Subseafloor Sedimentary Life in the South Pacific Gyre
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Subseafloor sedimentary life in the South Pacific Gyre Steven D’Hondta,1, Arthur J. Spivacka, Robert Pockalnya, Timothy G. Ferdelmanb, Jan P. Fischerb, Jens Kallmeyerc, Lewis J. Abramsd, David C. Smitha, Dennis Grahama, Franciszek Hasiuke, Heather Schruma, and Andrea M. Stancine aGraduate School of Oceanography, University of Rhode Island, Narragansett Bay Campus, South Ferry Road, Narragansett, RI 02882; bMax Planck Institute for Marine Microbiology, Celsiusstrasse 1, D-28359 Bremen, Germany; cDepartment of Geosciences, University of Potsdam, Haus 27, Zi. 0.34, Karl-Liebknecht-Strasse 24, 14476 Golm, Germany; and dDepartment of Geography and Geology, University of North Carolina at Wilmington, DeLoach Hall, 601 South College Road, Wilmington, NC 28403; and eDepartment of Geological Sciences, University of Michigan, 2534 C.C. Little Building, 1100 North University Avenue, Ann Arbor, MI 48109 Edited by Edward F. DeLong, Massachusetts Institute of Technology, Cambridge, MA, and approved May 6, 2009 (received for review November 23, 2008) The low-productivity South Pacific Gyre (SPG) is Earth’s largest oce- anic province. Its sediment accumulates extraordinarily slowly (0.1–1 60˚ m per million years). This sediment contains a living community that is characterized by very low biomass and very low metabolic activity. 30˚ 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 0˚ explored subseafloor communities. The net rate of respiration by the subseafloor sedimentary community at each SPG site is 1 to 3 orders -30˚ of magnitude lower than the rates at previously explored sites. Because of the low respiration rates and the thinness of the sediment, -60˚ interstitial waters are oxic throughout the sediment column in most of this region. Consequently, the sedimentary community of the SPG Sea-surface Chlorophyll (mg/m3) is predominantly aerobic, unlike previously explored subseafloor communities. Generation of H2 by radiolysis of water is a significant 0.01 0.03 0.1 0.3 1 3 10 electron-donor source for this community. The per-cell respiration rates of this community are about 2 orders of magnitude higher (in Fig. 1. Site locations on a map of time-averaged sea-surface chl-a concen- trations [Global SeaWiFS Chlorophyll (mean of September 1997–December oxidation/reduction equivalents) than in previously explored anaer- 2004)]. White dots mark sites analyzed for this study. Black dots mark sites obic subseafloor communities. Respiration rates and cell concentra- previously analyzed for subseafloor biomass and/or activity (2, 3). Dashed tions in subseafloor sediment throughout almost half of the world white lines delimit the area in each gyre where the sea-surface chlorophyll-a ocean may approach those in SPG sediment. (chl-a) concentration is Յ0.14 mg/m3. aerobic ͉ biomass ͉ oxic ͉ radiolysis ͉ respiration 130 m (SPG-12) (determined from 3.5-kHz sonar and seismic ife is previously unknown in the subseafloor sediment of the vast reflection profiles). At the deepest water sites in the low- Llow-productivity regions that dominate the open ocean. Past chlorophyll region of the SPG (sites SPG-1 to SPG-4 and SPG-9 studies have focused on sites relatively close to shore and beneath to SPG-11), the cored sediment is homogeneous brown clay major upwelling zones (1–4) (Fig. 1), where biological productivity capped by a nearly continuous layer of manganese (Mn) nodules. and organic flux to the seafloor are generally high (5). Their Discrete horizons of Mn nodules or Mn crust also occur deeper subseafloor [greater than 1.5 m below seafloor (mbsf)] sedimentary in the cored sediment at SPG-1 and SPG-10. Silt and sand-sized communities contain abundant living microbes (6–9). These com- Mn nodules and cosmic debris commonly occur within the brown munities (10, 11) and their metabolic activities (3, 12) are diverse. clay, but fossils, except for scattered ichthyoliths, do not. The Their activities are dominated by fermentation, sulfate reduction, cored sediment at the shallowest sites (SPG-6 and SPG-7) is and methanogenesis (13). Their principal food source is buried calcareous nannofossil-bearing clay. The sediment at SPG-5 is organic matter from the surface world (3). The environmental transitional between these 2 lithologies. Site SPG-12 lies outside properties of