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This book provides an up-to-date overview of the microbiology, biogeochemistry, and ecology of marine hydrocarbon seeps, a globally occurring habitat for specialized microorganisms and invertebrates that depend on natural hydrocarbon seepage as a food and energy source. Prominent examples include the briny hydrocarbon seeps and mud volcanoes on the continental slope of the Gulf of Mexico and in the Mediterranean, the hydrothermally heated hydrocarbon seeps at Guaymas Basin (Mexico), and the oil and gas seeps off the coast of California and in the Gulf of Mexico. Featuring topical chapters by leading researchers in the area, the book describes geological settings, chemical characteristics of hydrocarbon seepage, hydrocarbon-dependent microbial populations, and ecosystem structure and trophic networks at hydrocarbon seeps. Further, it also discusses applied aspects such as bioremediation potential (oil-degrading microorganisms).



1. Microbial Communities and Metabolisms at Hydrocarbon Seeps

Hydrocarbon seeps are common features of all oceans and are located mainly along the continental margins (Fig. 1). Seeps are locally restricted, yet highly productive hotspots of biodiversity that experience very different environmental conditions and energy regimes than the surrounding deep-sea sediments. Hydrocarbon seep ecosystems are mostly fueled by methane. Occasionally, seeps are found that emit the short-chain hydrocarbons ethane, propane or butane, and even oil and asphalt seeps have been described. Seep ecosystems therefore comprise ecological niches and microbial clades that are distinct from those found in deep-sea sediments, which are not fuelled by methane and other hydrocarbons. This chapter provides an overview of the communities thriving at marine hydrocarbon seeps and the microbial metabolisms that create these oases of life (with references to other chapters in this book). It highlights the current knowledge of the diversity and biogeography of seep microbial communities and presents possible mechanisms governing their community assembly.
S. Emil Ruff

2. Anaerobic Hydrocarbon-Degrading Sulfate-Reducing Bacteria at Marine Gas and Oil Seeps

Microorganisms are key players in our biosphere because of their ability to degrade various organic compounds including a wide range of hydrocarbons. At hydrocarbon seeps, microorganisms with the ability to utilize diverse hydrocarbons (such as methane, short- and long-chain alkanes,  or aromatic hydrocarbons) as carbon and electron source are significantly influencing biogeochemical cycles. Marine hydrocarbon seep sediments are hot spots for microbial activity, particularly for sulfate-reducing bacteria that show elevated respiration rates at these sites. At some seeps, more than 90% of sulfate reduction is potentially coupled to non-methane hydrocarbon oxidation, emphasizing the environmental relevance of these microorganisms and the need to identify key players in situ. Several hydrocarbon-degrading sulfate-reducing bacteria were enriched or isolated from marine sediments, however, in situ active microorganisms were to a large extent represented by uncultivated taxa. Here, we provide an overview of the current understanding of non-methane hydrocarbon-degrading sulfate-reducing bacteria at marine hydrocarbon seeps, including their in situ distribution, abundance, and activity.
Sara Kleindienst, Katrin Knittel

3. Guaymas Basin, a Hydrothermal Hydrocarbon Seep Ecosystem

The hydrothermal sediments of Guaymas Basin in the Gulf of California combine several microbial ecosystems. Since Guaymas Basin is an active hydrothermal spreading center, it sustains chemosynthetic microbial communities with inorganic electron donors such as sulfide, hydrogen, ammonia, and reduced metals within steep thermal gradients of hydrothermal sediments and chimneys. At the same time, Guaymas Basin is an organic-rich continental margin site, where high sedimentation rates resulting from high phytoplankton productivity and terrestrial runoff produce organic-rich sediments that support abundant heterotrophic microbial populations. Most interesting in the context of hydrocarbon seepage, hydrothermal heating of organic-rich sediments creates hot hydrocarbon seeps in Guaymas Basin. Aliphatic and aromatic hydrocarbons are generated under high temperature and pressure in the subsurface, and migrate to the sediment surface where they are assimilated and oxidized by hydrocarbon-oxidizing bacteria and archaea. This complex habitat mosaic results in unusually diverse microbial communities with new phylogenetic lineages and surprising physiological capabilities. This chapter provides some background and highlights recent microbial discoveries in Guaymas Basin.
Andreas Teske

