Microbial ecology of the dark ocean above, at, and below the seafloor

Abstract

The majority of life on Earth--notably, microbial life--occurs in places that do not receive sunlight, with the habitats of the oceans being the largest of these reservoirs. Sunlight penetrates only a few tens to hundreds of meters into the ocean, resulting in large-scale microbial ecosystems that function in the dark. Our knowledge of microbial processes in the dark ocean-the aphotic pelagic ocean, sediments, oceanic crust, hydrothermal vents, etc.-has increased substantially in recent decades. Studies that try to decipher the activity of microorganisms in the dark ocean, where we cannot easily observe them, are yielding paradigm-shifting discoveries that are fundamentally changing our understanding of the role of the dark ocean in the global Earth system and its biogeochemical cycles. New generations of researchers and experimental tools have emerged, in the last decade in particular, owing to dedicated research programs to explore the dark ocean biosphere. This review focuses on our current understanding of microbiology in the dark ocean, outlining salient features of various habitats and discussing known and still unexplored types of microbial metabolism and their consequences in global biogeochemical cycling. We also focus on patterns of microbial diversity in the dark ocean and on processes and communities that are characteristic of the different habitats.

Fig. 1.

Global maps of ocean water depth (A) and sediment thickness (B). The water depth scale is from less than 500 m (red) to 6,000+ m (purple). The sediment thickness scale is from 0 m (purple) to >2,000 m (red). Maps were created using GeoMapApp (www.geomapapp.org [474a]).

Fig. 2.

Schematics depicting a stylized cross section of dark ocean habitats (top; adapted from reference by permission of Macmillan Publishers Ltd., copyright 2007) and representations of sediment biogeochemical zonation (bottom). Note that the upper panel is not drawn to scale. In the lower panel, dominant electron acceptors in the various sediment habitats are indicated by vertical depth into sediment (note the logarithmic sediment depth scale). The relative quantity of organic matter deposited in each sediment type and the scale of metabolic rates in sediment are indicated by the grayscale bar, with dark shades indicating higher rates.

Fig. 3.

Photographs of representative sediment habitats in the dark ocean. (A) Surficial sediment from a methane seep in the Black Sea. (B) Mats of sulfur-oxidizing Beggiatoa on the sediment surface of the Northwestern Black Sea shelf. (C) Pacific Ocean abyssal plain sediment surface. (D) Compilation of deep sediment layers cored at Hole 1231 (Peru Margin) during Ocean Drilling Program Expedition 201. (Panel A courtesy of T. Treude, IfM Geomar, Kiel, Germany; panel B courtesy of K. Hissmann, JAGO-Team/IfM Geomar, Kiel, Germany; panel C was reprinted with permission of the Monterey Bay Aquarium Research Institute [courtesy of Ken Smith].)

Fig. 4.

Photographs of representative marine sediment seep and whale fall habitats. (A) Cross section of a methane-oxidizing microbial mat from a carbonate chimney formed at the seafloor in the anoxic Black Sea. (B) Whale fall ecosystem at the seafloor in the Pacific Ocean. (C) Barite chimney at a mud volcano in the Gulf of Mexico. (D) Close-up image of orange and white Beggiatoa bacteria overlying sulfidic sediment at a Gulf of Mexico cold seep. (Panel A courtesy of T. Treude, IfM Geomar, Kiel, Germany; panel B courtesy of Craig Smith, University of Hawaii; panels C and D courtesy of I. R. MacDonald, Florida State University.)

Fig. 5.

Photographs of representative oceanic crust and hydrothermal vent habitats in the dark ocean. (A) Nine-meter-tall extinct hydrothermal sulfide chimney off axis of the East Pacific Rise. (B) Active and inactive hydrothermal chimneys at Tu'I Malila vent field, Valu Fa Ridge. (C) Riftia pachyptila tube worms at East Pacific Rise. (D) Piece of altered basaltic oceanic crust from the Loihi Seamount being picked up by the ROV Jason submersible manipulator. (E) Young basalt flows overlaying older basalt flows at the East Pacific Rise. (F) White smoker hydrothermal chimney at Mariner vent field, Valu Fa Ridge. (G) Black smoker hydrothermal chimney being sampled by the submersible arm of DSV Alvin at the Juan de Fuca Ridge. (H) Sixty-meter-tall carbonate chimney at the Lost City hydrothermal vent field. (Panels A, D, and G courtesy of Woods Hole Oceanographic Institution; panels B, C, and F taken with the NDSF ROV Jason II, operated by the Woods Hole Oceanographic Institution, courtesy of C. Fisher [PSU] and the National Science Foundation Ridge 2000 program; panel E courtesy of Adam Soule, Woods Hole Oceanographic Institution; panel H courtesy of Deb Kelly.)

