12.4.2: Marine
The marine nitrogen cycle has been widely investigated, as nitrogen is one of the main limiting factors of primary production in the upper sunlit layers of the oceans (Arrigo, 2005; Codispoti, 1997) and the ocean accounts for about half of the global net primary production (Field et al., 1998; Gruber and Galloway, 2008). In the traditional view, the marine nitrogen cycle includes nitrogen fixation as the main input of nitrogen in the ocean and dinitrogen gas formed by denitrification as the main output, so that these two pathways are mainly responsible for the marine nitrogen budget status (Karl et al., 1997). Codispoti et al. (2001) suggested that, in the present-day ocean, the nitrogen budget is not in a steady state but rather out of balance, with denitrification fluxes being underestimated . Nitrogen fixation is mediated by few microorganisms, including cyanobacteria, while denitrification is performed by a wide range of microorganisms with different metabolic features, able to switch from aerobic to anaerobic nitrate \(\left(\mathrm{NO}_3^{-}\right)\)-dependent respiration modes (Lam and Kuypers, 2011). In this classical view, nitrification, representing the major oxidative part of the cycle, connecting organic nitrogen to \(\mathrm{NO}_3^{-}\)(Codispoti et al., 2001; Lam and Kuypers, 2011), was seen exclusively as an aerobic process carried out by ammonia-oxidizing bacteria (AOB) and nitrite-oxidizing bacteria, members of the \(\beta\) - and \(\gamma\) proteobacteria. The nitrification reaction is divided into two steps, performed by distinct bacterial groups. In the first part, ammonium \(\left(\mathrm{NH}_4^{+}\right)\)is oxidized to nitrite \(\left(\mathrm{NO}_2^{-}\right)\), whereas in the second \(\mathrm{NO}_2^{-}\)is oxidized to nitrate \(\left(\mathrm{NO}_3^{-}\right)\). In both cases, oxygen serves as the electron acceptor, although AOB have been reported to perform nitrification in suboxic conditions (Lam et al., 2007; Schmidt and Bock, 1997).
The overall understanding of the marine nitrogen cycle has substantially changed in the last decade (Fig. 1). Specific archaea were discovered to be important players in the marine nitrogen cycle (Venter et al., 2004) as some of them perform nitrification in the marine water column and sediment (Francis et al., 2005; Könneke et al., 2005; Wuchter et al., 2006). The group of archaea capable of nitrification has recently been relocated in a separate phylum named Thaumarchaeota (Brochier-Armanet et al., 2008; Spang et al., 2010). Compared to their bacterial counterpart, ammonia-oxidizing archaea (AOA) are often more abundant in the ocean (Karner et al., 2001; Lam et al., 2007; Wuchter et al., 2006), accounting for \(20 \%\) of picoplankton and \(40 \%\) of the estimated total number of cells (Karner et al., 2001). These microorganisms are able to cope with low-oxygen conditions (Coolen et al., 2007; Lam et al., 2007; Park et al., 2010; Pitcher et al., 2011b; Sinninghe Damsté et al., 2002a), have low substrate requirements (Martens-Habbena et al., 2009) and are able to utilize a highly energy-efficient \(\mathrm{CO}_2\)-fixation pathway (Könneke et al., 2014); new coastal marine AOA isolates show obligate mixotrophy and vary in their adaptive ability to different environmental parameters (Qin et al., 2014). All these features have been suggested to provide a reason for the observed dominance of AOA over AOB as ammonia oxidizers in the open oceans (Könneke et al., 2014; Pester et al., 2011). Moreover, a "novel" process in the nitrogen cycle, named anammox, was discovered. Anaerobic ammonia oxidizing (anammox) bacteria are a unique group of microorganisms member of the order Planctomycetales (Strous et al., 1999). They are able to oxidize ammonium \(\left(\mathrm{NH}_4^{+}\right)\)to molecular nitrogen \(\left(\mathrm{N}_2\right)\) under anoxic conditions, using nitrite \(\left(\mathrm{NO}_2^{-}\right)\)as the electron acceptor (van de Graaf et al., 1995). Anammox bacterial activity has been detected in marine anoxic sediments and waters (Dalsgaard et al., 2003; Kuypers et al., 2003; Thamdrup and Dalsgaard, 2002) and has been recognized to contribute, along with denitrifying bacteria, to the loss of \(\mathrm{N}_2\) from the ocean (Galán et al., 2009; Hamersley et al., 2007; Kuypers et al., 2005; Lam et al., 2009; Thamdrup et al., 2006). Despite different oxygen tolerances, anammox bacteria and Thaumarchaeota have been observed to coexist in different settings, particularly in oxygen-deficient zones (ODZs) and anoxic waters (Coolen et al., 2007; Francis et al., 2005; Lam et al., 2007; Pitcher et al., 2011b; Woebken et al., 2007). These two microbial groups can potentially benefit from each other, because the thaumarchaeotal nitrification might be coupled with the anammox process by providing the \(\mathrm{NO}_2^{-}\)anammox bacteria need and, at the same time, consume oxygen, to which anammox bacteria are sensitive. Alternatively, when nitrite is provided to anammox by other sources, the two groups might compete for \(\mathrm{NH}_4^{+}\)(Yan et al., 2012).
References
Arrigo, K. R.: Marine microorganisms and global nutrient cycles, Nature, 437, 349–356, 2005.
Brochier-Armanet, C., Boussau, B., Gribaldo, S., and Forterre, P.: Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota, Nat. Rev. Microbiol., 6, 245–52, 2008.
Codispoti, L. A.: The limits to growth, Nature, 387, 237–238, 1997.
Codispoti, L. A., Brandes, J. A., Christensen, J. P., Devol, A. H., Naqvi, S. W. A., Paerl, H. W., and Yoshinari, T.: The oceanic fixed nitrogen and nitrous oxide budgets: moving targets as we enter the anthropocene?, Sci. Mar., 65, 85–105, 2001.
Coolen, M. J. L., Abbas, B., van Bleijswijk, J., Hopmans, E. C., Kuypers, M. M. M., Wakeham, S. G., and Sinninghe Damsté, J. S.: Putative ammonia-oxidizing Crenarchaeota in suboxic waters of the Black Sea: a basin-wide ecological study using 16S ribosomal and functional genes and membrane lipids., Environ. Microbiol., 9, 1001–16, 2007.
Dalsgaard, T., Canfield, D. E., Petersen, J., Thamdrup, B., and Acuña-González, J.: N2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica., Nature, 422, 606–8, 2003.
Field, C. B., Behernefeld, M. J., Randerson, J. T., and Falkowski, P. G.: Primary production of the biosphere: integrating terrestrial and oceanic components, Science, 281, 237–240, 1998.
Francis, C. A., Roberts, K. J., Beman, J. M., Santoro, A. E., and Oakley, B. B.: Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean, Proc. Natl. Acad. