The deep biosphere buried in marine sediments was estimated to host an equal number of microbes as found in the above oceans 1 . It has been debated if these cells are alive and active 2 , and their per cell energy availability does not seem to allow for net population growth 3 . Here, we report the growth of anammox bacteria in ∼80,000 year old subsurface sediments indicated by their four orders of magnitude abundance increase in the nitrate-ammonia transition zone (NATZ). Their growth coincides with a local increase in anammox power supply. The genome of the dominant anammox bacterium from the NATZ was reconstructed and showed an increased index of replication confirming in situ active growth. The genome belongs to a new Scalindua species so far exclusively found in marine environments, which has the genetic capacity of urea and cyanate utilization and is enriched in genes allowing it to cope with external environmental stressors, such as energy limitation. Our results suggest that specific microbial groups are not only able to survive over geological timescales, but also thrive in the deep subsurface when encountering favorable conditions.
Microbial sulfate reduction is generally limited in the deep sea compared to shallower marine environments, but cold seeps and hydrothermal systems are considered an exception. Here, we report sulfate reduction rates and geochemical data from marine sediments and hydrothermal vent fields along the Arctic Mid Ocean Ridges (AMOR), to assess the significance of basalt-hosted hydrothermal activity on sulfate reduction in a distal deep marine setting. We find that cored marine sediments do not display evidence for sulfate reduction, apart from low rates in sediments from the Knipovich Ridge. This likely reflects the overall limited availability of reactive organic matter and low sedimentation rates along the AMOR, except for areas in the vicinity of Svalbard and Bear Island. In contrast, hydrothermal samples from the Seven Sisters, Jan Mayen and Loki’s Castle vent fields all demonstrate active microbial sulfate reduction. Rates increase from a few 10s to 100s of pmol SO 4 2- cm -3 d -1 in active high-temperature hydrothermal chimneys, to 10s of nmol SO 4 2- cm -3 d -1 in low-temperature barite chimneys and up to 110 nmol cm -3 d -1 in diffuse venting hydrothermal sediments in the Barite field at Loki’s Castle. Pore fluid and sediment geochemical data suggest that these high rates are sustained by organic compounds from microbial mats and vent fauna as well as methane supplied by high-temperature hydrothermal fluids. However, significant variation was observed between replicate hydrothermal samples and observation of high rates in seemingly inactive barite chimneys suggests that other electron donors may be important as well. Sediment sulfur isotope signatures concur with measured rates in the Barite field and indicate that microbial sulfate reduction has occurred in the hydrothermal sediments since the recent geological past. Our findings indicate that basalt-hosted vent fields provide sufficient electron donors to support microbial sulfate reduction in high- and low-temperature hydrothermal areas in settings that otherwise show very low sulfate reduction rates.
Abstract By consuming ammonium and nitrite, anammox bacteria form an important functional guild in nitrogen cycling in many environments, including marine sediments. However, their distribution and impact on the important substrate nitrite has not been well characterized. Here we combined biogeochemical, microbiological, and genomic approaches to study anammox bacteria and other nitrogen cycling groups in two sediment cores retrieved from the Arctic Mid-Ocean Ridge (AMOR). We observed nitrite accumulation in these cores, a phenomenon also recorded at 28 other marine sediment sites and in analogous aquatic environments. The nitrite maximum coincides with reduced abundance of anammox bacteria. Anammox bacterial abundances were at least one order of magnitude higher than those of nitrite reducers and the anammox abundance maxima were detected in the layers above and below the nitrite maximum. Nitrite accumulation in the two AMOR cores co-occurs with a niche partitioning between two anammox bacterial families (Candidatus Bathyanammoxibiaceae and Candidatus Scalinduaceae), likely dependent on ammonium availability. Through reconstructing and comparing the dominant anammox genomes (Ca. Bathyanammoxibius amoris and Ca. Scalindua sediminis), we revealed that Ca. B. amoris has fewer high-affinity ammonium transporters than Ca. S. sediminis and lacks the capacity to access alternative substrates and/or energy sources such as urea and cyanate. These features may restrict Ca. Bathyanammoxibiaceae to conditions of higher ammonium concentrations. These findings improve our understanding about nitrogen cycling in marine sediments by revealing coincident nitrite accumulation and niche partitioning of anammox bacteria.
The reconstruction of past climate variability using physical and geochemical parameters from lake sedimentary records is a well-established and widely used approach. These geological records are also known to contain large and active microbial communities, believed to be responsive to their surroundings at the time of deposition, and proceed to interact intimately with their physical and chemical environment for millennia after deposition. However, less is known about the potential legacy of past climate conditions on the contemporary microbial community structure. We analysed two Holocene-length (past 10 ka BP) sediment cores from the glacier-fed Ymer Lake, located in a highly climate-sensitive region on south-eastern Greenland. By combining physical proxies, solid as well as fluid geochemistry, and microbial population profiling in a comprehensive statistical framework, we show that the microbial community structure clusters according to established lithological units, and thus captures past environmental conditions and climatic transitions. Further, comparative analyses of the two sedimentary records indicates that the manifestation of regional climate depends on local settings such as water column depth, which ultimately constrains microbial variability in the deposited sediments. The strong coupling between physical and geochemical shifts in the lake and microbial variation highlights the potential of molecular microbiological data to strengthen and refine existing sedimentological classifications of past environmental conditions and transitions. Furthermore, this coupling implies that microbially controlled transformation and partitioning of geochemical species (e.g., manganese and sulphate) in Ymer lake today is still affected by climatic conditions that prevailed thousands of years back in time.
