Deep-sea hydrothermal fluids circulate through vast portions of the earth?s crust. Volcanically derived gases and products from water-rock reactions support chemolithoautotrophic microbial communities that might be pervasive within the subseafloor and contribute significantly to deep-ocean and subseafloor biomass production. Microorganisms in low-temperature terrestrial environments are commonly segregated by metabolism along chemical gradients. However, demonstration of a similar distribution pattern of organisms along geochemical gradients in deep-sea geothermal environments to date has been rare. The use of hyperthermophiles for such a study is ideal since these organisms are generally not found in contaminating background seawater and since their metabolisms likely reflect the chemistry and temperature of their environment.

Understanding the distribution of different types of chemolithoautotrophic hyperthermophiles in sulfide deposits and diffuse hydrothermal fluids will provide insight into the distribution of much larger populations of autotrophic organisms that may be living in the deep subsurface biosphere. This study will take an important step towards quantitative modeling of microbes in surface and subsurface vent environments by combining metabolic rates from laboratory culture studies with detailed field measurements of fluid chemistry constraints on metabolic reactions. The data will be critical to advancing whole-system models of hydrothermal systems.

This study will address 3 of the 7 fundamental goals in the RIDGE 2000 Science Plan: 1) determining how biological activity affects vent chemistry, 2) characterizing the forces and linkages that determine the structure and extent of the hydrothermal biosphere, and 3) examination of the nature and space/time extent of the deep subseafloor biosphere.

This study will include educational benefits in five areas: 1) graduate student training, 2) undergraduate student training, 3) scientific involvement of underrepresented groups, 4) application of information in courses taught by the investigators, and 5) public education outreach.

Project Report

Although hidden from view, volcanoes in the deep ocean provide a huge, global-scale habitat for microbes that live off the chemical energy produced by the interaction of seawater with hot rock and magmatic gases. Chemo-synthetic microbes form the base of a food chain that produces oases of unique hydrothermal life. There is an extremely high diversity of microbial life capable of deriving energy from hundreds of chemical reactions that occur when volcanic hot spring fluids mix with cold ambient seawater. There are many big questions related to this sub-seafloor biosphere: How much living organic material (biomass) is there? How fast do microbes produce biomass? How much of the total available energy is captured by microbes and converted to biomass? What are the effects on the overlying ocean? To answer these questions, we need to construct models of energy flow and biological productivity in hydrothermal systems. Our research for this project is designed to produce the essential building blocks for such models. The steps to create the building blocks include quantifying the available chemical free energy in real hydrothermal fluids, finding chemical evidence for microbial metabolic activity, collecting microbes and performing laboratory culture experiments to measure microbial reaction rates under different conditions. Our research focused on a few important reactions used by microbes at high temperature, including the production of methane from hydrogen and carbon dioxide (4H2 + CO2 = CH4 + 2H2O, a reaction that is completely independent from photo-synthesis). With the Alvin submersible and specialized sampling instruments, we collected carefully coordinated samples for chemistry and microbiology work from two different hydrothermal areas on the Juan de Fuca Ridge off the coast of Washington state. We found a significant difference in the number of methane-producing microbes between our two sites. This regional difference is due to differences in the underlying geology. The Axial Seamount site is volcanically active and produces higher concentrations of the primary gases that come from magma, so there is more energy available to produce methane and biomass. The Endeavour segment sites have less hydrogen and carbon dioxide and more pre-formed methane, so there is less energy available to produce methane. Unusually high methane in a few specific vent sites corresponds to high abundance of methane-producing microbes and high available chemical energy. We have collected DNA from all of the vent sites, and can use the sequence data to identify what specific microbes are present at the different sites. The culture experiments tell us how fast specific microbes produce biomass under conditions that relate to the real conditions in the sub-seafloor biosphere. The end result of this project is that we have significantly added to the building blocks required to model microbial productivity in hydrothermal systems. The building blocks we have produced are already being incorporated into ecological models under development by the larger scientific community. This is helping us to understand how this hidden part of our planet, the sub-seafloor biosphere, functions and how it impacts the ocean. This was a collaborative project between the University of Washington (D. Butterfield, M. Lilley, D. Kelley) and the University of Massachusetts (J. Holden), with significant contributions from graduate student A. Bourbonnais from the University of Victoria, B.C. Specific scientific products include fluid chemistry results, microbial cell counts, DNA sequence data, and microbial reaction rates from lab culture experiments. Some key publications to date include: Bourbonnais, A., S.K. Juniper, D.A. Butterfield, A.H. Devol, MMM Kuypers, G. Lavik, S.J. Hallam, C.B. Wenk, B.X. Chang, S.A. Murdock, M.F. Lehmann (2012) Activity and abundance of denitrifying bacteria in the subsurface biosphere of diffuse hydrothermal vents of the Juan de Fuca Ridge, Biogeosciences, 9, 4661-4678, doi:10.5194/bg-9-4661-2012. Ver Eecke, Helene, D.A. Butterfield, J.A. Huber, M.D. Lilley, E.J. Olson, K.K. Roe, L.J. Evans, A.Y. Merkel, H.V. Cantin, and J.F. Holden (2012) Hydrogen-limited growth of hyperthermophilic methanogens at deep-sea hydrothermal vents, Proc. Natl. Acad. Sci., 109, 13674-13679, doi:10.1073/pnas.1206632109. Opatkiewicz, A.D., D.A. Butterfield and J.A. Baross (2009) Individual hydrothermal vents at Axial Seamount harbor distinct subseafloor microbial communities, FEMS Microbiology Ecology, 70, 413-424. DOI: 10.1111/j.1574-6941.2009.000747.x In addition to our primary research products, we helped to produce high-resolution seafloor maps with an autonomous underwater vehicle and collected biological material for natural products research to discover potential new beneficial drugs.

Agency
National Science Foundation (NSF)
Institute
Division of Ocean Sciences (OCE)
Type
Standard Grant (Standard)
Application #
0731947
Program Officer
David L. Garrison
Project Start
Project End
Budget Start
2008-01-01
Budget End
2012-12-31
Support Year
Fiscal Year
2007
Total Cost
$394,225
Indirect Cost
Name
University of Washington
Department
Type
DUNS #
City
Seattle
State
WA
Country
United States
Zip Code
98195