SUMMARY 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.
Oceanic lithosphere exposed at the sea floor undergoes seawater-rock alteration reactions involving the oxidation and hydration of glassy basalt. Basalt alteration reactions are theoretically capable of supplying sufficient energy for chemolithoautotrophic growth. Such reactions have been shown to generate microbial biomass in the laboratory, but field-based support for the existence of microbes that are supported by basalt alteration is lacking. Here, using quantitative polymerase chain reaction, in situ hybridization and microscopy, we demonstrate that prokaryotic cell abundances on seafloor-exposed basalts are 3-4 orders of magnitude greater than in overlying deep sea water. Phylogenetic analyses of basaltic lavas from the East Pacific Rise (9 degrees N) and around Hawaii reveal that the basalt-hosted biosphere harbours high bacterial community richness and that community membership is shared between these sites. We hypothesize that alteration reactions fuel chemolithoautotrophic microorganisms, which constitute a trophic base of the basalt habitat, with important implications for deep-sea carbon cycling and chemical exchange between basalt and sea water.
Bacterioplankton of the marine Roseobacter clade have genomes that reflect a dynamic environment and diverse interactions with marine plankton. Comparative genome sequence analysis of three cultured representatives suggests that cellular requirements for nitrogen are largely provided by regenerated ammonium and organic compounds (polyamines, allophanate, and urea), while typical sources of carbon include amino acids, glyoxylate, and aromatic metabolites. An unexpectedly large number of genes are predicted to encode proteins involved in the production, degradation, and efflux of toxins and metabolites. A mechanism likely involved in cell-to-cell DNA or protein transfer was also discovered: vir-related genes encoding a type IV secretion system typical of bacterial pathogens. These suggest a potential for interacting with neighboring cells and impacting the routing of organic matter into the microbial loop. Genes shared among the three roseobacters and also common in nine draft Roseobacter genomes include those for carbon monoxide oxidation, dimethylsulfoniopropionate demethylation, and aromatic compound degradation. Genes shared with other cultured marine bacteria include those for utilizing sodium gradients, transport and metabolism of sulfate, and osmoregulation.In surface waters of the open ocean, 1 in 10 bacterial cells is a member of the Roseobacter group (17). In coastal waters, the number of Roseobacter cells increases to 1 in 5 (11, 19). Despite their obvious ecological success, however, roseobacters do not fit the stereotype of a small, metabolically conservative, "oligotrophic" bacterium (8, 18). Instead, they are large (0.08 m 3 ) (38), easily cultured (19), and respond readily to increased substrate availability (7). Analysis of the first Roseobacter genome sequence, that of Silicibacter pomeroyi, revealed a fairly large genome (4.5 Mb) housing abundant and diverse transporters, complex regulatory systems, and multiple pathways for acquiring carbon and energy in seawater. Roseobacters thus appear to be quite versatile from metabolic and ecological standpoints (43), with an assortment of strategies for obtaining carbon and nutrients and, directly or indirectly, affecting the biogeochemical status of seawater.The availability of two additional closed genome sequences of cultured roseobacters provides the opportunity for an ecologically based analysis of the genetic capabilities of this bacterial taxon. The three organisms are assumed to have different niches in the surface ocean based on the conditions of their isolation: S. pomeroyi is a free-living heterotrophic bacterioplankter obtained from coastal seawater (43), congener Silicibacter sp. strain TM1040 (96% 16S rRNA sequence identity to S. pomeroyi [ Fig. 1]) is an associate of the marine dinoflagellate Pfiesteria piscicida (1, 40), and Jannaschia sp. strain CCS1 (with 94% 16S rRNA sequence identity to the two Silicibacter species) represents a recently discovered class of marine aerobic bacteriochlorophyll a-based phototrophs (4). Our comparative an...
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