these previously sampled sites differ greatly from the low-chlorophyll region, and its cored sediment is dominantly environmental properties throughout most of the open ocean, where siliceous ooze with abundant diatom debris and sponge spicules. oceanic productivity and organic flux to the seafloor are very low (5). Mean sedimentation rates are extremely low in the low- To understand the extent and nature of subseafloor life in the chlorophyll region of the SPG (17) (Table 1). In general, they are low-productivity heart of the ocean, expedition Knox-02RR lowest at sites where the seafloor is below the calcite compen- surveyed and cored the sediment at 10 sites throughout the sation depth [Ϸ4,500 m below sea level in this region (18)] and South Pacific Gyre (SPG) and at 1 site at its southern margin sea-surface chlorophyll concentrations are below 0.1 mg chl/m3. (Fig. 1). The central SPG has been described as Earth’s largest Mean sedimentation rate is higher at our eastern-most sites, oceanic desert (14). The middle of the gyre is farther from where water depth is shallowest (allowing carbonate sediment to continents and productive oceanic regions than any other site on accumulate), and at our western-most sites, where sea-surface Earth. It contains the clearest seawater in the world (15). Its chlorophyll content is above 0.1 mg chl/m3 and the sites were organic flux to the seafloor is extremely low (5). The area of its south of the central gyre many tens of millions of years ago. The rate low-chlorophyll [Յ0.14 mg of chlorophyll-a/m3 (chl-a/m3)] re- gion (5.2 ϫ 107 km2) is more than twice the area of North America (equal to Ϸ19,000 Rhode Islands) (Fig. 1). Its subsea- Author contributions: S.D., A.J.S., R.P., and T.G.F. designed research; S.D., A.J.S., R.P., T.G.F., floor ecosystem has never before been explored. J.P.F., J.K., L.J.A., D.C.S., D.G., F.H., H.S., and A.M.S. performed research; S.D., A.J.S., R.P., T.G.F., J.P.F., J.K., L.J.A., D.C.S., D.G., F.H., H.S., and A.M.S. analyzed data; and S.D. wrote the paper. Results The authors declare no conflict of interest. This article is a PNAS Direct Submission. Sedimentation and Organic Burial. The cored sediment ranged in SCIENCES Freely available online through the PNAS open access option. age from 0 to 70 Ma and in depth below seafloor from 0 to 9 m ENVIRONMENTAL (Table 1). Total sediment thickness ranges from 1 m (SPG-7) to 1To whom correspondence should be addressed. E-mail: [email protected]. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0811793106 PNAS ͉ July 14, 2009 ͉ vol. 106 ͉ no. 28 ͉ 11651–11656 Downloaded by guest on September 27, 2021 Downloaded by guest on September 27, 2021 11652 Table. 1. Sediment properties and subseafloor (>1.5 mbsf) biogeochemical fluxes ͉ www.pnas.org Organic Organic Organic carbon carbon carbon burial burial Total content at rate at rate at Downward Upward Ϫ Basement water sediment Cored 0Ϫ5 cmbsf Ϸ0Ϫ5 cmbsf Ϸ150 cmbsf O2 flux at NO3 flux Radiolytic H2 ͞ cgi age (16) depth thickness sediment Sedimentation (dry weight (molC/ (molC/ 1.5 mbsf at 1.5 mbsf production ͞ 2 2 2 2 2 doi Site latitude longitude (Ma) (m) (m) (mbsf) rate (cm/kyr) %) cm /yr) cm /yr) (mol/cm /yr) (mol/cm /yr) (mol H2/cm /yr) ͞ 10.1073 SPG-1 Ϫ23°51ЈϪ165°39Ј 100 5697 71 7.79 0.031 0.33 3.6EϪ09 1.6EϪ09 Ϫ2.0EϪ08 6.9EϪ10 1.4EϪ08 SPG-2 Ϫ26°03ЈϪ156°54Ј 100 5127 17 8.20 0.017 0.53 3.2EϪ09 8.7EϪ10 Ϫ6.8EϪ09 3.5EϪ10 3.1EϪ09 ͞ SPG-3 Ϫ27°57ЈϪ148°35Ј 71 4852 5.49 5.49 0.008 0.42 1.2EϪ09 4.4EϪ10 Ϫ4.1EϪ09 5.4EϪ10 8.0EϪ10 pnas.0811793106 SPG-4 Ϫ26°29ЈϪ137°56Ј 33.5 4285 9 7.24 0.028 0.42 4.2EϪ09 1.6EϪ09 Ϫ5.4EϪ09 n.d. 1.6EϪ09 SPG-5 Ϫ28°27ЈϪ131°23Ј 24.1 4221 17 8.05 0.069 0.36 8.8EϪ09 3.8EϪ09 Ϫ7.6EϪ09 n.d. 3.0EϪ09 SPG-6 Ϫ27°55ЈϪ123°10Ј 13.5 3738 15 2.59 0.111 n.d. n.d. 7.0EϪ09 Ϫ2.2EϪ08 n.d. 2.7EϪ09 SPG-7 Ϫ27°44ЈϪ117°37Ј 6.1 3688 1.05 1.05 0.017 0.29 1.7EϪ09 n/a n/a n/a n/a SPG-9 Ϫ38°04ЈϪ133°06Ј 39 4925 20 7.05 0.051 0.38 9.5EϪ09 3.8EϪ09 Ϫ2.8EϪ09 3.0EϪ10 4.5EϪ09 SPG-10 Ϫ39°19ЈϪ139°48Ј 58 5283 21 5.63 0.037 0.56 1.0EϪ08 2.0EϪ09 Ϫ1.2EϪ08 6.0EϪ10 4.8EϪ09 SPG-11 Ϫ41°51ЈϪ153°06Ј 75 5076 67 2.98 0.089 0.51 2.2EϪ08 8.2EϪ09 Ϫ2.4EϪ09 1.6EϪ09 1.6EϪ08 SPG 12 Ϫ45°58ЈϪ163°11Ј 73 5306 130 4.98 0.178 0.34 3.0EϪ08 2.7EϪ08 n/a Ϫ3.1EϪ08 n.d n/a, not applicable; n.d., not determined. Program (ODP) Sites 1225 and 1226 and 3.1 through the near-surface zone in itsinaccessible initial few that million years almost after burial.