Sairah Y. Malkin

Chemical dispersants can suppress the activity of natural oil-degrading microorganisms

Significance Oil spills are a significant source of hydrocarbon inputs into the ocean. In response to oil spills, chemical dispersants are applied to the oil-contaminated seawater to disperse surface slicks into smaller droplets that are presumed to be more bioavailable to microorganisms. We provide evidence that chemical dispersants applied to either deep water or surface water from the Gulf of Mexico did not stimulate oil biodegradation. Direct measurement of alkane and aromatic hydrocarbon oxidation rates revealed either suppression or no stimulation of oil biodegradation in the presence of dispersants. However, dispersants affected microbial community composition and enriched bacterial populations with the ability to use dispersant-derived compounds as growth substrates, while oil-alone amendments enriched for natural hydrocarbon degraders. 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.

Natural occurrence of microbial sulphur oxidation by long-range electron transport in the seafloor

Recently, a novel mode of sulphur oxidation was described in marine sediments, in which sulphide oxidation in deeper anoxic layers was electrically coupled to oxygen reduction at the sediment surface. Subsequent experimental evidence identified that long filamentous bacteria belonging to the family Desulfobulbaceae likely mediated the electron transport across the centimetre-scale distances. Such long-range electron transfer challenges some long-held views in microbial ecology and could have profound implications for sulphur cycling in marine sediments. But, so far, this process of electrogenic sulphur oxidation has been documented only in laboratory experiments and so its imprint on the seafloor remains unknown. Here we show that the geochemical signature of electrogenic sulphur oxidation occurs in a variety of coastal sediment environments, including a salt marsh, a seasonally hypoxic basin, and a subtidal coastal mud plain. In all cases, electrogenic sulphur oxidation was detected together with an abundance of Desulfobulbaceae filaments. Complementary laboratory experiments in intertidal sands demonstrated that mechanical disturbance by bioturbating fauna destroys the electrogenic sulphur oxidation signal. A survey of published geochemical data and 16S rRNA gene sequences identified that electrogenic sulphide oxidation is likely present in a variety of marine sediments with high sulphide generation and restricted bioturbation, such as mangrove swamps, aquaculture areas, seasonally hypoxic basins, cold sulphide seeps and possibly hydrothermal vent environments. This study shows for the first time that electrogenic sulphur oxidation occurs in a wide range of marine sediments and that bioturbation may exert a dominant control on its natural distribution.

Microbial carbon metabolism associated with electrogenic sulphur oxidation in coastal sediments

Recently, a novel electrogenic type of sulphur oxidation was documented in marine sediments, whereby filamentous cable bacteria (Desulfobulbaceae) are mediating electron transport over cm-scale distances. These cable bacteria are capable of developing an extensive network within days, implying a highly efficient carbon acquisition strategy. Presently, the carbon metabolism of cable bacteria is unknown, and hence we adopted a multidisciplinary approach to study the carbon substrate utilization of both cable bacteria and associated microbial community in sediment incubations. Fluorescence in situ hybridization showed rapid downward growth of cable bacteria, concomitant with high rates of electrogenic sulphur oxidation, as quantified by microelectrode profiling. We studied heterotrophy and autotrophy by following 13C-propionate and -bicarbonate incorporation into bacterial fatty acids. This biomarker analysis showed that propionate uptake was limited to fatty acid signatures typical for the genus Desulfobulbus. The nanoscale secondary ion mass spectrometry analysis confirmed heterotrophic rather than autotrophic growth of cable bacteria. Still, high bicarbonate uptake was observed in concert with the development of cable bacteria. Clone libraries of 16S complementary DNA showed numerous sequences associated to chemoautotrophic sulphur-oxidizing Epsilon- and Gammaproteobacteria, whereas 13C-bicarbonate biomarker labelling suggested that these sulphur-oxidizing bacteria were active far below the oxygen penetration. A targeted manipulation experiment demonstrated that chemoautotrophic carbon fixation was tightly linked to the heterotrophic activity of the cable bacteria down to cm depth. Overall, the results suggest that electrogenic sulphur oxidation is performed by a microbial consortium, consisting of chemoorganotrophic cable bacteria and chemolithoautotrophic Epsilon- and Gammaproteobacteria. The metabolic linkage between these two groups is presently unknown and needs further study.

