Award Abstract # 1136451
Dimensions: Collaborative Research: An Integrated Study of Energy Metabolism, Carbon Fixation, and Colonization Mechanisms in Chemosynthetic Microbial Communities at Deep-Sea Vents

NSF Org: OCE
Division Of Ocean Sciences
Recipient: RUTGERS, THE STATE UNIVERSITY
Initial Amendment Date: September 12, 2011
Latest Amendment Date: September 12, 2011
Award Number: 1136451
Award Instrument: Standard Grant
Program Manager: David Garrison
OCE
 Division Of Ocean Sciences
GEO
 Directorate for Geosciences
Start Date: October 1, 2011
End Date: September 30, 2016 (Estimated)
Total Intended Award Amount: $420,434.00
Total Awarded Amount to Date: $420,434.00
Funds Obligated to Date: FY 2011 = $420,434.00
History of Investigator:
  • Costantino Vetriani (Principal Investigator)
    vetriani@marine.rutgers.edu
Recipient Sponsored Research Office: Rutgers University New Brunswick
3 RUTGERS PLZ
NEW BRUNSWICK
NJ  US  08901-8559
(848)932-0150
Sponsor Congressional District: 12
Primary Place of Performance: Rutgers University New Brunswick
71 Dudley Road
New Brunswick
NJ  US  08901-8521
Primary Place of Performance
Congressional District:
06
Unique Entity Identifier (UEI): M1LVPE5GLSD9
Parent UEI:
NSF Program(s): Dimensions of Biodiversity
Primary Program Source: 01001112DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 1319, 1650, 7968, 9117, 9169, EGCH
Program Element Code(s): 796800
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.050

ABSTRACT

Deep-sea hydrothermal vents, first discovered in 1977, are poster child ecosystems where microbial chemosynthesis rather than photosynthesis is the primary source of organic carbon. Significant gaps remain in our understanding of the underlying microbiology and biogeochemistry of these fascinating ecosystems. Missing are the identification of specific microorganisms mediating critical reactions in various geothermal systems, metabolic pathways used by the microbes, rates of the catalyzed reactions, amounts of organic carbon being produced, and the larger role of these ecosystems in global biogeochemical cycles. To fill these gaps, the investigators will conduct a 3-year interdisciplinary, international hypothesis-driven research program to understand microbial processes and their quantitative importance at deep-sea vents. Specifically, the investigators will address the following objectives:
1. Determine key relationships between the taxonomic, genetic and functional diversity, as well as the mechanisms of energy and carbon transfer, in deep-sea hydrothermal vent microbial communities.
2. Identify the predominant metabolic pathways and thus the main energy sources driving chemoautotrophic production in high and low temperature diffuse flow vents.
3. Determine energy conservation efficiency and rates of aerobic and anaerobic chemosynthetic primary productivity in high and low temperature diffuse flow vents.
4. Determine gene expression patterns in diffuse-flow vent microbial communities during attachment to substrates and the development of biofilms.

Integration: To address these objectives and to characterize the complexity of microbially-catalyzed processes at deep-sea vents at a qualitatively new level, we will pursue an integrated approach that couples an assessment of taxonomic diversity using cultivation-dependent and -independent approaches with methodologies that address genetic diversity, including a) metagenomics (genetic potential and diversity of community), b) single cell genomics (genetic potential and diversity of uncultured single cells), c) meta-transcriptomics and -proteomics (identification and function of active community members, realized potential of the community). To assess function and response to the environment, these approaches will be combined with 1) measurement of in situ rates of chemoautotrophic production, 2) geochemical characterization of microbial habitats, and 3) shipboard incubations under simulated in situ conditions (hypothesis testing under controlled physicochemical conditions). Network approaches and mathematical simulation will be used to reconstruct the metabolic network of the natural communities. A 3-day long project meeting towards the end of the second year will take place in Woods Hole. This Data Integration and Synthesis meeting will allow for progress reports and presentations from each PI, postdoc, and/or student, with the aim of synthesizing data generated to facilitate the preparation of manuscripts.

