Science of Qin Wei, University of Oklahoma: Archaeal ammonia oxidation in an oxygen-free world

Archaeal nitrification without oxygen (The single-cell organism can self-produce oxygen for ammonia oxidation) Science [IF: 47.
728] DOI: https://DOI.
org/10.
1126/science.
abn0373 Date of publication: 2022-01-06 Author: Willm Martens-Habbena1 Wei Qin (Qin Wei) 2 Main unit: 1 University of Florida (Department of Microbiology and Cell Science, University of Florida, Institute for Food and Agricultural Sciences, Fort Lauderdale Research and Education Center, Davie, FL 33314, USA) 2 Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK 73019, USA.
) Abstract Ammonia-oxidizing archaea (AOA) account for about 30% of the total marine planktonic microorganisms and play a key role in the marine nitrogen and carbon cycle
.

Marine AOA and nitrite oxidizing bacteria (NOB) relay the oxidation of ammonia nitrogen to nitrate nitrogen, which constitutes the main component of the marine inorganic nitrogen pool
.

The classical research paradigm holds that both AOA and NOB metabolism depend on molecular oxygen (O2) in the environment
.

However, recent evidence suggests that AOA and NOB are also widespread in strictly anoxic marine areas, challenging classical cognition
.

Recently, Kraft et al.
used ultra-sensitive dissolved oxygen probes and isotope tracer technology to demonstrate for the first time that marine AOA (Nitrosopumilus maritimus SCM1) can generate its own oxygen for its ammonia oxidation under anoxic conditions, and at the same time convert nitrite.
Reduced to nitrous oxide (N2O) and nitrogen (N2)
.

This major discovery provides a reasonable explanation for the existence of AOA in the anaerobic ocean, suggesting that AOA may play an important role in the process of nitrogen removal in the anaerobic ocean, and has important implications for the study of the evolutionary history of the Earth's nitrogen cycle
.

Nitrogen cycling in microaerobic zones Conceptual map of the roles of ammonia-oxidizing archaea (AOA) and nitrite-oxidizing bacteria (NOB) in marine nitrogen cycling in microaerophilic zones
.

Nitrification occurs under light-transmitting regions in ocean water bodies
.

But until now, it was thought to be impossible in anoxic regions
.

The paper by Kraft et al.
changes this possibility
.

The discovery of ammonia-oxidizing archaea has dramatically changed our understanding of the global nitrogen cycle
.

Genomic evolutionary analyses based on multiple molecular clock models suggest that archaeal ammonia oxidation originated at least 1 billion years ago
.

Modern AOA is one of the most abundant and ecologically successful star microbial taxa on Earth
.

In particular, AOA has a very high affinity for substrate ammonia and an efficient autotrophic carbon fixation pathway, and exhibits superior adaptability to extreme environments such as oligotrophic and low-energy deep oceans
.

And as the dominant microbial taxa in the marine ammonia oxidation process, AOA is capable of producing the strong greenhouse gas N2O
.

However, the physiological and ecological significance of AOA in the marine hypoxic environment remains an unsolved mystery so far
.

Although the importance of AOA in the global biogeochemical cycle is beyond doubt, its many important physiological and metabolic mechanisms are still very unclear
.

This is due to the low homology between AOA and the existing model microorganisms (genetic operating system), and the incomplete functional annotation at the genome level; the second is limited by the objective factors of the difficulty of AOA purification and cultivation and the low biomass yield
.

The study by Kraft et al.
revealed the ability of marine AOA to generate O2 and N2, taking our knowledge of AOA metabolic function and fitness to a new dimension
.

By using an ultra-sensitive (can detect down to 1 nanomol/L) micro dissolved oxygen sensor combined with 15N stable isotope labeling technology, it was first demonstrated that N.
maritimus is still capable of oxidizing ammonia to nitrite under hypoxic conditions , and the ability to reduce nitrite to N2O and N2
.

When the external oxygen was depleted, N.
maritimus started to produce oxygen and restored the oxygen concentration in the surrounding environment to 50-200 nanomol/L, suggesting that this strain is capable of both producing and (via ammonia oxidation) consuming oxygen
.

In addition, the authors conducted a series of control experiments to correct the interference of NO on the oxygen measurement, and at the same time excluded the interference of other possible reactive nitrogen and oxygen components to ensure the reliability of their research results
.

Although the rate of AOA's own oxygen production and ammonia oxidation is lower than that under external oxygen supply conditions and depends on the supply of external nitrite, based on the number of AOA cells in the marine anaerobic zone and the rate of AOA N2 production, the authors evaluated and found that The contribution rate of AOA to N2 production in this area is comparable to that of classical denitrification and anammox
.

Current biogeochemical models assume that classical nitrification cannot proceed in anoxic environments
.

The results of Kraft et al.
suggest that nitrogen cycling in anoxic regions of the ocean may be more complex than previously appreciated
.