4. The Gulf of Mexico: An Introductory Survey of a Seep-Dominated Seafloor Landscape

The Gulf of Mexico is home to numerous hydrocarbon seeps, brine lakes and mud volcanoes that provide habitats for hydrocarbon-dependent microbial communities; trophic linkages connect these hydrocarbon microbiota with benthic marine invertebrates and provide the foundation of complex benthic ecosystems that are ultimately sustained by hydrocarbon seepage. Sampling and reconnaissance by submersibles provide a first impression of the diversity of Gulf of Mexico hydrocarbon seeps, paving the way for further discoveries. This chapter provides on overview of selected hydrocarbon and brine seeps on the northern slope of the Gulf of Mexico that were visited and explored during two month-long cruises with research submersible Alvin and R/V Atlantis in 2010 and 2014.
Andreas Teske, Samantha B. Joye

5. Benthic Deep-Sea Life Associated with Asphaltic Hydrocarbon Emissions in the Southern Gulf of Mexico

At the Campeche Knolls in the southern Gulf of Mexico large-scale hydrocarbon emissions are associated with numerous salt tectonic structures. A notable feature of this area is the expulsion of highly viscous heavy oils, also referred to as asphalts, which form lava-like flows on the seafloor. These oil and asphalt seeps have been detected via satellite imaging of oil slicks at the ocean surface and by acoustically-detected gas emission sites in the water column. Here, we describe the type locality ‘Chapopote’ (Aztec word for tar) where the expelled hydrocarbons provide an energy source for microorganisms and subsequently the deep-sea fauna. In deeper asphalt layers and sediment, 16S rRNA gene sequences of archaea affiliated with Methanosaeta and bacteria of the Syntrophaceae were detected. Together with the observed light methane isotope values this indicates biogenic methanogenesis from aliphatic hydrocarbons at these depths. In shallow oil-soaked sediments gene sequences of hydrocarbon-degrading sulfate-reducing Deltaproteobacteria were found. These sediments showed high sulfate reduction but only minor methane oxidation rates. Asphalts and oil-soaked sediments freshly exposed to the surface were densely covered by microbial mats, signaling high metabolic activity. The surface microbial communities were dominated by diverse Gammaproteobacteria that likely oxidized hydrocarbons and reduced sulfur compounds. Surface asphalts were colonized by tube worms, mussels and sponges that host bacterial symbionts. In addition, grazing invertebrates such as sea cucumbers, shrimps, and crabs evidently fed on the microbial mats. This close link between the microbial and macro-benthic life demonstrates an efficient energy transfer to higher trophic levels from microbial hydrocarbon oxidation at the base of this unique asphalt-hosted ecosystem.
Gunter Wegener, Katrin Knittel, Gerhard Bohrmann, Florence Schubotz

6. Archaea in Mediterranean Sea Cold Seep Sediments and Brine Pools

Cold seeps host intense and complex biochemical processes, in particular methane and sulfur cycling. Microorganisms are key players in these habitats, producing or oxidizing methane, and reducing sulfate. Mediterranean cold seep mud volcanoes are natural laboratories allowing to study how reducing fluids from different volcanoes with distinct connections to the marine subsurface, influence composition and activities of benthic microbial communities. Methane-producing and-oxidizing archaea were detected in mud volcanoes associated with different seepage intensities, in hypersaline brine-impacted sediments, as well as in pockmark structures. Because the muds and fluids expelled from the center of the mud volcanoes ascend from deep sources, they could be windows into the deep biosphere, allowing a glimpse into the diversity of communities surviving in the deep subsurface.
Cassandre S. Lazar

7. The Microbial Communities of the East Mediterranean Sea Mud Volcanoes and Pockmarks

Mud volcanoes and pockmarks are sites which methane and other gases seep out towards the overlying water. This supply and the microbiologically-mediated processes of these cold seeps can be the basis of unique microbial habitats. Although mud volcanoes and pockmarks vary in the seepage rate and chemical composition of their outflows, the communities found in geographically adjacent systems seem to harbor comparable microbial communities. For the East Mediterranean Sea, only sporadic data exist on its major mud volcanoes and pockmarks collected through a few oceanographic cruises; however, further the knowledge of these systems should be gained by microbiological and sequence-based investigations.
Konstantinos Ar. Kormas, Alexandra Meziti

