EEC, MAA, and CRF conceived and designed the experiments. EEC performed the experiments and analyzed the data. KS and RSA contributed reagents/materials/analysis tools. EEC, MAA, KS, and CRF wrote the paper.
The authors have declared that no competing interests exist.
The deep-sea vestimentiferan tubeworm
Modeling the interactions between deep-sea tubeworms and bacteria/archaea at hydrocarbon seeps provides a solution to their long term energy source and could help to explain the tubeworm's extreme longevity.
Complex positive species interactions have been shown to expand the ecological niche and increase the persistence of the organisms involved in a variety of systems. In terrestrial systems, increased diversity of mycorrhizal symbionts is correlated with increased biodiversity of plant communities, resulting in greater stability and longer persistence at the community level [
A diverse chemosynthetic community relies on the sulfide generated as a by-product of anaerobic degradative processes in the Gulf of Mexico [
In this study, we address the question of whether known biogeochemical processes could supply sulfide at rates sufficient to match the requirements of long-lived
The model predicts that inputs from known sources, including diffusion and advection of deep sulfide along with reduced seawater sulfate, will support a moderately-sized aggregation of 1,000 individuals for an average of 39 y (range, 22 to 78 y) (
Equilibrium line (1:1 ratio) and average, maximum, and minimum values for 1,000 iterations presented. Supply rate based on known sources without sulfate release by tubeworm roots shown in blue. Sulfide supply declines below demand after approximately 40 y. Supply rate including sulfate release from tubeworm roots shown in red, with sulfate release constrained by tubeworm symbionts' sulfide oxidation rate. Sulfide supply exceeds demand for the duration of the model.
An alternate hypothesis to explain the discordance between estimated sulfide supply and uptake rates is the presence of locally elevated seepage rates. Sensitivity analyses were carried out to determine the potential effects of uncertainty in seepage rate on supply estimated for aggregations without root sulfate release. A 10% increase in seepage rate resulted in a 5.6% increase in sulfide supply to aggregations 200 y old and older. This corresponds to only 16.4% of the sulfide required, which does not serve to extend aggregation survivorship (average, 39 y; range, 21 to 79 y) beyond that determined for lower flow rates. To supply the sulfide flux required by older aggregations, seepage rate would have to be at least 363 mm · y−1. This is over ten times greater than the rate used in the model (32 mm · y−1), which is the highest region-wide estimate for the Gulf of Mexico [
The high degree of variability in growth rate and recruitment rate could also affect the ratio of supply and demand in the model. In an aggregation exhibiting anomalously low recruitment, the size of the rhizosphere would increase more rapidly than the biomass of the aggregation. This would lead to high rates of sulfide delivery and generation and low rates of sulfide uptake by tubeworm roots. When initial recruitment rate (
While the model was based on empirical data to the greatest degree possible, estimates of many of the parameters necessary to resolve the model were not available or are extremely difficult to measure in deep water with existing technology. Uptake rates were measured in the laboratory [
The second version of the model is based on the assumption that
Tubeworm sulfate release, in conjunction with high sulfide uptake rates, could contribute to the observation of declining advection rate in older aggregations. By increasing sulfate flux to deeper sediments,
In order to prevent the precipitation of carbonate directly on the root surface,
The release of sulfate by tubeworm roots potentially explains the frequent observation of highly degraded hydrocarbons in the vicinity of large tubeworm aggregations [
Sources of sulfide include advection and diffusion of sulfide from deep sources (yellow) or sulfate reduction using methane (blue), buried organic carbon (green), or C6+ hydrocarbons (dark grey) as electron donors. Sulfate is provided by diffusion from sediments surrounding the rhizosphere, diffusion at the sediment–water interface, and release from tubeworm roots.
