mesocosms with worms present had a significantly greater flux of iron to the water column and different microbial communities, except under very hypoxic conditions where the worms did not survive. In addition to these environmental studies we have also sequenced the genomes of three new isolates of Fe-oxidizing Zetaproteobacteria from marine sediments.  Each isolate belongs to a novel clade, including those that we see as most representative of those present in coastal sediments. One of these strains has a number of significant differences in it's electron transport chain for growing on iron, indicating it has a unique physiology, likely adapted for it's sedimentary habitat.

 Broader Impacts. Our results systematically show, for the first time, the presence of iron-oxidizing bacteria, principally the Zetaproteobacteria, in coastal marine sediments, and provide estimates for their global importance in an active iron cycle. They also demonstrate the direct association of iron-oxidizing communities with bioturbating macrofauna. Direct linkages between bioturbating animals and microbial populations that result in important functional activities is a poorly understood phenomena in benthic microbial ecology. This work has also quantitated the effects of hypoxia on iron release from the sediments using manipulative laboratory experiments. An important impact of climate change on marine environments is a predicted increase in low O2 or hypoxic zones in the ocean. These experiments will help in predictions of how those conditions may impact the marine iron cycle, which in turn impacts productivity in the ocean. The project resulted in training for a postdoctoral scientist, ongoing collaborations with faculty, and Ph.D students at Harvard University a collaborating institution on the project, and training for 4 undergraduate students. There have been 13 publications and presentations at national or international meeting supported by the project, several more publications are in preparation. Data from the project has been distributed to the sequence read archive at Genbank, the Integrated Microbial Genome database, and BCO-DMO (https://www.bco-dmo.org/project/544584).

 


Last Modified: 06/01/2018
Modified by: David Emerson

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