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Aerobic Microbial Respiration in 86-Million-Year-Old Deep-Sea Red Clay

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Science  18 May 2012:
Vol. 336, Issue 6083, pp. 922-925
DOI: 10.1126/science.1219424

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Deep Breathing

Living microbes have been discovered many meters into marine sediments. On a cruise in the North Pacific Gyre, Røy et al. (p. 922) discovered that oxygen occurred for tens of meters into the sediment. The bacteria living in these sediments were respiring the oxygen but at a slower rate than the supply of organic material dropping out of the water column, allowing these ancient deep marine sediments to remain oxygenated. Modeling showed that the rate of respiration of specific carbon decreased as a function of sediment depth, that is, its age. Thus aerobic metabolism can persist in deep marine sediments.

Abstract

Microbial communities can subsist at depth in marine sediments without fresh supply of organic matter for millions of years. At threshold sedimentation rates of 1 millimeter per 1000 years, the low rates of microbial community metabolism in the North Pacific Gyre allow sediments to remain oxygenated tens of meters below the sea floor. We found that the oxygen respiration rates dropped from 10 micromoles of O2 liter−1 year−1 near the sediment-water interface to 0.001 micromoles of O2 liter−1 year−1 at 30-meter depth within 86 million-year-old sediment. The cell-specific respiration rate decreased with depth but stabilized at around 10−3 femtomoles of O2 cell−1 day−1 10 meters below the seafloor. This result indicated that the community size is controlled by the rate of carbon oxidation and thereby by the low available energy flux.

The discovery of living microbial communities in deeply buried marine sediments (1, 2) has spurred interest in life under extreme energy limitation (3). The subtropical gyres are the most oligotrophic regions of the oceans. Primary productivity in the surface waters of the gyres is low, yet within the same order of magnitude as the surrounding open ocean (Fig. 1). Oxygen penetrates many meters into the seabed below the gyres, which indicates extremely low rates of microbial community respiration (4, 5) in contrast to the rest of the seabed (4), where in general oxygen penetration is limited to millimeters to decimeters depth, according to a square root function of the organic matter flux (69).

Fig. 1

Cruise track, sampling sites, and primary production along the cruise track. The primary production was estimated from Sea-WiFs remote-sensing data converted into integrated primary productivity averaged over 10 years by the Institute of Marine and Coastal Sciences Ocean Primary Productivity Team (Rutgers, State University of New Jersey) using the algorithms from (25). The shaded areas mark the data along the actual cruise track. The inserted graphs show the oxygen distribution in the sediment at the sampled sites. Sites 4 and 7 on the equator followed the trend in the other equatorial sites and are omitted for clarity only. At site 9 we retrieved only 4 m of core, but the profile was similar to sites 10 and 11. By site 11, we reoccupied the GPC-3 site that has been studied in great detail [e.g., (14)].

On R/V Knorr voyage 195, we collected sediment cores up to 28 m along the equator and into the North Pacific Gyre and measured the oxygen distribution throughout the retrieved cores by using needle-shaped optical O2 sensors (PreSens Precision Sensing GmbH, Regensburg, Germany) (Fig. 1). Along the equator, from the Galapagos (site 3) and 4700 km westward into the Pacific Ocean (site 8), the oxygen flux across the sediment-water interface decreased moderately from 60 to 45 mmol m−2 year−1, whereas the oxygen penetration depth increased from 6 to 9.5 cm (Fig. 1 and table S1). The trend in oxygen flux followed the trend in primary production in the surface water. The increase in oxygen penetration depth in the sediment along the equator is less pronounced than the decrease in oxygen flux, which is expected from the general relation between oxygen flux and oxygen penetration (10). From the equator (site 8) and into the North Pacific Gyre (site 11), the primary productivity decreased by 50%, but the oxygen penetration depth increased from 9 cm to greater than 30 m. Such a large change in oxygen penetration cannot be explained by less productivity in the gyre nor by the increase in water depth (11).

