Affinity informs environmental cooperation between ammonia-oxidizing archaea (AOA) and anaerobic ammonia-oxidizing (Anammox) bacteria

Straka, Levi; Meinhardt, Kelley A.; Bollmann, Annette; Stahl, David A.; Winkler, Mari-K.H.

doi:10.1038/s41396-019-0408-x

Cited by 92 publications

(58 citation statements)

References 30 publications

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“…These two metabolic traits may not only enable Ca. S. sediminis to have access to alternative energy sources (i.e., urea and cyanate), but also provide it with an internal source of ammonium allowing it to persist under the severe competition disadvantage relative to ammonia-oxidizing Thaumarchaeota ( 43 ) in the upper oxic sediment layers.…”

Section: Resultsmentioning

confidence: 99%

Geochemical transition zone powering microbial growth in subsurface sediments

Zhao

Mogollón

Abby

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

117

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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 aScalinduaspecies which we nameCandidatus 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.

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Section: Resultsmentioning

confidence: 99%

Geochemical transition zone powering microbial growth in subsurface sediments

Zhao

Mogollón

Abby

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

117

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“…S. sediminis to have access to alternative energy sources (i.e. urea and cyanate), but also provide it with extra ammonium to persist under the severe competition disadvantage with ammonia oxidizing Thaumarchaeota 31 in the upper low-oxic sediment layers.…”

Section: Main Textmentioning

confidence: 99%

In situgrowth of anammox bacteria in subseafloor sediments

Zhao

Mogollón

Abby

et al. 2019

Preprint

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The deep biosphere buried in marine sediments was estimated to host an equal number 18 of microbes as found in the above oceans 1 . It has been debated if these cells are alive 19 and active 2 , and their per cell energy availability does not seem to allow for net 20 population growth 3 . Here, we report the growth of anammox bacteria in ~80,000 year 21 old subsurface sediments indicated by their four orders of magnitude abundance 22 increase in the nitrate-ammonia transition zone (NATZ). Their growth coincides with a 23 local increase in anammox power supply. The genome of the dominant anammox 24 bacterium from the NATZ was reconstructed and showed an increased index of 25 replication confirming in situ active growth. The genome belongs to a new Scalindua 26 species so far exclusively found in marine environments, which has the genetic capacity 27 of urea and cyanate utilization and is enriched in genes allowing it to cope with external 28 environmental stressors, such as energy limitation. Our results suggest that specific 29 microbial groups are not only able to survive over geological timescales, but also thrive 30 in the deep subsurface when encountering favorable conditions. 31 32 Main text 33 The global cell numbers of microbes in marine sediments is estimated to be on the order of 34 2.9-5.4×10 29 equaling up to 1/3 rd of the total prokaryotic biomass on Earth 1,4 . A considerable 35 portion of these cells reside beyond the bioturbation zone and constitute the marine deep 36 biosphere 5 . Microbial cells in the subseafloor sediments are sealed off from recruitment of 37 new cells and fresh substrates from the surface, and therefore are thought to suffer severe 38 energy limitations 3 . Despite this, several lines of circumstantial evidence indicate that the 39 deep microbial biosphere is alive 6,7 , but with extremely slow metabolic rates 8,9 and long 40 turnover times of hundreds to thousands of years 2,10 . Although microbial growth (net biomass 41 production) was frequently assumed 10,11 and recently observed in laboratory incubations 12 , 42 concrete evidence of in situ microbial growth in the marine deep biosphere is lacking. 43Energy availability is considered one of the most fundamental factors limiting life, but 44 has not been explicitly demonstrated to control the changes of microbial communities in the 45 deep biosphere 13 . Whereas the deep sedimentary realm is a stable environment with low 46 energy availability, geochemical transition zones such as the sulfate-methane transition 47 growth associated with increased power availabilities in ~ 80,000 year old subsurface 55 sediments. 56 We retrieved four sediment cores (2.0-3.6 meters long) from the seabed of the Arctic 57 Mid-Ocean Ridge (AMOR) at water depths of 1653 -3007 m ( Fig. 1a and Table S1), to 58 perform high vertical resolution geochemical measurements and microbiological analyses. All 59 four cores exhibited similar geochemical profiles ( Fig. 2a-c), summarized as follows: 1) O 2 60 monotonically decreased and was deplet...

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“… 39 ). The colonization and expansion of terrestrial and freshwater ecosystems may have led to the development of localized nitrogen-rich copiotrophic environments like those preferred by AOB today 54 , 58 , 59 . These changes may have provided opportunities for the convergent evolution of multiple lineages of ammonia oxidizing bacteria, particularly Nitrosomonadaceae and Nitrosococcaceae.…”

Section: Introductionmentioning

confidence: 99%

Phanerozoic radiation of ammonia oxidizing bacteria

Ward

Johnston

Shih

2021

Sci Rep

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The modern nitrogen cycle consists of a web of microbially mediated redox transformations. Among the most crucial reactions in this cycle is the oxidation of ammonia to nitrite, an obligately aerobic process performed by a limited number of lineages of bacteria (AOB) and archaea (AOA). As this process has an absolute requirement for O2, the timing of its evolution—especially as it relates to the Great Oxygenation Event ~ 2.3 billion years ago—remains contested and is pivotal to our understanding of nutrient cycles. To estimate the antiquity of bacterial ammonia oxidation, we performed phylogenetic and molecular clock analyses of AOB. Surprisingly, bacterial ammonia oxidation appears quite young, with crown group clades having originated during Neoproterozoic time (or later) with major radiations occurring during Paleozoic time. These results place the evolution of AOB broadly coincident with the pervasive oxygenation of the deep ocean. The late evolution AOB challenges earlier interpretations of the ancient nitrogen isotope record, predicts a more substantial role for AOA during Precambrian time, and may have implications for understanding of the size and structure of the biogeochemical nitrogen cycle through geologic time.

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Affinity informs environmental cooperation between ammonia-oxidizing archaea (AOA) and anaerobic ammonia-oxidizing (Anammox) bacteria

Cited by 92 publications

References 30 publications

Geochemical transition zone powering microbial growth in subsurface sediments

Geochemical transition zone powering microbial growth in subsurface sediments

In situgrowth of anammox bacteria in subseafloor sediments

Phanerozoic radiation of ammonia oxidizing bacteria

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