The global geographic distribution of subseafloor sedimentary microbes and the cause(s) of that distribution are largely unexplored. Here, we show that total microbial cell abundance in subseafloor sediment varies between sites by ca. five orders of magnitude. This variation is strongly correlated with mean sedimentation rate and distance from land. Based on these correlations, we estimate global subseafloor sedimentary microbial abundance to be 2.9·10 29 cells [corresponding to 4.1 petagram (Pg) C and ∼0.6% of Earth's total living biomass]. This estimate of subseafloor sedimentary microbial abundance is roughly equal to previous estimates of total microbial abundance in seawater and total microbial abundance in soil. It is much lower than previous estimates of subseafloor sedimentary microbial abundance. In consequence, we estimate Earth's total number of microbes and total living biomass to be, respectively, 50-78% and 10-45% lower than previous estimates.deep biosphere | cell enumeration | global microbial biomass | subsurface life B acteria and archaea drive many fundamental processes in marine sediment, including oxidation of organic matter, production of methane and other hydrocarbons, and removal of sulfate from the ocean (1-3). Previous studies of subseafloor sediment from ocean margins and the eastern equatorial Pacific Ocean reported high abundances of microbial cells (2). RNA studies indicate that many of these cells are active (4), have a diverse community composition (5, 6), and exhibit high diversity in their anaerobic metabolic activity (5). Cell counts from these environments generally show little variation between sites (2, 7) and decrease logarithmically with sediment depth, although there can be sharp peaks of high cell densities in zones of anaerobic methane-oxidation (2, 8).In 1998, Whitman et al. (9) (Fig. 1A). In these regions, dissolved oxygen penetrates deeply into the sediment and microbial activity is generally aerobic (5, 11). Metabolic activity per cell is extremely low among the anaerobes of both ocean margins and upwelling regions (12) and the aerobes of the open-ocean gyres (5, 11).The differences between cell counts from ocean margins and upwelling areas and cell counts from oceanic gyres raise three questions. First, how does the abundance of microbes in subseafloor sediment vary throughout the world ocean? Second, what property or properties are likely to control that variation? Third, how does this variation affect estimates of total subseafloor sedimentary biomass and Earth's total biomass?
Materials and MethodsTo address these questions, we compiled our cell counts from the South Pacific Gyre (5), the North Pacific Gyre, and the eastern equatorial Pacific Ocean with previously published counts from ocean margins and the equatorial Pacific Ocean (Fig. 1B). We limited this compilation to sites with cell counts both above and below 1 m below sea floor (mbsf). To compare the data from different sites, we parameterized the cell distribution at each site by plotting cell abundance...
The low-productivity South Pacific Gyre (SPG) is Earth's largest oceanic province. Its sediment accumulates extraordinarily slowly (0.1-1 m per million years). This sediment contains a living community that is characterized by very low biomass and very low metabolic activity. At every depth in cored SPG sediment, mean cell abundances are 3 to 4 orders of magnitude lower than at the same depths in all previously explored subseafloor communities. The net rate of respiration by the subseafloor sedimentary community at each SPG site is 1 to 3 orders of magnitude lower than the rates at previously explored sites. Because of the low respiration rates and the thinness of the sediment, interstitial waters are oxic throughout the sediment column in most of this region. Consequently, the sedimentary community of the SPG is predominantly aerobic, unlike previously explored subseafloor communities. Generation of H 2 by radiolysis of water is a significant electron-donor source for this community. The per-cell respiration rates of this community are about 2 orders of magnitude higher (in oxidation/reduction equivalents) than in previously explored anaerobic subseafloor communities. Respiration rates and cell concentrations in subseafloor sediment throughout almost half of the world ocean may approach those in SPG sediment.aerobic ͉ biomass ͉ oxic ͉ radiolysis ͉ respiration
Ammonia-oxidizing archaea (AOA) dominate microbial communities throughout oxic subseafloor sediment deposited over millions of years in the North Atlantic Ocean. Rates of nitrification correlated with the abundance of these dominant AOA populations, whose metabolism is characterized by ammonia oxidation, mixotrophic utilization of organic nitrogen, deamination, and the energetically efficient chemolithoautotrophic hydroxypropionate/hydroxybutyrate carbon fixation cycle. These AOA thus have the potential to couple mixotrophic and chemolithoautotrophic metabolism via mixotrophic deamination of organic nitrogen, followed by oxidation of the regenerated ammonia for additional energy to fuel carbon fixation. This metabolic feature likely reduces energy loss and improves AOA fitness under energy-starved, oxic conditions, thereby allowing them to outcompete other taxa for millions of years.
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