Structure and function of microorganisms in the methanic sediments of the Helgoland mud area, North Sea, Germany

Abstract

The Helgoland mud area was characterized by high sedimentation rates prior to 1250 AD, most likely accounted for by the disintegration of the Helgoland Island during this period. Presumably, high amounts of terrigenous metals (e.g. Fe and Mn minerals) and organic matter were deposited as a result of the high sedimentation rates. Evident from the deposition of high amounts of organic matter and metals in the past are the shallow sulfate-methane transition zone (due to rapid organic matter-dependent electron acceptor consumption) and elevated concentrations of dissolved metals (Fe and Mn) in the methanic zone of the Helgoland mud area. Such high concentrations of dissolved Fe and Mn have been observed in other highly-depositional environments (e.g. Argentine Basin, Bothnian Sea, Aarhus Bay etc.). However, whether biotic or abiotic, the source of elevated dissolved iron in the methanic zone is still not known. Amid several hypotheses, the exact mechanisms of iron reduction in methanic zones of marine sediments are also still a matter of debate. Therefore, as a first step to understanding the potential involvement of microorganisms in iron reduction in the methanic zone in marine sediments, this work provides a 16S rRNA gene-based characterization and quantification of bacteria and archaea populations in the surface and subsurface sediments of the Helgoland mud area. In addition, this work links iron reduction in the methanic zone of the Helgoland mud area to biotic activities and suggested microbial populations which may have been involved in iron cycling therein. High and depth-wisely increasing concentrations of NH4 in pore-water measurements from subsurface sediments of many highly-depositional environments around the world suggest that organic matter degradation is still ongoing in deeper sediments. Nevertheless, molecular information about the composition and diagenetic changes of organic matter from surface to subsurface sediments are few. On this front, this doctoral work shows that the most dominant bacteria and archaea populations in the subsurface sediments of the Helgoland mud area are influenced by concentration of organic matter, thus potentially important for organic matter degradation therein. Molecular characterization of a potentially bio-available portion of sedimentary organic matter (the water-extractable fraction) in the surface and subsurface sediments, using Fourier Ion Cyclotron Resonance Mass Spectrometry, most 7 importantly reveals that while aliphatic, N-rich compounds, presumably of algal origin are preferentially degraded in the surface sediments, O-rich, aromatic compounds, most likely of terrestrial origin are utilized in deeper sediments. These results are consistent with observations in subsurface soils of peatlands suggesting similar diagenetic alterations of organic matter in marine subsurface sediments. It is a three decade-old finding that when poorly-crystalline Mn (IV) is added to marine sediments, there is a rapid formation of sulfate which is linked to biological activity. However, knowledge of the diversity of microorganisms involved in this reaction is limited. In experiments investigating the potential for chemolithotrophic Mn (IV) reduction in subsurface sediments of the Helgoland mud area, this work uncovers novel uncultured Deltaproteobacteria (tentatively named Marine Sediment Manganese-reducing Enrichment, MSME Cluster) potentially involved Mn (IV)-dependent sulfate formation in marine sediments. Overall, this work adds to the current body of knowledge on microbe-mineral or geo-microbiological interactions in marine sediments. The finding that hematite enhanced methanogenesis (by 25 48 % faster) in a year-long slurry incubations with sediments from the subsurface sediment of the Helgoland mud area also provide a basis for future studies on how (semi)conductive iron minerals such as hematite, goethite, and pyrite may mediate electron transfer between specific bacterial populations and methanogens in the Helgoland mud area.