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Even though sediment macrofauna are widespread in the global seafloor, the influence of these fauna on microbial communities that drive sediment biogeochemical cycles remains poorly understood. According to recent field investigations, macrofaunal activities control bacterial and archaeal community structure in surface sediments, but the inferred mechanisms have not been experimentally verified. Here we use laboratory microcosms to investigate how activities of two major polychaete guilds, the lugworms, represented by Abarenicola pacifica, and the clamworms, represented by Nereis vexillosa, influence microbial communities in coastal sediments. A. pacifica treatments show >tenfold increases in microbial cell-specific consumption rates of oxygen and nitrate, largely due to the strong ventilation activity of A. pacifica. While ventilation resulted in clearly elevated percentages of nitrifying archaea (Nitrosopumilus spp.) in surface sediments, it only minorly affected bacterial community composition. By comparison, reworking - mainly by deposit-feeding of A. pacifica - had a more pronounced impact on microorganismal communities, significantly driving down abundances of Bacteria and Archaea. Within the Bacteria, lineages that have been linked to the degradation of microalgal biomass (e.g., Flavobacteriaceae and Rhodobacteraceae), were especially affected, consistent with the previously reported selective feeding of A. pacifica on microalgal detritus. In contrast, N. vexillosa, which is not a deposit feeder, did not significantly influence microbial abundances or microbial community structure. This species also only had a relatively minor impact on rates of oxygen and nitrogen cycling, presumably because porewater exchanges during burrow ventilation by this species were mainly restricted to sediments immediately surrounding the burrows. Collectively our analyses demonstrate that macrofauna with distinct bioturbation modes differ greatly in their impacts on microbial community structure and microbial metabolism in marine sediments., Frontiers in Marine Science, 10, ISSN:2296-7745

Summary Seagrasses are one of the most efficient natural sinks of carbon dioxide (CO 2 ) on Earth1. Despite covering less than 0.1 % of coastal regions, they have the capacity to bury up to 10 % of marine organic matter 1 and can bury the same amount of carbon 35 times faster than tropical rainforests 2 . On land, the soil’s ability to sequestrate carbon is intimately linked to microbial metabolism 3 . Despite the growing attention to the link between plant production, microbial communities, and the carbon cycle in terrestrial ecosystems 4–6 , these processes remain enigmatic in the sea. Here, we show that seagrasses excrete organic sugars, namely in the form of sucrose, into their rhizospheres. Surprisingly, the microbial communities living underneath meadows do not fully use this sugar stock in their metabolism. Instead, sucrose piles up in the sediments to mM concentrations underneath multiple types of seagrass meadows. Sediment incubation experiments show that microbial communities living underneath a meadow use sucrose at low metabolic rates. Our metagenomic analyses revealed that the distinct community of microorganisms occurring underneath meadows is limited in their ability to degrade simple sugars, which allows these compounds to persist in the environment over relatively long periods of time. Our findings reveal how seagrasses form blue carbon stocks despite the relatively small area they occupy. Unfortunately, anthropogenic disturbances are threatening the long-term persistence of seagrass meadows. Given that these sediments contain a large stock of sugars that heterotopic bacteria can degrade, it is even more important to protect these ecosystems from degradation.

Metal-sulfides are wide-spread in marine benthic habitats. At deep-sea hydrothermal vents, they occur as massive sulfide chimneys formed by mineral precipitation upon mixing of reduced vent fluids with cold oxygenated sea water. Although microorganisms inhabiting actively venting chimneys and utilizing compounds supplied by the venting fluids are well studied, only little is known about microorganisms inhabiting inactive chimneys. In this study, we combined 16S rRNA gene-based community profiling of sulfide chimneys from the Manus Basin (SW Pacific) with radiometric dating, metagenome (n = 4) and metaproteome (n = 1) analyses. Our results shed light on potential lifestyles of yet poorly characterized bacterial clades colonizing inactive chimneys. These include sulfate-reducing Nitrospirae and sulfide-oxidizing Gammaproteobacteria dominating most of the inactive chimney communities. Our phylogenetic analysis attributed the gammaproteobacterial clades to the recently described Woeseiaceae family and the SSr-clade found in marine sediments around the world. Metaproteomic data identified these Gammaproteobacteria as autotrophic sulfide-oxidizers potentially facilitating metal-sulfide dissolution via extracellular electron transfer. Considering the wide distribution of these gammaproteobacterial clades in marine environments such as hydrothermal vents and sediments, microbially accelerated neutrophilic mineral oxidation might be a globally relevant process in benthic element cycling and a considerable energy source for carbon fixation in marine benthic habitats.

