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Microbial ecology

Metabolism of the deep

Nature volume 456, pages 712714 (11 December 2008) | Download Citation

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Certain microorganisms from the domain Archaea seem to be big players in the marine carbon and nitrogen cycles. A study linking their abundance in the deep sea to their likely metabolic profile refines this view.

The deep ocean covers two-thirds of our planet and teems with microbial life. Understanding the roles of deep-sea microbial communities is therefore essential for understanding global biogeochemical cycling, which in turn is pivotal for all other forms of life. Some of the most abundant creatures in the deep sea are the Crenarchaeota, microorganisms that belong to the domain Archaea. In recent years, it has been suggested1,2,3,4 that members of one major group of Crenarchaeota have a central role in the ocean's nitrogen cycle, because they perform the first step in the process that converts ammonia to nitrate. Furthermore, they were thought to be autotrophs (organisms that fix inorganic carbon for growth, rather than acquiring carbon from organic sources), thus also implicating them in the carbon cycle.

But on page 788 of this issue5, Agogué et al. propose that neither of these ideas is true for all Crenarchaeota. Their data suggest that some of these organisms — especially those residing in the deeper oceanic waters of the subtropical and tropical North Atlantic Ocean — do not carry genes for the main enzyme involved in ammonia oxidation, and that deep-sea Crenarchaeota depend on organic sources of carbon.

Agogué and colleagues' findings contribute to the current debate about the ecological role of Crenarchaeota in marine and terrestrial environments. Variants of genes that encode ammonia monooxygenase — the enzyme that oxidizes ammonia (Fig. 1) — were recently detected1,2,4,6 in archaeal genomes. When coupled with the fact that there are hundreds (and sometimes thousands) more archaea than ammonia-oxidizing bacteria in many terrestrial and marine environments, archaea suddenly emerged as probable major contributors to the nitrogen cycle2,3,5,7,8.

Figure 1: Nitrification in the global nitrogen cycle.
Figure 1

Ammonia oxidation is the first step of nitrification, the process in which ammonia (NH3, of organic origin) is oxidized to nitrate ions (NO3). Nitrification occurs on land and in the oceans and is essential for the global cycling of nitrogen. The process was long thought to be performed solely by bacteria, but certain archaea (Crenarchaeota) have recently been shown to be capable of ammonia oxidation, and to contain genes for ammonia monooxygenase (AMO, the key enzyme involved in ammonia oxidation). a, AMO converts ammonia into hydroxylamine (NH2OH). b, Hydroxylamine is converted by the same microorganisms into nitrite ions (NO2) — a protein that catalyses this process has not yet been found in archaea. c, Other specialized bacteria complete nitrification by converting nitrite ions to nitrate ions. d, The nitrate is then either assimilated into organic matter or denitrified by other microorganisms to produce nitrogen, which escapes into the atmosphere. e, 'Anammox' bacteria can also convert ammonia and nitrite ions into nitrogen. f, Nitrogen is fixed mostly by specialized bacteria, producing ammonia. This can be incorporated into organic matter, or oxidized as the cycle continues. Agogué et al.5 show that ammonia-oxidizing archaea are abundant in the North Atlantic Ocean, but not in the deep sea of equatorial regions.

This finding was surprising because, for the past hundred years, ammonia oxidation had been considered to be performed exclusively by specialist bacteria. The isolation and laboratory cultivation of ammonia-oxidizing archaea confirmed the hypothesis that certain Crenarchaeota are capable of generating energy through ammonia oxidation in an oxygen-dependent process, and thereby fix carbon from inorganic sources, just like their bacterial counterparts1,9,10. But it remained to be shown whether the high abundance of the archaeal amoA gene (which encodes ammonia monooxygenase) in the environment reflects a high archaeal contribution to ammonia oxidation. Furthermore, there was the question of whether all Crenarchaeota in moderate environments contribute to ammonia oxidation.

Apparently not. Agogué et al.5 do not find evidence for ammonia oxidizers in the deep sea of equatorial regions. They took water samples from different depths in the North Atlantic Ocean, and at latitudes ranging from polar regions down to the Equator. They then quantified the ratio of the number of archaeal amoA genes in the samples to the total number of Crenarchaeota, the latter number being determined by measuring the abundance of an RNA gene that is ubiquitous in these organisms.

The results5 indicate that the ratio decreases markedly from subpolar to equatorial regions, and also from subsurface waters to the deep ocean. Whereas the concentrations of amoA genes found at all depths in polar regions were high, they were 1,000 times lower than the concentration of total Crenarchaeota found in the bathypelagic waters (1,000–4,000 metres) of subtropical regions. The authors therefore conclude that most deep-sea Crenarchaeota in subtropical waters do not oxidize ammonia. Perhaps tellingly, the concentration of ammonia in subtropical deep waters is considerably lower than in the equivalent polar regions, where potential ammonia oxidizers are found in high numbers.

Agogué et al. also measured the ability of microorganisms taken from the locations described above to fix inorganic carbon. They found that the decreases in amoA abundance seen in their experiments5 mirror the observed patterns of carbon fixation — as the ability of marine microorganisms to fix carbon declines, so does the number of amoA genes in the archaeal population. This in turn suggests that deep-sea Crenarchaeota are not autotrophs.

Although these findings5 significantly refine our perception of crenarchaeotal metabolisms in the ocean, some caveats remain. The authors' gene-detection method assumes that archaeal amoA genes are similar to known amoA genes. But it is difficult to rule out the possibility that Agogué et al. simply missed specific variations of amoA genes that are typical of deep-water Crenarchaeota alone. Numerous cases exist in microbial ecology in which DNA-detection methods completely overlooked specific groups of genes, including amoA genes.

Similarly, Agogué and colleagues' data do not conclusively prove that deep-sea Crenarchaeota are not autotrophic. But their conclusions are supported by evidence from a series of previous studies11,12,13,14 that reported the incorporation of organic carbon sources into Crenarchaeota, thus indicating that at least some Crenarchaeota are heterotrophic — they take up organic carbon for growth.

It was not clear from the earlier studies11,12,13,14 whether heterotrophic growth is a fallback option for otherwise autotrophic, ammonia-oxidizing archaea, or whether distinct populations of Crenarchaeota exist that are strictly either heterotrophic or autotrophic. Agogué and colleagues' findings5 suggest the existence of specific heterotrophic Crenarchaeota, devoid of the amoA gene, that live preferably in deep ocean waters (see Suppl. Fig. S4 of Agogué et al.).

Nevertheless, the success of archaea in many disparate environments might still turn out to be based on the organisms' ability to switch from an autotrophic to a heterotrophic lifestyle, depending on environmental conditions. Several lines of evidence suggest that all (or most) soil Crenarchaeota are potential ammonia oxidizers7,8. Yet it is difficult to imagine that the large populations of these archaea in terrestrial habitats are merely based on this form of metabolism, especially where ammonia and/or oxygen concentrations are low. So although molecular studies such as those of Agogué et al. are undoubtedly valuable in raising hypotheses, additional techniques — including methods for probing isotope uptake by single cells, techniques for cultivating microorganisms in the laboratory, and biochemical analyses — will be indispensable for shedding light on the physiology and ecological impact of the ubiquitous and enigmatic Crenarchaeota.

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  1. Christa Schleper is in the Department of Genetics in Ecology, University of Vienna, Althanstrasse 14, A-1090 Vienna, Austria.  christa.schleper@univie.ac.at

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