Intellectual Merit. Combining the community expression profile with diversity and metagenomic analyses as well as process and habitat characterization will be unique to hydrothermal vent microbiology. The approach will provide new insights into the functioning of deep-sea vent microbial communities and the constraints regulating the interactions between the microbes and their abiotic and biotic environment, ultimately enabling us to put these systems into a quantitative framework and thus a larger global context.

Broader Impacts. This is an interdisciplinary and collaborative effort between 4 US and 4 foreign institutions, creating unique opportunities for networking and fostering international collaborations. This will also benefit the involved students (2 graduate, several undergraduate) and 2 postdoctoral associates. This project will directly contribute to many educational and public outreach activities of the involved PIs, including the WHOI Dive & Discover program; single cell genomics workshops and Cafe Scientifique (Bigelow); REU (WHOI, Bigelow, CIW); COSEE and RIOS (Rutgers), and others. The proposed research fits with the focus of a number of multidisciplinary and international initiatives, in which PIs are active members (SCOR working group on Hydrothermal energy and the ocean carbon cycle, http://www.scorint. org/Working_Groups/wg135.htm; Deep Carbon Observatory at CIW, https://dco.gl.ciw.edu/; Global Biogeochemical Flux (GBF) component of the Ocean Observatories Initiative (OOI), http://www.whoi.edu/GBF-OOI/page.do?pid=41475)

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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(Showing: 1 - 10 of 28)
Bertrand, E. M., Keddis, R., Groves, J. T., Vetriani, C. and Narehood Austin, R. "Identity and mechanisms of alkane-oxidizing metalloenzymes from deep-sea hydrothermal vents" Front. Microbiol. , v.4 , 2013 , p.109 10.3389/fmicb.2013.00109
Bertrand, E. M., Keddis, R., Groves, J. T., Vetriani, C. and Narehood Austin, R. "Identity and mechanisms of alkane-oxidizing metalloenzymes from deep-sea hydrothermal vents." Front. Microbiol. , v.4 , 2013 , p.109
Bertrand, E. M., Keddis, R., Groves, J. T., Vetriani, C. and Narehood Austin, R. "Identity and mechanisms of alkane-oxidizing metalloenzymes from deep-sea hydrothermal vents." Front. Microbiol. , v.4 , 2013 , p.109
Bertrand, E. M., Keddis, R., Groves, J. T., Vetriani, C. and Narehood Austin, R. "Identity and mechanisms of alkane-oxidizing metalloenzymes from deep-sea hydrothermal vents." Front. Microbiol.. , 2013 , p.109 DOI: 10.3389/fmicb.2013.00109
Giovannelli, D., Chung, M., Staley, J., Starovoytov, V., Le Bris, N. and Vetriani, C. "Sulfurovum riftiae sp. nov., a mesophilic, thiosulfate-oxidizing, nitrate-reducing chemolithoautotrophic Epsilonproteobacterium isolated from the tube of the deep-sea hydrothermal vent polychaete, Riftia pachyptila." Sulfurovum riftiae sp. nov., a mesophilic, thiosulfate-oxidizing, nitrate-reducing chemolithoautotrophic Epsilonproteobacterium isolated from the tube of the deep-sea hydrothermal vent polychaete, Riftia pachyptila. Intl. J. Syst. Evol. Microbiol. 66:2697 , v.66 , 2016 , p.2697 10.1099/ijsem.0.001106
Grosche, A., Sekaran, H., Pérez-Rodríguez, I., Starovoytov, V. and Vetriani, C. "Cetia pacifica gen. nov., sp. nov., a novel chemolithoautotrophic, thermophilic, nitrate-ammonifying bacterium from a deep-sea hydrothermal vent" Intl. J. Syst. Evol. Microbiol. , v.65 , 2015 , p.1144 doi:10.1099/ijs.0.000070
Grosche, A., Sekaran, H., Pérez-Rodríguez, I., Starovoytov, V. and Vetriani, C. "Cetia pacifica gen. nov., sp. nov., a novel chemolithoautotrophic, thermophilic, nitrate-ammonifying bacterium from a deep-sea hydrothermal vent." Intl. J. Syst. Evol. Microbiol. , v.65 , 2015 , p.1144 10.1099/ijs.0.000070
Houghton, J.L., Foustoukos, D., Flynn T., Vetriani, C., Brandley, A., Fike, D. "Thiosulfate oxidation by Thiomicrospira thermophila: metabolic flexibility in response to ambient geochemistry" Environ. Microbiol. , v.18 , 2016 , p.3057 10.1111/1462-2920.13232
O'Brien, C. E., Giovannelli, D., Govenar, B., Luther, G. W., Lutz, R. A., Shank, T. M. and Vetriani, C. "Microbial biofilms associated with fluid chemistry and megafaunal colonization at post-eruptive deep-sea hydrothermal vents" Deep-Sea Res. II , v.121 , 2015 , p.31 doi:10.1016/j.dsr2.2015.07.020
O'Brien, C. E., Giovannelli, D., Govenar, B., Luther, G. W., Lutz, R. A., Shank, T. M. and Vetriani, C. "Microbial biofilms associated with fluid chemistry and megafaunal colonization at post-eruptive deep-sea hydrothermal vents." Deep-Sea Res. II , v.121 , 2015 , p.31 10.1016/j.dsr2.2015.07.020
Patwardhan, S. and Vetriani, C. "Varunaivibrio sulfuroxidans gen. nov., sp. nov., a facultatively chemolithoautotrophic, mesophilic alphaproteobacterium from a shallow-water gas vent at Tor Caldara, Tyrrhenian Sea" Intl. J. Syst. Evol. Microbiol. , v.66 , 2016 , p.3579 10.1099/ijsem.0.001235
(Showing: 1 - 10 of 28)

