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Microbial Ecology of the Dark Ocean Above, At, and Below the Seafloor

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Microbial Ecology of the Dark Ocean Above, At, and Below the Seafloor MICROBIOLOGY AND MOLECULAR BIOLOGY REVIEWS, June 2011, p. 361–422 Vol. 75, No. 2 1092-2172/11/$12.00 doi:10.1128/MMBR.00039-10 Copyright © 2011, American Society for Microbiology. All Rights Reserved. Microbial Ecology of the Dark Ocean above, at, and below the Seafloor† Beth N. Orcutt,1,2 Jason B. Sylvan,2 Nina J. Knab,2 and Katrina J. Edwards2,3* Center for Geomicrobiology, Aarhus University, 8000 Aarhus, Denmark1; Marine Environmental Biology Section, Department of Biological Sciences, University of Southern California, Los Angeles, California 900892; and Department of Earth Sciences, University of Southern California, Los Angeles, California 900893 INTRODUCTION .......................................................................................................................................................362 DARK OCEAN HABITATS—AN OVERVIEW ......................................................................................................362 METABOLIC REACTIONS IN THE DARK OCEAN ..........................................................................................367 Electron Sources .....................................................................................................................................................369 Organic matter....................................................................................................................................................369 Hydrogen..............................................................................................................................................................369 Methane................................................................................................................................................................369 Reduced sulfur compounds ...............................................................................................................................370 Reduced iron compounds...................................................................................................................................370 Ammonium...........................................................................................................................................................370 Other electron donors ........................................................................................................................................371 Electron Sinks .........................................................................................................................................................371 Oxygen..................................................................................................................................................................371 Nitrate and nitrite ..............................................................................................................................................371 Manganese and iron oxides...............................................................................................................................372 Oxidized sulfur compounds (sulfate, sulfite, elemental sulfur, and thiosulfate) ......................................372 Carbon dioxide ....................................................................................................................................................372 Other Microbial Processes in the Dark Ocean ..................................................................................................372 DOMINANT REACTIONS AND MICROORGANISMS IN DARK OCEAN HABITATS...............................372 The Aphotic Pelagic Ocean....................................................................................................................................374 General physical and chemical parameters ....................................................................................................374 Metabolic reactions ............................................................................................................................................374 Microbial distribution and diversity ................................................................................................................375 Marine Sediments...................................................................................................................................................377 General physical and chemical characteristics ..............................................................................................378 Metabolic reactions ............................................................................................................................................378 Microbial distribution and diversity ................................................................................................................382 Oceanic Crust..........................................................................................................................................................384 General physical and chemical characteristics ..............................................................................................384 Metabolic reactions ............................................................................................................................................385 Microbial distribution and diversity ................................................................................................................386 Hydrothermal Vents—Vent Fluids and Hydrothermal Chimneys ...................................................................387 General physical and chemical characteristics ..............................................................................................388 Metabolic reactions ............................................................................................................................................388 Microbial distribution........................................................................................................................................390 Hydrothermal Plumes ............................................................................................................................................391 General physical and chemical characteristics ..............................................................................................391 Metabolic reactions ............................................................................................................................................392 Microbial distribution and diversity ................................................................................................................393 MICROBIAL ECOLOGY OF THE DARK OCEAN..............................................................................................395 Broad Patterns in Prokaryotic Microbial Biogeography...................................................................................395 Taxonomy of Dark Ocean Prokaryotic Microbial Communities......................................................................396 Cultivated Prokaryotes from the Dark Ocean....................................................................................................403 * Corresponding author. Mailing address: Department of Biological Sciences, University of Southern California, 3616 Trousdale Blvd., Los Angeles, CA 90089. Phone: (213) 821-4390. Fax: (213) 740- 8123. E-mail: [email protected]. † Supplemental material for this article may be found at http://mmbr .asm.org/. 361 362 ORCUTT ET AL. MICROBIOL.MOL.BIOL.REV. Microbial Eukaryotes and Viruses in the Dark Ocean .....................................................................................408 MAGNITUDE OF PROKARYOTIC BIOMASS IN THE DARK OCEAN .........................................................408 CONCLUSIONS AND FUTURE DIRECTIONS....................................................................................................409 ACKNOWLEDGMENTS ...........................................................................................................................................410 REFERENCES ............................................................................................................................................................410 INTRODUCTION and, thus, society. Microbes are the principal custodians of the environment, balancing and maintaining Earth’s global biogeo- The majority of the Earth’s habitable environments are chemical cycles. Although researchers have recognized for physically located in environments that do not receive sunlight. many years the importance of studying the dark ocean, our Indeed, the largest potential habitats on Earth are located in understanding of this realm has lagged behind that of its sunlit the ocean, which covers approximately 70% of the Earth’s counterparts in the terrestrial and marine realms due to the surface (Fig. 1). The ocean’s average depth is 4,000 m and difficulty in accessing it, as studies in the dark ocean are both reaches as deep as 11,000 m in the Marianas Trench. Depend- technically challenging and expensive. Despite these obstacles, ing on the quantity of particulate matter in the water, signifi- new generations of researchers and experimental tools have cant levels of sunlight—the driver of photosynthesis—pene- emerged, in the last decade in particular, owing to dedicated trate only a few tens to hundreds of meters (300 m maximum) research programs to explore the dark ocean biosphere. In this into the water. Thus, from a quantitative
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