The volumetric oxygen consumption rates down the length of the core were modeled at high resolution from the deep oxygen profiles we obtained. In the model, we calculated carbon mineralization as the product of the measured particulate organic carbon concentration at each depth (Corg) and an initially unknown and depth-dependent reactivity (k) of the Corg. For simplicity, we assume a 1:1 molar ratio between carbon oxidation and O2 consumption. We further assumed that k decreases monotonically with time (t), and that the decrease can be described by a power law function (12):k = A × (t + t0)B (1)The mass balance of oxygen throughout the core, taking into account molecular diffusion and oxygen consumption, was solved using the software Comsol Multiphysics. Measured depth-dependent values for porosity, molecular diffusion coefficient (Dm), and Corg were fed into the model as smoothed tabulated files and interpolated to fit the modeling grid. Parameters in Eq. 1 were varied to find the best fit to the measured deep oxygen profiles, resulting in the volumetric oxygen consumption rate along the length of the core and the relation between carbon age and oxidation rate. This approach had two advantages relative to calculating the reaction rate for oxygen only from profile curvature within discrete intervals (13). First, we avoided lumping high rates in the upper part of an interval with lower rates in the lower part, because this invariably leads to underestimation of the rates at the top of the interval. This is critical near the sediment surface, where the rates changed rapidly. Second, the relation between carbon reactivity and age can be used to predict how burial velocity influences the depth distribution of oxygen consumption and thus oxygen distribution (see below).

The deep oxygen profiles in the North Pacific Gyre were modeled well by assuming that the degradability of organic matter in the sediment follows a simple power law function of carbon age (Fig. 2A). Oxygen penetration depth in the seabed beneath the North Pacific Gyre is more than 30 m. In the Atlantic gyres, with a similar organic carbon flux to the deep seafloor, oxygen penetrates only to 0.2 to 0.5 m in the sediment (8). The difference is a result of the low sedimentation rate in the North Pacific Gyre, where 90% of the organic matter mineralization in the 100-m deep oxic sediment at site 11 takes place in the top 6 cm. Carbon burial from the upper bioturbated zone into the deeper sediment is extremely slow, and the material is therefore highly refractory at depth. The fraction of total carbon mineralization that takes place below 1 m is about 1%.

Fig. 2

Oxygen distribution in the seabed below the North Pacific Gyre at site 11. (A) Data originate from three independent sediment cores. The curve illustrates the fit used to calculate volume-specific oxygen consumption rates. (Inset) Data and fit for lower part of core. (B) Curve is the modeled volumetric oxygen consumption rates. Open circles are the cell-specific oxygen consumption rates obtained by dividing the volumetric oxygen consumption rate by cell counts.

The effect of low sedimentation rates on oxygen distribution was shown by using a numerical model similar to the one used to quantify oxygen consumption rates. Instead of feeding the measured carbon concentration profile into the model, we imposed a flux of carbon to the sediment surface. Burial was implemented as a downward advective term. Carbon and oxygen consumption were implemented by Eq. 1 with the fit parameters determined from site 11. We then varied the burial rate and calculated steady-state oxygen profiles (Fig. 3).

Fig. 3

Oxygen profiles modeled from a constant influx of organic material but varying sediment accumulation rates. All profiles represent the same oxygen uptake rate at the sediment surface. Symbols show measured oxygen profiles from site 9 (circles) and site 11 (squares).

The shape of the theoretical oxygen distributions are close to those observed in the North Pacific Gyre (Fig. 3). All modeled profiles have the same oxygen gradient, that is, total oxygen flux, at the sediment-water interface because the scenarios are modeled with the same carbon input and because practically all the carbon is mineralized. At decreasing sedimentation rates, oxygen penetrates deeper because relatively less mineralization happens far below the surface. A shorter distance of diffusion between the sediment surface and the depth of mineralization caused less overall depletion of oxygen, although the total depth-integrated oxygen consumption was the same. A sudden shift in oxygen penetration, from dm range to the full depth of the sediment, occurs in a relatively narrow range of sedimentation rates of 1 to 5 mm per 1000 years. The sedimentation rate at site 11 has been stable at about 0.2 mm per 1000 years for the past 70 million years, with a moderate increase occurring during the most recent 2.5 million years (14).