Cable bacteria generate a firewall against euxinia in seasonally hypoxic basins

Significance Seasonal hypoxia is increasing in coastal areas worldwide, as more nutrients are delivered to the coastal ocean and water temperatures are rising due to climate change. Hypoxia reaches a particularly harmful stage when sulfide, which is highly toxic for marine life, is released to the bottom water. Here, we document a natural microbial mechanism that counteracts the release of free sulfide, thus preventing the most adverse stage of seasonal hypoxia. Electricity-generating cable bacteria produce a large pool of oxidized sedimentary iron minerals, which efficiently bind free sulfide. As cable bacteria are likely abundant in many seasonally hypoxic basins worldwide, their “firewall” mechanism may be widespread. Seasonal oxygen depletion (hypoxia) in coastal bottom waters can lead to the release and persistence of free sulfide (euxinia), which is highly detrimental to marine life. Although coastal hypoxia is relatively common, reports of euxinia are less frequent, which suggests that certain environmental controls can delay the onset of euxinia. However, these controls and their prevalence are poorly understood. Here we present field observations from a seasonally hypoxic marine basin (Grevelingen, The Netherlands), which suggest that the activity of cable bacteria, a recently discovered group of sulfur-oxidizing microorganisms inducing long-distance electron transport, can delay the onset of euxinia in coastal waters. Our results reveal a remarkable seasonal succession of sulfur cycling pathways, which was observed over multiple years. Cable bacteria dominate the sediment geochemistry in winter, whereas, after the summer hypoxia, Beggiatoaceae mats colonize the sediment. The specific electrogenic metabolism of cable bacteria generates a large buffer of sedimentary iron oxides before the onset of summer hypoxia, which captures free sulfide in the surface sediment, thus likely preventing the development of bottom water euxinia. As cable bacteria are present in many seasonally hypoxic systems, this euxinia-preventing firewall mechanism could be widely active, and may explain why euxinia is relatively infrequently observed in the coastal ocean.

Rapid redox signal transmission by cable bacteria beneath a photosynthetic biofilm

ABSTRACT Recently, long filamentous bacteria, belonging to the family Desulfobulbaceae, were shown to induce electrical currents over long distances in the surface layer of marine sediments. These “cable bacteria” are capable of harvesting electrons from free sulfide in deeper sediment horizons and transferring these electrons along their longitudinal axes to oxygen present near the sediment-water interface. In the present work, we investigated the relationship between cable bacteria and a photosynthetic algal biofilm. In a first experiment, we investigated sediment that hosted both cable bacteria and a photosynthetic biofilm and tested the effect of an imposed diel light-dark cycle by continuously monitoring sulfide at depth. Changes in photosynthesis at the sediment surface had an immediate and repeatable effect on sulfide concentrations at depth, indicating that cable bacteria can rapidly transmit a geochemical effect to centimeters of depth in response to changing conditions at the sediment surface. We also observed a secondary response of the free sulfide at depth manifest on the time scale of hours, suggesting that cable bacteria adjust to a moving oxygen front with a regulatory or a behavioral response, such as motility. Finally, we show that on the time scale of days, the presence of an oxygenic biofilm results in a deeper and more acidic suboxic zone, indicating that a greater oxygen supply can enable cable bacteria to harvest a greater quantity of electrons from marine sediments. Rapid acclimation strategies and highly efficient electron harvesting are likely key advantages of cable bacteria, enabling their success in high sulfide generating coastal sediments.

