Half of the microbial cells in the Earth's oceans are found in sediments. Many of these cells are members of the Archaea, single-celled prokaryotes in a domain of life separate from Bacteria and Eukaryota. However, most of these archaea lack cultured representatives, leaving their physiologies and placement on the tree of life uncertain. Here we show that the uncultured miscellaneous crenarchaeotal group (MCG) and marine benthic group-D (MBG-D) are among the most numerous archaea in the marine sub-sea floor. Single-cell genomic sequencing of one cell of MCG and three cells of MBG-D indicated that they form new branches basal to the archaeal phyla Thaumarchaeota and Aigarchaeota, for MCG, and the order Thermoplasmatales, for MBG-D. All four cells encoded extracellular protein-degrading enzymes such as gingipain and clostripain that are known to be effective in environments chemically similar to marine sediments. Furthermore, we found these two types of peptidase to be abundant and active in marine sediments, indicating that uncultured archaea may have a previously undiscovered role in protein remineralization in anoxic marine sediments.
During the Deepwater Horizon oil well blowout in the Gulf of Mexico, the application of 7 million liters of chemical dispersants aimed to stimulate microbial crude oil degradation by increasing the bioavailability of oil compounds. However, the effects of dispersants on oil biodegradation rates are debated. In laboratory experiments, we simulated environmental conditions comparable to the hydrocarbon-rich, 1,100 m deep plume that formed during the Deepwater Horizon discharge. The presence of dispersant significantly altered the microbial community composition through selection for potential dispersant-degrading Colwellia, which also bloomed in situ in Gulf deep waters during the discharge. In contrast, oil addition to deepwater samples in the absence of dispersant stimulated growth of natural hydrocarbon-degrading Marinobacter. In these deepwater microcosm experiments, dispersants did not enhance heterotrophic microbial activity or hydrocarbon oxidation rates. An experiment with surface seawater from an anthropogenically derived oil slick corroborated the deepwater microcosm results as inhibition of hydrocarbon turnover was observed in the presence of dispersants, suggesting that the microcosm findings are broadly applicable across marine habitats. Extrapolating this comprehensive dataset to real world scenarios questions whether dispersants stimulate microbial oil degradation in deep ocean waters and instead highlights that dispersants can exert a negative effect on microbial hydrocarbon degradation rates.
Dispersants are globally and routinely applied as an emergency response to oil spills in marine ecosystems with the goal of chemically enhancing the dissolution of oil into water, which is assumed to stimulate microbially mediated oil biodegradation. However, little is known about how dispersants affect the composition of microbial communities or their biodegradation activities. The published findings are controversial, probably owing to variations in laboratory methods, the selected model organisms and the chemistry of different dispersant-oil mixtures. Here, we argue that an in-depth assessment of the impacts of dispersants on microorganisms is needed to evaluate the planning and use of dispersants during future responses to oil spills.
The Deepwater Horizon (DWH) oil well blowout generated an enormous plume of dispersed hydrocarbons that substantially altered the Gulf of Mexico's deep-sea microbial community. A significant enrichment of distinct microbial populations was observed, yet, little is known about the abundance and richness of specific microbial ecotypes involved in gas, oil and dispersant biodegradation in the wake of oil spills. Here, we document a previously unrecognized diversity of closely related taxa affiliating with Cycloclasticus, Colwellia and Oceanospirillaceae and describe their spatio-temporal distribution in the Gulf's deepwater, in close proximity to the discharge site and at increasing distance from it, before, during and after the discharge. A highly sensitive, computational method (oligotyping) applied to a data set generated from 454-tag pyrosequencing of bacterial 16S ribosomal RNA gene V4-V6 regions, enabled the detection of population dynamics at the sub-operational taxonomic unit level (0.2% sequence similarity). The biogeochemical signature of the deep-sea samples was assessed via total cell counts, concentrations of short-chain alkanes (C 1 -C 5 ), nutrients, (colored) dissolved organic and inorganic carbon, as well as methane oxidation rates. Statistical analysis elucidated environmental factors that shaped ecologically relevant dynamics of oligotypes, which likely represent distinct ecotypes. Major hydrocarbon degraders, adapted to the slow-diffusive natural hydrocarbon seepage in the Gulf of Mexico, appeared unable to cope with the conditions encountered during the DWH spill or were outcompeted. In contrast, diverse, rare taxa increased rapidly in abundance, underscoring the importance of specialized subpopulations and potential ecotypes during massive deep-sea oil discharges and perhaps other large-scale perturbations.