Additional sulfate flux from tubeworm roots could also explain the high apparent sulfate diffusion coefficients determined for tubeworm-impacted sediments [
While the proposed interactions between symbiotic tubeworms and sulfate-reducing bacteria are essential for the persistence of
The model results presented here are consistent with the hypothesis that
This study couples an individual-based population growth and sulfide uptake model [
Population model includes individual size-specific growth and mortality rates, and population size-specific recruitment rate. Growth rate was determined by in situ staining of tubeworm aggregations using a blue chitin stain (in situ photograph of stained aggregation demonstrating annual growth shown here) and collection after 12–14 mo. Diagenetic model included advection and diffusion of sulfate, sulfide, methane, bicarbonate, and hydrogen ions as well as organic carbon content of sediments. Fluxes across the rhizosphere (root system) boundary were compared to sulfide uptake rates for simulated aggregations to determine whether sulfide supply could match the required uptake rates of aggregations (for specific methodology see methods). HC, C6+ hydrocarbons; orgC, organic carbon; ox, oxidation reaction; red, reduction reaction.
The population growth model follows the methodology presented in [
At the beginning of each iteration, population growth parameters are chosen for the following population growth model:
where
where
The value of
Once recruitment was determined for that year, the individual-based portion of the model began. Each individual was traced through time with respect to its length, root length, mass, mortality probability, mass-specific sulfide uptake rate, sulfate excretion rate, and hydrogen ion elimination rate. Growth rates of tubeworms were determined by staining tubes in situ (
Size-specific growth of
(A) Growth function and 95% confidence interval for size-specific growth.
(B) Error function fitted to the residuals of the model.
Length
The ratio of root length to tube length was determined from individual length using the following function:
Annual mortality rate was approximated as the size-specific frequency of empty tubes in collected aggregations [
where
By using generalized population growth parameters in the model presented here, we attempt to encompass the range of empirical data from sampled aggregations in our examination of sulfide uptake and supply rates. Taken together, the population growth model including recruitment, growth, and mortality provides a good qualitative if not quantitative fit for any individual aggregation, reflecting the size frequency of tubeworms within sampled aggregations [
Individual sulfide uptake was allowed to vary within the range of laboratory-determined sulfide uptake rates according to that individual's growth rate for that year:
where
Known sources of sulfide available to
Concentrations of all chemical species in the sediments surrounding the rhizosphere were derived from the dataset included in Arvidson et al. [
Dissolved organic carbon (DOC) concentration was used as an estimate of methane concentration. While other forms of DOC make up this total concentration, methane accounts for 90%–95% of the hydrocarbon gasses dissolved in pore waters [
Solid and liquid phase organic carbon was separated into hydrocarbons and buried organic material according to their relative concentrations in hydrocarbon seep and surrounding Gulf of Mexico sediments. Background sediments on the ULS contain 0.71% organic carbon by weight [
The following functions were fitted to the sulfide, sulfate, and methane concentration profiles (
Points represent average concentration at a given depth from 13 sediment cores taken around the periphery of tubeworm aggregations (see
where
where
For sediments encompassed by the rhizosphere, sulfide, sulfate, methane, DOC, and hydrogen ion concentration profiles were determined iteratively prior to model implementation using a central difference scheme:
where
aDiffusion coefficients all corrected for temperature, pressure, and salinity according to Stumm and Morgan [
bAll disassociation constants corrected for temperature, salinity, and pressure according to Stumm and Morgan [
where
where α is 1.7344 and β is 1.0104 for HS−, α is 0.2111 and β is 0.3363 for SO42−, and α is 0.1626 and β is 0.2518 for CH4. Diffusional fluxes of sulfide, sulfate, and methane were calculated according to the first and second derivatives of the concentration profiles as determined by the diameter of each disc.