Electrogenic Sulfur Oxidation by Cable Bacteria in Bivalve Reef Sediments

Cable bacteria induce long-distance electron transport in the seafloor and can exert a powerful control on the elemental cycling in marine sediments by creating extreme excursions in porewater pH. Yet, the natural distribution of cable bacteria is still largely unknown, and so their role in coastal biogeochemical cycling remains poorly quantified. Here we show that cable bacteria can be abundant in the sediments of intertidal bivalve reefs, where they strongly influence the pore water geochemistry, resulting in a potentially beneficial interaction between the sulfur oxidizing microbes and biodepositing fauna. Cable bacteria occurred in sediments accumulating within mussel and oyster reefs in the Wadden Sea (The Netherlands), at cumulative filament densities up to 1038 m cm-2. Additionally, cable bacteria were found at moderately high cumulative filament densities (up to 56 m cm-2) in a heavily bioturbated sandy sediment adjacent to the muddy reefs. Microsensor profiling revealed strong sulfide removal and intense acid generation associated with the electrogenic sulfide oxidation metabolism of the cable bacteria. Strongly elevated concentrations of dissolved calcium (up to 35 mM), manganese (up to 250 µM), and iron (up to 700 µM) were observed in the pore waters, consistent with acidity-driven dissolution of calcium carbonates and iron sulfides. This field study provides substantive evidence that cable bacteria exert a decisive control on the cycling of sulfur and carbonate minerals in cohesive coastal sediments, and identifies that the distribution and influence of cable bacteria covers a greater range of natural habitats than previously believed.

Reply to Prince et al.: Ability of chemical dispersants to reduce oil spill impacts remains unclear.

Chemical dispersants are applied to oil-contaminated areas as a primary response to oceanic oil spills. The impacts of dispersants on microbial community composition and activity, particularly hydrocarbon turnover, are debated. Kleindienst et al. (1) demonstrated that Corexit 9500, a dispersant, can suppress the activity of oil-degrading microorganisms. Chemically enhanced water-accommodated fractions (CEWAFs) were used for these experiments because the deepwater plume that formed following the Deepwater Horizon (DWH) blowout consisted of the water-accommodated fraction: Roughly half of the discharged oil, along with dispersants applied at the wellhead, was entrained in the deepwater plume (2). Using CEWAFs assured an appropriate simulation of the DWH plume chemistry. Prince et al. (3) claim that the method used to produce CEWAFs would leave … [↵][1]5To whom correspondence should be addressed. Email: mjoye{at}uga.edu. [1]: #xref-corresp-1-1

Where Light and Nutrients Collide: The Global Distribution and Activity of Subsurface Chlorophyll Maximum Layers

A satellite view of the world’s oceans presents a mosaic of high chlorophyll (Chla) regions adjacent vast Chla deserts. However, such a view is limited because it reflects conditions of near surface waters only, and misses the vast and sometimes permanent regions of elevated Chla that can exist in subsurface waters. Subsurface chlorophyll maximum layers (SCMLs) are widespread features of the global ocean and are composed of phytoplankton communities that are chromatically and nutritionally adapted to these environments. In this chapter, we first outline the drivers that structure the formation and persistence of SCMLs in marine systems. We develop a simple model that predicts the global distribution and seasonal persistence of SCMLs and find that during any given season, between 59 and 73 % of the ocean may support an SCML. Using a well established global net primary production model, we further predict that approximately 47 % of ocean primary production occurs within SCMLs, a surprisingly large fraction, given the degree of light limitation at these depths. For context, we synthesize key works that have investigated primary production, phytoplankton biomass, and/or nutrient turnover within SCMLs across a range of ocean biomes. These recent studies support previous hypotheses that SCMLs are important sites for new production, and indicate that this new production largely occurs during times when SCMLs are moving deeper into nutriclines or when they are supplied with nutrients through other mechanisms (e.g., tides). In a final section, we draw upon our formative studies in limnology to make linkages between marine and lacustrine systems in terms of the structure and function of SCMLs. Because of large gradients in size, optical properties, and nutritional status across lakes, these systems may present ideal environments to test hypotheses related to the regulation and consequences of SCML productivity.