Fig. 6.

Photographs of commonly used sampling tools for dark ocean research. (A) ROV Jason II, Woods Hole Oceanographic Institution. (B) ROV/AUV Nereus, Woods Hole Oceanographic Institution. (C) Rosette of Niskin water sampling bottles and a CTD (conductivity, temperature, depth) sensor package. (D) Multicoring device for collecting surficial sediments. (E) Scientific ocean drilling vessel RV JOIDES Resolution for collecting deep sediments and hard rock. (F) View from the inside of the Johnson SeaLink submersible, Harbor Branch Oceanographic Institute, working at a cold seep in the Gulf of Mexico. (G) Launch of the Johnson SeaLink submersible, Harbor Branch Oceanographic Institute. (Panels A and C courtesy of J. Sylvan; panel B courtesy of Robert Elder, copyright the Woods Hole Oceanographic Institution; panels D and G courtesy of B. Orcutt; panel E courtesy of William Crawford, IODP/TAMU; panel F courtesy of I. R. MacDonald.)

Fig. 7.

Composition of bacterial communities in various dark ocean habitats based on the percentages of different bacterial phyla documented in clone libraries of the 16S rRNA gene containing nearly full-length sequences. Each line represents a different sample set from one environment. The numbers after the references indicate the numbers of sequences in the sample clone library. Samples are grouped by habitat type, as indicated in the far left margin. Abbreviations and acronyms: pel., pelagic; ODP, Ocean Drilling Program; IODP, Integrated Ocean Drilling Program; carb., carbonate; HT, hydrothermal; HI, Hawaii; JdF, Juan de Fuca Ridge; EPR, East Pacific Rise; chalco., chalcopyrite; BS, black smoker; WS, white smoker; HV, hydrothermal vent; LCHF, Lost City hydrothermal field; ALOHA, Station ALOHA, Pacific Ocean, north of Hawaii; srfc, surface; SAGM, South African gold mine; GN, Guerrero Negro, Baja, CA. References correspond to reference numbers 60, 64, 88a, 93, 124, 166, 186, 196a, 202, 213, 215, 219a, 224, 232, 240, 242, 289, 290, 293, 307a, 335a, 346, 346a, 354, 357a, 372, 386, 392, 397, 400, 407, 409, 414, 424, 442, 443, 444, 447, 449, 456, 467, 476, 479, 499a, 506a, 518, 520, 535, 544, 566, 580a, 581, 590, 591, and 592.

Fig. 8.

Composition of archaeal communities in various dark ocean habitats based on the percentages of different archaeal phyla documented in clone libraries of the 16S rRNA gene containing nearly full-length sequences. Each line represents a different sample set from one environment. Samples are grouped by habitat type, as indicated in the far left margin. Abbreviations and acronyms are the same as in Fig. 7, with the addition of LIS for Long Island Sound. See reference 545 for more information on archaeal group naming conventions. References correspond to reference numbers 60, 93, 124, 135, 163, 166, 186, 195, 202, 206, 213, 224, 232, 240, 242, 289, 290, 346a, 354, 392, 397, 406a, 407, 408, 409, 417, 424, 436, 442, 443, 467, 469, 473, 475, 476, 493, 494, 506a, 509, 520, 524, 535, 544, 581, 585, and 592.

Fig. 9.

Phylogenetic tree of Alphaproteobacteria groups commonly found in dark ocean habitats. The most common groups are indicated with bold text. Colored symbols indicate which habitats are represented in the common groups.

Fig. 10.

Phylogenetic tree of Gammaproteobacteria groups commonly found in dark ocean habitats. The most common groups are indicated with bold text. Colored symbols indicate which habitats are represented in the common groups.

Fig. 11.

Phylogenetic tree of Deltaproteobacteria groups commonly found in dark ocean habitats. The most common groups are indicated with bold text. Colored symbols indicate which habitats are represented in the common groups.

Fig. 12.

Phylogenetic tree of Epsilonproteobacteria groups commonly found in dark ocean habitats. The most common groups are indicated with bold text. Colored symbols indicate which habitats are represented in the common groups.

Fig. 13.

Phylogenetic tree of Archaea groups commonly found in dark ocean habitats. The most common groups are indicated with bold text. Colored symbols indicate which habitats are represented in the common groups.