| NSF Org: |
IOS Division Of Integrative Organismal Systems |
| Recipient: |
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| Initial Amendment Date: | May 28, 2013 |
| Latest Amendment Date: | May 28, 2013 |
| Award Number: | 1257532 |
| Award Instrument: | Standard Grant |
| Program Manager: |
Irwin Forseth
IOS Division Of Integrative Organismal Systems BIO Directorate for Biological Sciences |
| Start Date: | June 1, 2013 |
| End Date: | May 31, 2018 (Estimated) |
| Total Intended Award Amount: | $320,001.00 |
| Total Awarded Amount to Date: | $320,001.00 |
| Funds Obligated to Date: |
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| History of Investigator: |
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| Recipient Sponsored Research Office: |
4202 E FOWLER AVE TAMPA FL US 33620-5800 (813)974-2897 |
| Sponsor Congressional District: |
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| Primary Place of Performance: |
4202 East Fowler Avenue Tampa FL US 33620-5200 |
| Primary Place of
Performance Congressional District: |
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| Unique Entity Identifier (UEI): |
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| Parent UEI: |
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| NSF Program(s): | Integrtv Ecological Physiology |
| Primary Program Source: |
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| Program Reference Code(s): |
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| Program Element Code(s): |
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| Award Agency Code: | 4900 |
| Fund Agency Code: | 4900 |
| Assistance Listing Number(s): | 47.074 |
ABSTRACT
All life on Earth depends upon the fixation of carbon dioxide to organic carbon by organisms that power this process with light energy or high-energy chemicals. There are four known pathways that catalyze carbon fixation. Based on phylogenetic distributions and functional attributes, it has been posited that the Calvin Benson Bassham cycle, found in plants, algae, and some bacteria, dominates in aerobic terrestrial and marine aerobic habitats due to its resilience to oxygen, while other 'oxygen sensitive' carbon fixation pathways are relegated to hypoxic or anoxic environs like vents and hot springs.
Contrary to this supposition, there are symbioses found in hypoxic diffuse flows around hydrothermal vents in which the bacterial partner uses the Calvin Benson Bassham cycle. Tubeworm-bacterial symbioses, in particular Riftia pachyptila ("Riftia"), are the dominant keystone species at hydrothermal vents in the Pacific Ocean. These symbiotic systems fix carbon at mass specific rates comparable to the fastest growing plants. Surprisingly, recent studies suggest that the bacterial symbionts use two carbon fixation pathways, the Calvin Benson Bassham cycle and the reductive tricarboxylic acid cycle. The use of these two pathways by a single organism (the bacterium) to fix carbon is unprecedented, and may be a strategy to cope with the high variability in environmental conditions encountered by hydrothermal vent organisms.
For the work proposed here, Riftia will be incubated in high-pressure aquaria under conditions that mimic the environmental variations found in situ. Biochemical assays on the bacteria and tubeworm host will be used to ascertain the relationship between environmental conditions, metabolic activity and differential use of the two pathways, to understand how they act in concert to sustain carbon fixation in a dynamic environment. These data will considerably further the understanding of the influence of environment on carbon fixation by bacteria as well as plants, and will also be helpful for determining why different organisms have the different carbon fixing pathways.
We are equally committed to the proposed scientific research and our proposed education and outreach. We plan to support three major programs: (1) graduate student development (2) undergraduate mentoring, and (3) the design of high-impact educational curricula using real research data and experiences. This study will enable the support and training of undergraduate and graduate students who will be intimately involved in designing and engineering the experiments, analyzing the data, and formally presenting and documenting the work. The proposed research contains significant field and laboratory components, which affords students and teachers the opportunities to participate in this project at a variety of levels.
PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH
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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.
Deep sea hydrothermal vent tubeworm Riftia pachyptila dominates vents in Eastern Pacific Ocean. This organism has been the focus of physiological study since its discovery in 1981. What is clear from previous studies is that this organism, which lacks a mouth, gut or anus, relies entirely on endosymbiotic bacteria for nutrition. This is remarkable, given the large size (1 meter long, 2 cm diameter) and rapid growth rates (1 kg/yr). The symbionts are housed in the trophosome organ, and power carbon dioxide fixation by oxidizing poisonous hydrogen sulfide gas. Carbon dioxide, hydrogen sulfide, and oxygen are delivered from the hydrothermal vent environment to the symbionts in the trophosome by a well-developed circulatory system. Previous study has indicated that the host is fed by the symbionts both by 'milking' them for small organic compounds, and also by digesting some of them.
Early studies indicated that the endosymbiotic bacterial used the Calvin cycle, which is the same pathway used by plants, for carbon dioxide fixation. However, more recent studies have suggested that these bacteria can also use the reductive citric acid cycle for carbon dioxide fixation as well. Recent studies have also suggested that the symbionts might be able to use hydrogen gas oxidation to power carbon dioxide fixation, and that they may be able to supplement oxygen with nitrate. Clarifying such basic aspects of this symbiotic system's physiology is relevant, since it is an ecosystem-structuring primary producer at hydrothermal vents, much the way as corals are at reefs.
The purpose of our study was to clarify these key aspects of the physiology of this symbiosis. We collected samples during two research cruises to hydrothermal vent sites in the Eastern Pacific in 2014 and 2016. We incubated tubeworms in high-pressure aquaria in the presence of high and low concentrations of hydrogen sulfide and measured enzyme activities, since earlier studies had indicated that energy supply might influence whether the symbionts were using the Calvin cycle or the reductive citric acid cycle. We also incubated freshly harvested symbionts in the presence of alternative electron donors and acceptors (hydrogen and nitrate) to see whether these compounds could be used to power carbon dioxide fixation by these symbionts. In addition, we also used stable isotope measurements of biomass and lipids, which can be used to make inferences about the activities of the Calvin cycle and reductive citric acid cycles.
We found that both pathways were present and active, whether the sulfide concentrations were high or low, and this was also supported by our stable isotope measurements. We found no evidence for hydrogen utilization by the symbionts, but we did see strong evidence for use of nitrate as an electron acceptor.
Our results are significant as they are the first unambiguous determination of simultaneous activities of the Calvin cycle and reductive citric acid cycle. This is interesting because genome sequences of microorganisms suggest that this might be the case in a variety of other organisms. Simultaneous operation of both cycles begs the question of why this would be an advantage for this and other organisms. Determining why this is the case is likely to be helpful as we engineer other carbon-fixing organisms to catalyze processes of industrial importance.
In the course of our studies, two graduate students (Mary Mangiapia, MS; Juliana Leonard, PhD candidate) were supported. The research has been incorporated into two undergraduate courses at USF (Genomics; Microbial Physiology Lab). Four papers have been published in top-tier peer reviewed journals, and include 165 USF undergraduate students as coauthors. Three more manuscripts are in preparation, and include 22 more USF undergraduate student coauthors.
Last Modified: 06/21/2018
Modified by: Kathleen M Scott
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