The total sediment thickness at the core sites in the North Pacific Gyre is 88 to 100 m (15). Extrapolation of the oxygen gradient at the bottom of the cores suggests that the entire sediment column is oxic, at least at site 11. The fully oxic sediment column excludes anaerobic metabolic pathways that normally dominate subsurface mineralization of organic matter in the seabed. This provides a unique opportunity to quantify carbon mineralization rates as a function of sediment age across a long time span. Both traditional nonparametric modeling of oxygen consumption rates from profile curvature (13) and the applied power law model yielded volumetric oxygen consumption rates that decreased from 10 μmol O2 liter−1 year−1 at a depth of 0.5 m below the sediment-water interface to 0.001 μmol O2 liter−1 year−1 in sediment older than 66 million years, that is, buried below 20 to 30 m at site 11 (16) (Fig. 2B).

The fit to a simple power law model (Fig. 2A) gave an exponent of –1.7, in contrast with an exponent of –1 reported by (12). Other continuously decreasing functions could have been used to describe the trend in the data, for example, a reactive continuum model that assumes exponential depletion of multiple hypothetical pools of complex organic matter (17, 18). That approach is comparable to ours because a power law can be expressed as a sum of many exponential functions. We prefer the power law for its simplicity and because a model based on changing chemical properties of dead organic matter agreed well with the chemical alterations that occurred during aging and maturation.

The number of prokaryotic cells in the surface sediment of the North Pacific Gyre was 108 cells cm−3. The cell counts decreased along the length of the core to 103 cells cm−3 at 20 m below the sea floor. Below that depth, the cell density was too low to enumerate by fluorescence microscope counting even after cell extraction (19). The cell density decreased relatively less down along the core than the volumetric oxygen consumption rate. The mean oxygen consumption rate per cell therefore decreased with increasing sediment depth and age (Fig. 2B). The per-cell respiration rate appeared to stabilize at around 10−3 fmol cell−1 day−1. This overlaps with the range of cell-specific sulfate reduction rates in coastal subsurface sediments (20, 21), but it is 3 orders of magnitude below the cell-specific respiration rate of anaerobic heterotrophs in pure culture (22) and below the respiration rate devoted to maintenance in the slowest-growing chemostat cultures (23). Thus, life in the subsurface is probably more similar to cultures in long-term stationary state (24) than to growing cultures. The higher cell-specific respiration rates reported previously from deeply oxygenated sediments in the South Pacific Gyre (5) are not comparable because those are average rates for the entire sediment column and are skewed upward by relatively high rates of metabolism at the sediment-water interface.

The similarity in mean metabolic rate per cell between sites with very different mineralization rates and different terminal electron acceptors suggests that these microbial communities may be living at the minimum energy flux needed for prokaryotic cells to subsist and that the total available energy flux ultimately controls the microbial community size in the deep biosphere.

Supplementary Materials

www.sciencemag.org/cgi/content/full/336/6083/922/DC1

Materials and Methods

Table S1

References (26, 27)

References and Notes

  1. Acknowledgments: The assistance from E. Caporelli, B. Costello, and E. Benway at Woods Hole Oceanographic Institution (WHOI) was crucial for our participation in the R/V Knorr cruise. We thank B. Gribsholt, the shipboard science party, the WHOI long-coring team, and the crew of the R/V Knorr for cooperation at sea. Net primary production data were provided by R. O’Malley from Oregon State University (www.science.oregonstate.edu/ocean.productivity/index.php). Our study was funded by the Danish National Research Foundation, the German Max Planck Society, Aarhus University, the German Federal Ministry of Research and Education via the GeoEnergie Project, and the U.S NSF (OCE grant 0752336 and the NSF-funded C-DEBI Science and Technology Center). This is C-DEBI publication number 130.
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