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.

The biological communities that inhabit deep-sea hydrothermal vents are supported by chemosynthetic microorganisms that convert the energy associated with inorganic chemical species of volcanic origin into biochemical energy (ATP), which in turn is used to convert carbon dioxide into organic carbon. In particular, bacteria belonging to the Epsilonproteobacteria and Aquificales play an important role as primary producers at deep-sea hydrothermal vents. Epsilonproteobacteria and Aquificales exhibit similar metabolisms – i.e. the oxidation of reduced sulfur compounds and hydrogen with both oxygen and nitrate or the oxidation of hydrogen with elemental sulfur coupled to the fixation of inorganic carbon – and thus occupy a similar ecological niche, but at different temperatures (Epsilonproteobacteria: 20°C - 70°C; Aquificales: 60°C - 90°C). However, little is known about the preferential or simultaneous use of these alternative e-donors/acceptors and the conditions under which the corresponding enzymes are expressed.

In the course of this study, we elucidated some of the central metabolic pathways used by microorganisms that colonize deep-sea vents by forming biofilm communities. Overall our observations indicate that, by fixing CO2 via the reductive tricarboxylic cycle (rTCA) and conserving energy via the reduction of nitrate to either dinitrogen gas or to ammonium, vent bacteria are of particular interest as they link the carbon and nitrogen cycles at in these geothermal habitats.

We also investigated how vent Epsilonproteobacteria communicate among each other via chemical signaling (quorum sensing) and we showed that pathogenic members of this group of bacteria inherited the quorum sensing pathways from their thermophilic bvent relatives.

Major outcomes from this project include thirteen peer-reviewed publications and an article for the general public soon to be published in the magazine Scientia.

Further  information about this project was disseminated on the Deep-Sea Microbiology Lab website (https://marine.rutgers.edu/deep-seamicrobiology/index.html), including a description of the oceanographic expedition sponsored by this project (https://marine.rutgers.edu/deep-seamicrobiology/at26-10.html), photo and instructional videos (https://marine.rutgers.edu/deep-seamicrobiology/gallery.html) and the Lab's rationale to study the phisiology (https://marine.rutgers.edu/deep-seamicrobiology/Physiology.html), ecology (https://marine.rutgers.edu/deep-seamicrobiology/Ecology.html) and evolution (https://marine.rutgers.edu/deep-seamicrobiology/Evolution.html) of marine prokaryotes.


Last Modified: 05/12/2017
Modified by: Costantino Vetriani

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