Make way, make way; Nitrosopumilus maritimus (strain SCM1).

Understanding of the nitrogen cycle has been revised in the past few years by the discovery of ammonia oxidation carried out by archaea. Metagenomic studies of both seawater and soil have revealed the presence of putative ammonia monooxygenase genes (amoA) in uncultivated archaea, strongly suggesting that members of this domain possess the ability to oxidise ammonia. Analysis of the growth in pure culture of the first marine archaea to be cultured confirmed chemolithoautrophic growth employing aerobic oxidation of ammonia to nitrite.

The discovery of Nitrosopumilus maritimus (strain SCM1), by revealing significant gaps in our knowledge of microbial ammonia oxidation, now raises a variety of critical questions about the diversity, ecology, and evolutionary origins of ammonia oxidation-based metabolism. Until the discovery of ammonia oxidation (the first nitrification step of the nitrogen cycle), it was thought to be carried out only by bacterial autotrophs. Ammonia-oxidizing archaea (AOA) are members of the proposed novel Phylum Thaumarchaea, and are now recognized as a ubiquitous component of marine plankton, as well as being found in almost all environments. N. maritimus has a high copper-dependency for ammonia oxidation and electron transport, which is distinctly different from known ammonia-oxidizing bacteria.  

Analysis of sequenced genomes indicates that ammonia AOA may employ a unique biochemistry. Thaumarchaea contain the putative ammonia mono-oxygenase genes amoA, amoB and amoC, but lack the homologues used by bacteria to carry out the second step in the nitrification process, i.e. the components required for electron flow between hydroxylamine and ubiquinone. Unexpectedly, it appears that Nitrosopumilus maritimus utilizes a copper-based system of electron transport rather than the typical iron-based one prevalent in bacteria. Genome analysis has also indicated that AOA, although chemolithoautotrophs like ammonia-oxidizing bacteria, likely fix CO₂ in a different way from bacterial ammonia oxidisers, in which RuBisCo is the key enzyme. N. maritimus probably employs a mechanism similar but not identical to the 3-hydroxypropionate/4-hydroxybutyrate pathway of the hyperthermophile Metallosphaera sedula for autotrophic carbon assimilation.

AOA appear to be well adapted to oligotrophic environments with low oxygen, and Nitrosopumilus maritimus is uniquely capable of growth at the extremely low ammonia levels found in ocean waters. Positive correlations of archaeal cell counts and amo genes with nitrite maxima in the oceans were initially suggestive that most ammonia oxidation in this environment is archaeal-derived. Furthermore, the presence of AOA in extreme environments and various mesophilic biomes suggests that AOA are adapted to growth conditions that differ from those of ammonia-oxidizing bacteria, indicating niche separation. AOA have been found to be the dominant ammonia oxidisers in most surface soils. As soil depth increases, the number of AOA remains constant, whereas the number of ammonia-oxidizing bacteria decreases dramatically. The archaeal community seems to be dominant in soils with low nitrogen and low nitrification rates. The dominance of archaeal communities under limiting nutrition conditions can be attributed to their adaptation to chronic energy stress, and this might be a primary factor in differentiating bacterial and archaeal ecology.

Archaea are known to be involved in other parts of the nitrogen cycle. The discovery of nitrogen fixation in methanogens extended the distribution of this important activity to the archaeal domain, and more recently archaeal nitrogen fixation has been documented at hyperthermophilic temperatures. Unusual regulatory mechanisms have been reported for archaeal nitrogen fixation.

AOA typically greatly outnumber bacterial ammonia oxidisers in many common environments, and are among the most abundant micro-organisms on Earth. However, as they are difficult to cultivate, some aspects of their physiology and contribution to biogeochemical pathways are still speculative.

It is anticipated that the availability of a genome sequence will greatly accelerate studies of the physiology of this novel isolate, offer an important perspective on the origins and diversification of ammonia-oxidizing microorganisms, and provide an essential framework for interpreting partial genome sequence recovered from past and ongoing environmental surveys of environments inhabited by low-temperature Crenarchaeota. More generally, it should contribute to a better understanding of the biogeochemical cycling of nitrogen and carbon.

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Footnote: 

Two cultures of Nitrosopumilus maritimus strain SCM1 were grown in 500 ml of media in 1 L flasks. Genome sequencing was performed on high-molecular-weight DNA extracted from the two cultures and a completely sequenced and closed genome of N. maritimus was obtained through collaboration with the Joint Genome Institute. Whole-genome shotgun sequencing of 3-, 8-, and 40-kb DNA libraries produced at least 8× coverage of the entire genome.

References

Walker, C.B., de la Torre, J.R., Klotz, M.G., Urakawa, H., Pinel, N., Arp, D.J., Brochier-Armanet, C., Chain, P.S.G., Chan, P.P., Gollabgir, A., Hemp, J., Hugler, M., Karr, E.A., Konneke, M., Shin, M., Lawton, T.J., Lowe, T., Martens-Habbena, W., Sayavedra-Soto, L.A., Lang, D., Sievert, S.M., Rosenzweig, A.C., Manning, G. & Stahl, D.A. (2010). Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. PNAS 107(19), 8818-8823.