Iron is the most abundant redox-active metal in the Earth's crust. The one electron transfer between the two most common redox states, Fe(II) and Fe(III), plays a role in a huge range of environmental processes from mineral formation and dissolution to contaminant remediation and global biogeochemical cycling. It has been appreciated for more than a century that microorganisms can harness the energy of this Fe redox transformation for their metabolic benefit. However, this is most widely understood for anaerobic Fe(III)-reducing or aerobic and microaerophilic Fe(II)-oxidizing bacteria. Only in the past few decades have we come to appreciate that bacteria also play a role in the anaerobic oxidation of ferrous iron, Fe(II), and thus can act to form Fe(III) minerals in anoxic settings. Since this discovery, our understanding of the ecology of these organisms, their mechanisms of Fe(II) oxidation and their role in environmental processes has been increasing rapidly. In this article, we bring these new discoveries together to review the current knowledge on these environmentally important bacteria, and reveal knowledge gaps for future research.
Biogeochemical and microbiological data indicate that the anaerobic oxidation of non-methane hydrocarbons by sulfate-reducing bacteria (SRB) has an important role in carbon and sulfur cycling at marine seeps. Yet, little is known about the bacterial hydrocarbon degraders active in situ. Here, we provide the link between previous biogeochemical measurements and the cultivation of degraders by direct identification of SRB responsible for butane and dodecane degradation in complex on-site microbiota. Two contrasting seep sediments from Mediterranean Amon mud volcano and Guaymas Basin (Gulf of California) were incubated with 13 C-labeled butane or dodecane under sulfate-reducing conditions and analyzed via complementary stable isotope probing (SIP) techniques. Using DNA-and rRNA-SIP, we identified four specialized clades of alkane oxidizers within Desulfobacteraceae to be distinctively active in oxidation of short-and long-chain alkanes. All clades belong to the Desulfosarcina/Desulfococcus (DSS) clade, substantiating the crucial role of these bacteria in anaerobic hydrocarbon degradation at marine seeps. The identification of key enzymes of anaerobic alkane degradation, subsequent b-oxidation and the reverse Wood-Ljungdahl pathway for complete substrate oxidation by protein-SIP further corroborated the importance of the DSS clade and indicated that biochemical pathways, analog to those discovered in the laboratory, are of great relevance for natural settings. The high diversity within identified subclades together with their capability to initiate alkane degradation and growth within days to weeks after substrate amendment suggest an overlooked potential of marine benthic microbiota to react to natural changes in seepage, as well as to massive hydrocarbon input, for example, as encountered during anthropogenic oil spills.
Summary Marine gas and hydrocarbon seeps are hot spots of sulfate reduction which is fuelled by methane, other short‐chain alkanes or a complex mixture of hydrocarbons. In this study, we investigated the global distribution and abundance of sulfate‐reducing bacteria (SRB) in eight gas and hydrocarbon seeps by catalysed reporter deposition fluorescence in situ hybridization (CARD‐FISH). The majority of Deltaproteobacteria were assigned to specific SRB groups, i.e. 83 ± 14% at gas seeps and 61 ± 35% at hydrocarbon seeps, indicating that the probe set used was sufficient for classification of marine SRB. Statistical analysis showed that SRB abundance and distribution were significantly influenced by habitat type and sediment depth. Members of the Desulfosarcina/Desulfococcus (DSS) clade strongly dominated all sites. Our data indicated the presence of many diverse and highly specialized DSS species of low abundance rather than a single abundant subgroup. In addition, SEEP‐SRB2, an uncultured deep‐branching deltaproteobacterial group, was ubiquitously found in high abundances at all sites. SEEP‐SRB2 members occurred either in a novel association with methanotrophic archaea in shell‐type ANME‐2/SEEP‐SRB2 consortia, in association with ANME‐1 archaea in Black Sea microbial mats or as single cells. Two other uncultured groups, SEEP‐SRB3 and SEEP‐SRB4, were preferentially detected in surface sediments from mud volcanoes.
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