Nitrite accumulation and anammox bacterial niche partitioning in Arctic Mid-Ocean Ridge sediments.

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.

Mapping Microbial Abundance and Prevalence to Changing Oxygen Concentration in Deep-Sea Sediments Using Machine Learning and Differential Abundance.

Oxygen constitutes one of the strongest factors explaining microbial taxonomic variability in deep-sea sediments. However, deep-sea microbiome studies often lack the spatial resolution to study the oxygen gradient and transition zone beyond the oxic-anoxic dichotomy, thus leaving important questions regarding the microbial response to changing conditions unanswered. Here, we use machine learning and differential abundance analysis on 184 samples from 11 sediment cores retrieved along the Arctic Mid-Ocean Ridge to study how changing oxygen concentrations (1) are predicted by the relative abundance of higher taxa and (2) influence the distribution of individual Operational Taxonomic Units. We find that some of the most abundant classes of microorganisms can be used to classify samples according to oxygen concentration. At the level of Operational Taxonomic Units, however, representatives of common classes are not differentially abundant from high-oxic to low-oxic conditions. This weakened response to changing oxygen concentration suggests that the abundance and prevalence of highly abundant OTUs may be better explained by other variables than oxygen. Our results suggest that a relatively homogeneous microbiome is recruited to the benthos, and that the microbiome then becomes more heterogeneous as oxygen drops below 25 µM. Our analytical approach takes into account the oft-ignored compositional nature of relative abundance data, and provides a framework for extracting biologically meaningful associations from datasets spanning multiple sedimentary cores.

Ammonia-oxidizing archaea have similar power requirements in diverse marine oxic sediments.

Energy/power availability is regarded as one of the ultimate controlling factors of microbial abundance in the deep biosphere, where fewer cells are found in habitats of lower energy availability. A critical assumption driving the proportional relationship between total cell abundance and power availability is that the cell-specific power requirement keeps constant or varies over smaller ranges than other variables, which has yet to be validated. Here we present a quantitative framework to determine the cell-specific power requirement of the omnipresent ammonia-oxidizing archaea (AOA) in eight sediment cores with 3-4 orders of magnitude variations of organic matter flux and oxygen penetration depth. Our results show that despite the six orders of magnitude variations in the rates and power supply of nitrification and AOA abundances across these eight cores, the cell-specific power requirement of AOA from different cores and depths overlaps within the narrow range of 10-19-10-17 W cell-1, where the lower end may represent the basal power requirement of microorganisms persisting in subseafloor sediments. In individual cores, AOA also exhibit similar cell-specific power requirements, regardless of the AOA population size or sediment depth/age. Such quantitative insights establish a relationship between the power supply and the total abundance of AOA, and therefore lay a foundation for a first-order estimate of the standing stock of AOA in global marine oxic sediments.

Geochemical transition zone powering microbial growth in subsurface sediments.

No other environment hosts as many microbial cells as the marine sedimentary biosphere. While the majority of these cells are expected to be alive, they are speculated to be persisting in a state of maintenance without net growth due to extreme starvation. Here, we report evidence for in situ growth of anaerobic ammonium-oxidizing (anammox) bacteria in ∼80,000-y-old subsurface sediments from the Arctic Mid-Ocean Ridge. The growth is confined to the nitrate-ammonium transition zone (NATZ), a widespread geochemical transition zone where most of the upward ammonium flux from deep anoxic sediments is being consumed. In this zone the anammox bacteria abundances, assessed by quantification of marker genes, consistently displayed a four order of magnitude increase relative to adjacent layers in four cores. This subsurface cell increase coincides with a markedly higher power supply driven mainly by intensified anammox reaction rates, thereby providing a quantitative link between microbial proliferation and energy availability. The reconstructed draft genome of the dominant anammox bacterium showed an index of replication (iRep) of 1.32, suggesting that 32% of this population was actively replicating. The genome belongs to a Scalindua species which we name Candidatus Scalindua sediminis, so far exclusively found in marine sediments. It has the capacity to utilize urea and cyanate and a mixotrophic lifestyle. Our results demonstrate that specific microbial groups are not only able to survive unfavorable conditions over geological timescales, but can proliferate in situ when encountering ideal conditions with significant consequences for biogeochemical nitrogen cycling.

Microbial Community Structure in Arctic Lake Sediments Reflect Variations in Holocene Climate Conditions.

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.