Abstract

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.

Highlights

  • No other environment hosts as many microbial cells as the marine sedimentary biosphere

  • In order to investigate the global occurrence of this particular geochemical transition zones (GTZs), we searched through geochemical profiles from earlier studies and identified the nitrate–ammonium transition zone (NATZ) at 63 additional sites (Fig. 1B and see SI Appendix, Fig. S1 for the porewater nitrate and ammonium profiles)

  • Combining with the recently reported resilience of anammox bacteria in arid soils [28], our results indicate that these organisms are able to survive prolonged periods of suboptimal conditions, and proliferate once they encounter more energetically favorable ones in NATZ sediments up to ∼80,000-y-old sediment (i.e., 160 cm deep sediment in GC04 with a sedimentation rate of 2 cm/Ky) [29]

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Summary

Introduction

No other environment hosts as many microbial cells as the marine sedimentary biosphere. 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. By combining a variety of biogeochemical and molecular methods to describe the energetics and genetics of the bacteria specialized in anaerobic ammonium oxidation, we show that despite prolonged exposure to highly unfavorable conditions for tens of thousands of years, these bacteria exhibit remarkable net population growth when reaching their niche: the nitrate– ammonium transition zone This common, yet understudied, geochemical transition zone represents an oasis in the sedimentary energetic desert, and the growth it supports is of major importance for the global nitrogen cycle

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