It is worth noting that some scholars have recently proposed that nitrite in the anaerobic area of ​​the ocean may generate oxygen through disproportionation, which in turn supports the active NOB metabolism in the anaerobic area of ​​the ocean
.

However, this theoretical mechanism remains to be experimentally verified
.

The detection of free O2 production in N.
maritimus raises a new scientific question whether this part of O2 produced by AOA can be used for nitrite oxidation in the anaerobic zone
.

Obviously, further analysis of the complex microbial nitrogen cycle network in the hypoxic marine environment and in-depth analysis of the process of global ocean nitrogen loss still depend on more research in the future
.

Currently known biological oxygen production processes mainly include the use of H2O to generate oxygen through photosystem II proteins, and related organisms include plants, algae, and cyanobacteria; the use of reactive oxygen species (ROS) to generate oxygen through catalase and superoxide dismutase.
; the use of perchlorate/chlorate to produce oxygen by microbial perchlorate/chlorate reductase; and the production of oxygen and nitrogen by nitrite-dependent methanotrophic bacteria through the process of nitric oxide disproportionation
.

However, except for two putative nitrite reductase homologous proteins, none of the genes encoding the above-mentioned key enzymes in the oxygen production process were found in the N.
maritimus genome, and the experimental data further ruled out the use of ROS production in this strain under hypoxic conditions.
the possibility of oxygen
.

Therefore, the process mechanism of N.
maritimus producing oxygen and nitrogen is still unclear
.

Due to the lack of biochemical research precedent, Kraft et al.
can only tentatively speculate on the underlying process mechanism of this pathway
.

Based on isotopic evidence, the authors propose the simplest and most thermodynamically feasible metabolic pathway, including nitrite reduction, conversion of NO to O2 and N2O, and then reduction of N2O to N2
.

Although this metabolic model confers the classical metabolic function of putative nitrite reductases in all mesophilic AOAs, its further biochemical mechanism remains unclear, which also provides a new insight into the hitherto incompletely elucidated archaeal ammonia oxidation pathway.
research ideas
.

Future research should further focus on whether this oxo-ammonium oxidation is limited to anoxic conditions, or is broadly associated with the classical archaeal ammonia oxidation process, and whether this metabolic mode is widespread in soils, sediments, and marine and terrestrial in the subsurface AOA
.

The intracellular oxygen production pathway detected in both distant nitrite-dependent methanotrophic bacteria and ammonia-oxidizing archaea suggests that this intracellular oxygen production (and simultaneous oxygen consumption) process may be widespread in a variety of microorganisms exist
.

Therefore, it is speculated that this metabolic mode may have been the main driving force for the evolution of the microbial nitrification process and the evolution of the Earth's nitrogen cycle before the increase in the Earth's oxygen concentration caused by the Great Oxidation Event 2.
4 billion years ago
.

About the Author Qin Wei is an Assistant Professor at the University of Oklahoma
.

2006-2010, Environmental Science, Beijing Normal University, B.
S.
; 2010-2016, University of Washington, Seattle, Environmental Microbiology, Ph.
D.
University of Washington School of Oceanography, Postdoctoral Fellow (Simons Foundation Postdoctoral Fellow); 2020-present, Department of Microbiology and Plant Biology, University of Oklahoma, Assistant Professor
.

As the core backbone, he has participated in a number of interdisciplinary research projects, including the NSF Dimensions of Biodiversity Program, the Simons Collaboration on Ocean Processes and the Simons Collaboration on Ocean Processes.
and Ecology; SCOPE); participated in 4 international cooperative ocean-going scientific expeditions; wrote 6 chapters of "Marine and Soil Ammonia-oxidizing Archaea Taxonomy, Physiology and Ecology" in Bergey's Manual of Systematic Bacteriology; Wrote Chapter 15 "Methods for the Characterization of Functional Microorganisms in the Process of Nitrogen Transformation"; published in the internationally renowned academic journals Science, PNAS, ISME Journal, Environmental Microbiology, Environmental Science and Technology, Water Research, Limnology and Oceanography Nearly 30 papers; invited to give academic reports at Caltech, Princeton University, Cornell University and other universities; served as a reviewer of NSF research projects, as well as Nature Communications, ISME Journal, Environmental Microbiology, Microbiome, mBio , Reviewer for academic journals such as Limnology and Oceanography
.

He has won the "National Outstanding Self-funded International Student Scholarship" (2016), "Simons Foundation Postdoctoral Fellowship in Marine Microbial Ecology, the first Chinese to receive this scholarship" (2017-2020), "American University Postdoctoral Fellowship in Marine Microbial Ecology" (2017-2020), "American University Postdoctoral Fellowship in Marine Microbial Ecology" national Oceanographic laboratory system chief scientist training program Fellowship (UNOLS chief scientist training program Fellowship) "(2019) and so on
.

Translation: Wang Baozhan, Wan Xianhui, Zheng Yue Editor in charge: Ma Tengfei Nanjing Agricultural University Review: Liu Yongxin Institute of Genetics and Development, Chinese Academy of Sciences Source: Metagenomics
.

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