8. Large Sulfur-Oxidizing Bacteria at Gulf of Mexico Hydrocarbon Seeps

Large sulfide-oxidizing bacteria occur as visually conspicuous microbial mats in a wide range of sedimentary habitats, including estuarine and coastal marine sediments, and deep-sea vents and seeps. The microbial mats spread on the surface of sulfide-rich sediments, thus intercepting and oxidizing sulfide that diffuses upwards from the underlying sulfate reduction zone, or, that reaches the surface by advection of reduced fluids. The first intermediate of bacterial sulfide oxidation, elemental sulfur, is stored within the cytoplasm as globules, and serves as energy reserve. Large sulfide oxidizers have a wide metabolic repertoire, including autotrophic carbon fixation, sulfide and sulfur oxidation to sulfuric acid, nitrate reduction to ammonia or nitrogen gas, as well as polyphosphate storage and release causing local phosphate supersaturation and precipitation. Large sulfur-oxidizing bacteria are widespread at hydrocarbon seeps in the Gulf of Mexico, where numerous types with different morphology, phylogenetic affiliation, and physiology have been documented. In this chapter, we provide an overview of large sulfur-oxidizing bacteria in the Gulf of Mexico. We also incorporate previously unpublished sequencing data for selected filaments, and include recent observations of new morphological variants, including one that resembles sheathed marine Thioploca spp., but which shows a distinguished, unique branching morphology.
Andreas Teske, Verena Carvalho

9. Growth Patterns of Giant Deep Sea Beggiatoaceae from a Guaymas Basin Vent Site

We studied the growth of giant filamentous sulfur oxidizing bacteria of the family Beggiatoaceae collected from a hydrothermal seep area in the Guaymas Basin. We measured the incorporation of 14C-bicarbonate tracer into individual filaments using a microimager that allows quantitative determination of the distribution of radioisotopes with 20 µm resolution. Filaments incorporated label along their entire length; thus growth occurred uniformly throughout these whole filaments and not only at their tips. Uptake of 14C-bicarbonate was strongly stimulated by reducing the pH from 8.2, the value near the sediment surface, to 7.05, as found within 1–2 mm below the surface; the presence of oxygen or sulfide had no effect. Thus, Beggiatoaceae strongly prefer assimilation of CO2 over other DIC species. In consequence, migration of these motile filaments into deeper sediments, where sharply decreasing pH increases the availability of CO2, will favor cell growth. Genomic evidence was found for periplasmic carbonic anhydrases, indicative of the carbon concentration mechanism.
Dirk de Beer, Timothy Ferdelman, Barbara J. MacGregor, Andreas Teske, Charles A. Schutte

10. Uncovering Microbial Hydrocarbon Degradation Processes: The Promise of Stable Isotope Probing

Traditional microbiological methods for the identification of microorganisms after they have been isolated in pure culture have revealed key players in the degradation of hydrocarbons. But have we identified them all? The conspicuous enrichment of an uncultured Oceanospirillales in a sub-surface hydrocarbon plume during the Deepwater Horizon oil spill is one of many examples highlighting that we are not there yet in this respect. Culture-dependent methods typically miss identifying 99% of microorganisms originating from environmental samples, and are on their own ineffective in resolving the diversity and function of natural microbial communities. Stable isotope probing (SIP) is a technique used to identify a target group of microorganisms which can actively metabolize a specific substrate in an environmental sample and, thus, under in situ-like conditions. The technique involves incubating an environmental sample with an isotopically-labeled (e.g., 13C, or 15N) substrate and allowing the label to become incorporated into the biomass (e.g. DNA, RNA, protein, PLFAs) of those microorganisms capable of metabolizing the substrate. The labeled biomolecules are then isolated and analyzed to identify the organisms that actively incorporated the isotope label. SIP based on DNA or RNA are quite similar methods by the nature of their execution, albeit with subtle differences. The technique has a high phylogenetic resolution, and has provided many new insights to this day concerning microbial biodegradation of specific compounds and putative interrelationships of microbial activities with biogeochemical processes. This chapter provides an overview on the methodology, its caveats, and gives examples of applications for exploring the diversity of microbial hydrocarbon degraders in seep and other benthic habitats.
Tony Gutierrez, Sara Kleindienst
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