Microbial activity in the marine deep biosphere: progress and prospects

Abstract

The vast marine deep biosphere consists of microbial habitats within sediment, pore waters, upper basaltic crust and the fluids that circulate throughout it. A wide range of temperature, pressure, pH, and electron donor and acceptor conditions exists-all of which can combine to affect carbon and nutrient cycling and result in gradients on spatial scales ranging from millimeters to kilometers. Diverse and mostly uncharacterized microorganisms live in these habitats, and potentially play a role in mediating global scale biogeochemical processes. Quantifying the rates at which microbial activity in the subsurface occurs is a challenging endeavor, yet developing an understanding of these rates is essential to determine the impact of subsurface life on Earth's global biogeochemical cycles, and for understanding how microorganisms in these "extreme" environments survive (or even thrive). Here, we synthesize recent advances and discoveries pertaining to microbial activity in the marine deep subsurface, and we highlight topics about which there is still little understanding and suggest potential paths forward to address them. This publication is the result of a workshop held in August 2012 by the NSF-funded Center for Dark Energy Biosphere Investigations (C-DEBI) "theme team" on microbial activity (www.darkenergybiosphere.org).

Keywords: C-DEBI; IODP; biogeochemistry; deep biosphere; oceanic crust; sediment; subsurface microbiology.

Figure 1

Map of the locations where rates of microbial activity in deep sediment have been measured (through radio-isotope tracer techniques) or inferred from modeling of vertical geochemical parameters during drilling program expeditions. This map does not include hydrocarbon seep environments. Map created using ArcGIS 9. References used are (Oremland et al., ; Tarafa et al., ; Whelan et al., ; Cragg et al., , ; de Angelis et al., ; Cragg et al., ; Lein et al., ; Fossing et al., ; Hoehler et al., ; Tsunogai et al., ; D'Hondt et al., ; , ; Böttcher et al., ; Joye et al., , ; Lam et al., , ; Orcutt et al., ; Parkes et al., ; Niemann et al., ; Sivan et al., ; Wang et al., ; Nunoura et al., ; Omoregie et al., ; Schippers et al., ; Wankel et al., , ; Yoshioka et al., ; Lomstein et al., ; Nickel et al., ; Røy et al., ; Ziebis et al., ; Maignien et al., 2013).

Figure 2

Representative ranges of microbial activity in the marine deep biosphere based on literature values of measured and modeled volumetric rates. Starred rate measurements derive from measurements of in situ conditions; all others derive from ex situ incubation experiments. Note that the value from Wankel et al. (2011) assumes a depth of 10 cm. Environments include some deep sediment locales as well as “windows” to the deep biosphere such as hydrothermal vents. Rates of different metabolisms are normalized to moles of electrons per unit time per unit volume. Dagger denotes references where the ranges of bar in graph reflect the 8-fold difference in moles of electrons per methane molecule for methanogenesis depending on the substrate—8 mol e- per 1 mol CO₂ vs. 1 mol e- per 1 mol acetate. References used are (de Angelis et al., ; Iversen and Jørgensen , Jørgensen, ; Lein et al., ; Fossing et al., ; Joye et al., , ; Orcutt et al., Biddle et al., ; Niemann et al., ; Wang et al., ; Nunoura et al., ; Omoregie et al., ; Wankel et al., , ; Lomstein et al., ; Røy et al., ; Maignien et al., 2013).

Figure 3

Global marine sediment organic matter oxidation by electron acceptor and habitat, based on data published elsewhere (Thullner et al., 2009) and reprinted here with permission. Pie chart sections represent the percentage of organic matter delivered to the seafloor that is oxidized by the indicated electron acceptor in the upper 50 cm of sediment. The depths of the seawater-sediment interface for each environment are listed below each chart. Sufficient data were not reported to include Mn(IV) as an electron acceptor, but note that it is generally only 10% of the values for Fe(III) (Thullner et al., 2009). Other fates of organic matter degradation (e.g., fermentation and methanogenesis) were not considered in the study [methanogenesis accounts for about 5% of global carbon mineralization (Jørgensen and Kasten, 2006)].

Figure 4

Relative percentage of different sedimentary habitats (by area) compared to the relative amounts of cumulative organic matter degradation in those habitats, based on data presented elsewhere (Thullner et al., 2009) and reprinted here with permission. Note that only habitats between 60°N and 60°S were considered in this study, and that the study assumed that all organic matter was degraded in the upper 30 cm of sediment.