Microbial activity in energy-rich and redox-variable ecosystems

Abstract

Microbial mineralization in intertidal sandy sediments plays an essential role in coastal carbon cycling. Surface sediments in these dynamic systems frequently switch between oxic and anoxic conditions depending on factors such as tides and waves. Additionally, they are occasionally subjected to the sudden, high deposition of organic material. When the production rate of the reduced products of anaerobic degradation is higher than the transport rate of oxygen into the sediments, reduced intermediates can accumulate and eventually be exported from the sediments. The aim of this study was to improve the understanding of the response of microbial activity to dynamics in electron donor and acceptor availability, particularly of anaerobic microbial degradation of the organic material.

In Chapter 2, a sandy beach on the island of Helgoland was explored, which regularly receives large depositions of kelp debris. A combination of in situ and laboratory microsensing, 35S radiotracer incubations, porewater and sediment analyses, and molecular analyses was used to address the impact of kelp deposition on microbial mineralization and community composition in underlying sandy sediments. The sedimentary biogeochemical conditions on the beach were distinct, with high concentrations of nutrients, dissolved organic and inorganic carbon, and a low pH. Kelp deposition shaped the microbial community, which is optimized for the use of kelp material. The community could immediately degrade kelp upon deposition, which fostered high production rates of reduced products. As these rates were higher than the transport rate of oxygen into the sediments, sulfide accumulated and was exported from the sediments. The export of sulfide to the sea led to the development of a diverse community of filamentous sulfide-oxidizing bacteria.

As Chapter 2 highlighted that the microbial community in sediments associated with kelp deposits must be highly specialized to be able to deal with the complex organic material in kelp, Chapter 3 aimed to illuminate the adaptation of microbial communities in these sediments to the degradation of kelp-derived carbohydrate substrates. Oxygen microsensor and 35S radiotracer methods showed strong increases in aerobic respiration and sulfate reduction rates after the addition of specific carbohydrates. The community was indeed specialized to the degradation of kelp-derived carbohydrates. Remarkably, kelp-derived polysaccharides often led to higher aerobic respiration rates than monomers. Monosaccharide analysis and microarray analysis were used to determine the substrate pools in sediments. Respiration rates were up two orders of magnitude higher than in reference sediments, though substrate pools were approximately equal. Thus, substrate turnover rates are much higher on beaches with regular kelp deposition, where microbial communities are more active and are specialized in the carbohydrates they often encounter.

Chapter 4 focused on illuminating the effect of transient oxygen exposure on the efficiency of microbial mineralization in an intertidal sandflat in the Wadden Sea. This included testing the hypothesis that reactive oxygen species (ROS) are present in high concentrations in intertidal permeable sediments and control microbial mineralization rates. We incubated sediment slurries that transitioned from oxic to anoxic conditions and slurries that were anoxic throughout the incubation period. Furthermore, we measured hydrogen peroxide concentrations in porewater. Sulfate-reducing bacteria in intertidal permeable sediments are frequently exposed to oxygen. Yet, this did not select for sulfate-reducing bacteria that perform sulfate reduction in the presence of oxygen. Whereas oxygen inhibited sulfate reduction, the sulfate-reducing bacteria were not eliminated by oxygen, but sulfate reduction instantly resumed after oxygen was depleted. The presence of oxygen even boosted subsequent sulfate reduction in the anoxic period. This could be related to oxygen-stimulated hydrolysis of macromolecules during the oxic period. High levels of ROS were found in the porewater of the intertidal flat. ROS are detrimental for microorganisms, as they are able to degrade cellular components and thus lead to cell death. Indeed, removal of ROS in slurry incubations led to strongly increased microbial mineralization rates. This study highlights the contradictory effects of redox shifts on mineralization efficiency, with the presence of oxygen increasing efficiency of subsequent anaerobic processes, even though ROS appeared to inhibit mineralization.

In Chapter 5, a sulfide-oxidizing community forming egg-shaped sulfur structures on top of a hot smoker in the deep-sea was studied. Hydrodynamics around such structures are dominated by diffusion, contrary to the advection-dominated system of Chapter 2. Both studied systems are characterized by input of reduced material in an oxic ecosystem, and are therefore out of thermodynamic equilibrium. Comparison between the systems described in Chapter 2 and Chapter 5 aimed to further illuminate the oxidative side of the sulfur cycle in the two contrasting energy-rich redox-variable systems. Different environmental conditions, including hydrodynamics, select for specific sulfide-oxidizing communities and morphologies. The mixing of sulfide into turbulent oxygenated seawater led to the development of filamentous mats of sulfide-oxidizing bacteria growing on rocks at the low tide waterline of the beach (Chapter 2). This attachment prevents the sulfide-oxidizing bacteria from being washed away, and the filamentous structure allows them to make optimal use of the dynamic conditions of the turbulent seawater. On the other hand, the egg-shaped gelatinous sulfur structure produced by sulfide-oxidizing bacteria (Chapter 5) might result from the narrow overlap of oxygen and sulfide which are provided from the same direction.

Overall, this study shows that changes in the availability of electron donors and acceptors, and thus redox dynamics, have a large effect on microbial activity. Large influxes of organic material result in a system that is out of thermodynamic equilibrium, and exports reduced compounds towards the sea. Microbial communities are optimized for these conditions, and can directly access the available organic material, while also being able to make use of the reduced compounds that result from microbial mineralization. Sulfide-oxidizing bacteria at the low tide waterline are adapted to the especially dynamic conditions of this environment. While the production of ROS reduces microbial mineralization, the presence of oxygen should not only be seen as an inhibitor of anaerobic microbial mineralization, but also as crucial to the production of electron donors available at the start of anoxia. This study therefore highlights the importance of spatio-temporal dynamics in electron donor and acceptor availability for microbial activity.