Single cell genomic and transcriptomic evidence for the use of alternative nitrogen substrates by anammox bacteria

Ganesh, Sangita; Bertagnolli, Anthony D.; Bristow, Laura A.; Padilla, Cory C.; Blackwood, Nigel; Aldunate, Montserrat; Bourbonnais, Annie; Altabet, Mark A.; Malmstrom, Rex R.; Woyke, Tanja; Ulloa, Osvaldo; Konstantinidis, Konstantinos T.; Thamdrup, Bo; Stewart, Frank J.

doi:10.1038/s41396-018-0223-9

Cited by 50 publications

(40 citation statements)

References 82 publications

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“…Recent studies demonstrated the utilization of cyanate as a substrate for ammonia oxidation and nitrogen assimilation by thermophilic and marine AOA and marine anammox organisms (24)(25)(26). In the AOA strain Nitrososphaera gargensis, this capability is based on the release of ammonia from cyanate by the enzymatic activity of cyanate hydratase (cyanase) (24).…”

Section: Resultsmentioning

confidence: 99%

Activity and Metabolic Versatility of Complete Ammonia Oxidizers in Full-Scale Wastewater Treatment Systems

Yang

Daims

Liu

et al. 2020

mBio

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The recent discovery of complete ammonia oxidizers (comammox) contradicts the paradigm that chemolithoautotrophic nitrification is always catalyzed by two different microorganisms. However, our knowledge of the survival strategies of comammox in complex ecosystems, such as full-scale wastewater treatment plants (WWTPs), remains limited. Analyses of genomes and in situ transcriptomes of four comammox organisms from two full-scale WWTPs revealed that comammox were active and showed a surprisingly high metabolic versatility. A gene cluster for the utilization of urea and a gene encoding cyanase suggest that comammox may use diverse organic nitrogen compounds in addition to free ammonia as the substrates. The comammox organisms also encoded the genomic potential for multiple alternative energy metabolisms, including respiration with hydrogen, formate, and sulfite as electron donors. Pathways for the biosynthesis and degradation of polyphosphate, glycogen, and polyhydroxyalkanoates as intracellular storage compounds likely help comammox survive unfavorable conditions and facilitate switches between lifestyles in fluctuating environments. One of the comammox strains acquired from the anaerobic tank encoded and transcribed genes involved in homoacetate fermentation or in the utilization of exogenous acetate, both pathways being unexpected in a nitrifying bacterium. Surprisingly, this strain also encoded a respiratory nitrate reductase which has not yet been found in any other Nitrospira genome and might confer a selective advantage to this strain over other Nitrospira strains in anoxic conditions. IMPORTANCE The discovery of comammox in the genus Nitrospira changes our perception of nitrification. However, genomes of comammox organisms have not been acquired from full-scale WWTPs, and very little is known about their survival strategies and potential metabolisms in complex wastewater treatment systems. Here, four comammox metagenome-assembled genomes and metatranscriptomic data sets were retrieved from two full-scale WWTPs. Their impressive and—among nitrifiers—unsurpassed ecophysiological versatility could make comammox Nitrospira an interesting target for optimizing nitrification in current and future bioreactor configurations.

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Section: Resultsmentioning

confidence: 99%

Activity and Metabolic Versatility of Complete Ammonia Oxidizers in Full-Scale Wastewater Treatment Systems

Yang

Daims

Liu

et al. 2020

mBio

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“…Urea and cyanate are two dissolved organic nitrogen compounds ubiquitously present in seawater 26 , and also detected in marine sediment porewater 27 . The utilizations of these two compounds have been suggested for Scalindua lineages found in oxygen minimum zones based on chemical measurements 28,29 and supported by single-cell genome sequencing 30 . Here we expand this observation to marine sediments, by unambiguously identifying a urease and two cyanases in a single sediment Ca.…”

Section: Main Textmentioning

confidence: 94%

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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“…The ability to use cyanate as a source of reductant (i.e., ammonia) and carbon (i.e., carbon dioxide) may also be an important ecological adaptation of ammonia-oxidizing microorganisms, with implications for soil nitrification. Although only a few genomes of ammonia-oxidizing archaea and complete ammonia-oxidizing (comammox) organisms are known to encode cyanases (5,42,43), another but yet unknown enzyme may be involved in the decomposition of cyanate. Kitzinger et al (7) found that an isolate of a marine ammonia-oxidizing archaeon lacking a cyanase can oxidize cyanate to nitrite.…”

Section: Resultsmentioning

confidence: 99%

“…Cyanate (NCO -) is an organic nitrogen compound that has mainly been of interest in medical science due to its negative effect on protein conformation and enzyme activity (e.g., 1), in chemical industry as industrial feedstock, and in industrial wastewater treatment, where it is produced in large amounts, especially during cyanide removal (e.g., 2,3). However, in recent years, cyanate received more attention in marine biogeochemistry and microbial ecology, with the discovery of the involvement of cyanate in central nitrogen (N) cycling processes, namely in nitrification and anaerobic ammonia oxidation (anammox) (4,5).…”

Section: Introductionmentioning

confidence: 99%

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Cyanate – a low abundant but actively cycled nitrogen compound in soil

Mooshammer

Wanek

Jones

et al. 2020

Preprint

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Cyanate (NCO-) can serve as a nitrogen and/or carbon source for different microorganisms and even additionally as an energy source for autotrophic ammonia oxidizers. Despite the widely distributed genetic potential for direct cyanate utilization among bacteria, archaea and fungi, the availability and environmental significance of cyanate is largely unknown, especially in terrestrial ecosystems. We found relatively low concentrations of soil cyanate, but its turnover was rapid. Contrary to our expectations, cyanate consumption was clearly dominated by biotic processes, and, notably, cyanate was produced in-situ at rates similar to that of cyanate formation from urea fertilizer, which is believed to be one of the major sources of cyanate in the environment. Our study provides evidence that cyanate is actively turned over in soils and represents a small but continuous nitrogen/energy source for soil microbes, potentially contributing to a selective advantage of microorganisms capable of direct cyanate utilization.

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Single cell genomic and transcriptomic evidence for the use of alternative nitrogen substrates by anammox bacteria

Cited by 50 publications

References 82 publications

Activity and Metabolic Versatility of Complete Ammonia Oxidizers in Full-Scale Wastewater Treatment Systems

Activity and Metabolic Versatility of Complete Ammonia Oxidizers in Full-Scale Wastewater Treatment Systems

In situgrowth of anammox bacteria in subseafloor sediments

Cyanate – a low abundant but actively cycled nitrogen compound in soil

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