The model estimates sulfide availability to the aggregation as a whole by summing the fluxes separately determined for each 2-cm disc composing the rhizosphere. Depth-dependant boundary conditions were set for each disc separately based on the sediment profiles (
where
where
where ϕ
Points represent average porosity at a given depth from 13 sediment cores taken around the periphery of tubeworm aggregations (see
Diffusion across the sediment–water interface of the rhizosphere was also considered as an additional input of sulfate and hydrogen ions. This was included as one-dimensional diffusion across a circular surface (subtracting the area encompassed by the tubeworm tubes) with diffusion distance equal to rhizosphere diameter, and concentration differential from seawater concentration to the average concentration within the rhizosphere. Sulfate and hydrogen ion diffusion across the root surface was then added (if included in the set of model realizations) as simple Fickian diffusion. Concentration differential was the difference between internal concentration and average concentration for each disc of the rhizosphere assuming roots were evenly proportioned according to the volume encompassed by each disc. Internal sulfate concentration and pH (
Within the rhizosphere, sulfide generation may be limited by sulfate supply, electron donor availability, or sulfate reduction rate. Sulfate supply was determined as the sum of flux across the series of discs approximating the rhizosphere dome, across the sediment–water interface, and from root sulfate (if available). Available sulfate is utilized for anaerobic methane oxidation first (the more energetically favorable process), then hydrocarbon and organic matter degradation. Electron donors included methane, complex hydrocarbons, and buried organic material. Solid and liquid phase hydrocarbons and organic material were assumed to be homogenous within the rhizosphere. Methane supply was determined as the sum of flux across each rhizosphere disc boundary. Hydrocarbon and organic material concentrations were determined as the amounts encompassed within the rhizosphere volume minus that oxidized in previous years. Sulfate reduction rate was determined from the relative amounts of the various electron donors with higher rates (0.71 μmol · ml−1 · h−1) for methane oxidation and lower rates (0.083 μmol · ml−1 · h−1) for organic matter or hydrocarbon degradation [
Total hydrogen sulfide availability to the aggregation was determined as the sum of sulfide diffusion and advection across each rhizosphere disc and sulfide generated within the rhizosphere from sulfate reduction according to the following reactions:
Bicarbonate (HCO3−) is generated at a 1:1 stoichiometry during anaerobic methane oxidation and a 2:1 stoichiometry in the degradation of organic material. As hydrocarbons are degraded forming smaller chain hydrocarbons and organic acids, bicarbonate is generated at different stoichiometries. Because different-sized hydrocarbons and organic acids were not accounted for in the model, a rough average of these stoichiometries (1.47:1) based on toluene, ethylbenzene, xylene, and hexadecane degradation [
In order to account for carbonate precipitation, the model traced DIC concentration, calcium concentration, hydrogen ion concentration, buffer capacity, carbonate saturation, and carbonate precipitation rate. The buffer state of the rhizosphere was calculated to determine changes in pH resulting from hydrogen ion flux. Buffer capacity (
where
Saturation state is highly dependent on the degree to which calcium and bicarbonate form complexes with other ions. The “free” calcium was determined as the proportion of calcium that is not associated with complexed bicarbonate (HCO3−), carbonate (CO32−), hydroxyl (OH−), or sulfate (SO42−) ions. Free carbonate was determined as the amount not forming complexes with calcium (Ca+) or magnesium (Mg+) ions in solution. Saturation state was then calculated from the product of the concentrations of free calcium and carbonate divided by the solubility product constant. If the saturation state was above one, then carbonate precipitation occurred at a rate determined by:
where
At the end of each annual time step, model output included average length of individuals, population size, sulfide uptake rate, sulfide supply rate, root sulfate flux (if included), root hydrogen ion flux, amount of sulfide supply accounted for by each process (sulfide seepage, anaerobic methane oxidation, organic matter degradation, and hydrocarbon degradation), number of individuals that could be supported by sulfide supply, carbonate precipitation rate, volume of carbonate precipitate, and pH.
We would like to acknowledge K. Montooth, P. Hudson, and five anonymous reviewers for providing helpful comments on drafts of the manuscript. We are indebted to J. Freytag, S. Dattagupta, D. Bergquist, R. Carney, and R. Sassen for the many discussions and advice provided. EEC acknowledges funding from the Center for Environmental Chemistry and Geochemistry at Pennsylvania State University and the Nancy Foster Scholarship Program at the National Oceanographic and Atmospheric Administration (NOAA). This work was supported by the U.S. Minerals Management Service, the NOAA National Undersea Research Program, and the National Science Foundation.
dissolved inorganic carbon
dissolved organic carbon ULS