At deep sea hydrothermal fields, a mixing gradient between hot reduced fluids and cold oxygenated sea water creates a number of micro-environments with different physico-chemical conditions in direct proximity to each other. Although many of the key microorganisms in these environments have been identified and described, a systematic understanding of their distribution across the mixing gradient and their niche partitioning is still missing. In my doctoral thesis, I investigated the interplay of geochemical settings, microbial community structures, and diversification of microorganisms in three collaborative studies of hydrothermal vent fields in the Atlantic and Pacific Oceans. Taken together, this thesis provides a detailed overview of the microbial community structures in hydrothermal vents. It deepens our understanding of niche differentiation of major marine sulfur oxidizers, and offers valuable insights into microbial diversification.

This study aims to test recent developments for advancing the isotope diffusive exchange technique in order to adapt it to high salinity porewaters and, in a more general way, to solutions with low water activities. This report documents work performed to: 1) investigate factors that might influence the results of the isotope diffusive exchange technique for saline solutions through solution-solution experiments; and 2) benchmark the adapted diffusive exchange method using rock samples previously equilibrated with synthetic solutions of known composition (chemical and isotopic). Two different rocks have been used to perform the benchmarking tests: 1) Queenston Shale from Ontario, Canada; and 2) Opalinus Clay from the Mont Terri Underground Research Laboratory (URL), Switzerland. Solution-solution diffusive-exchange experiments showed that perturbing factors include: 1) the water activity mismatch between the test and sample solutions; 2) the weight difference between the test and sample solutions; and 3) contrasting chemical compositions (NaCl versus CaCl2) between test and sample solutions. Benchmarking of the isotope diffusive exchange method using rock samples equilibrated with synthetic solutions has tested: 1) whether or not the isotopic composition obtained by the diffusive exchange method actually corresponds to the composition of the porewater; and 2) if there are additional perturbing factors, i.e., other than those identified in the solution-solution experiments. Equilibration of Opalinus Clay and Queenston Shale rocks (which are saturated with porewater at experiment initiation) with 0.3 and 5 molal NaCl, and 2.5 and 5 molal CaCl2 synthetic solutions has been performed successfully by immersing 2 to 4 cm diameter rock pieces into air-tight PVC containers for periods of 62 and 90 days, respectively. Equilibrium was apparently attained in about 1 day for Opalinus Clay rock samples, and 4 days for the Queenston Shale rock samples. The rock samples never disaggregated during these experiments, even at 0.3 molal NaCl solution concentrations. The density of the equilibrated rocks, in all cases, is lower than that of the intact porewater-saturated rock and increases with increasing salinity of the synthetic solution. This is probably because the confining pressure in the equilibration experiments is low compared to in-situ conditions. The rock density correlates with its water content, which is higher in low salinity solutions. Data obtained from Opalinus Clay and Queenston Shale rock experiments indicate that the diffusive exchange method gives reliable results of the isotope composition (δ18O and δ2H) of the porewater at all salinities when the chemistries of the porewater and test waters are similar. Results for δ18O values are shifted up by about 1‰ for contrasting chemistries (NaCl versus CaCl2), and insignificantly for δ2H. The diffusive exchange technique gives reliable results for rocks with water content as low as 0.5 wt%. For unknown reasons, the use of the diffusive exchange method for obtaining the water content of the rock gave good results at high salinities (≥2.5 molal), but overestimated values at low salinities (0.3 molal).

We investigated the impact of kelp deposition on the geochemistry and microbial community composition of beach sands on the island of Helgoland (North Sea). The composition of the microbial community at a beach with regular kelp deposition appeared shaped by this regular input of organic material, as indicated by significantly higher proportions of aerobic degraders, fermenters, and sulfur cycling microorganisms. Rapid degradation of deposited kelp by this community leads to high levels of dissolved organic and inorganic carbon and nutrients, a lower pH and anoxia. Aerobic respiration, fermentation, Fe- and SO42− reduction, and methanogenesis were strongly enhanced, with SO42− reduction being the main process in kelp degradation. SO42− reduction rates increased 20- to 25-fold upon addition of kelp. The main route of electrons from kelp to SO42− was not via CO and H2, as expected, but via organic fermentation products. O2 supply by the tides was not sufficient and reduced intermediates escaped from the sediment with tidal water retraction. The resulting extremely high levels of free sulfide (>10 mmol L−1) lead to abundant filamentous growth of sulfur-oxidizing bacteria largely composed of a rare O2-adapted Sulfurovum lacking the expected denitrification genes. Our results show that regular kelp deposition strongly enhances the thermodynamic disequilibrium in the beach sand habitat, leading to a dramatic enhancement of the sulfur cycle.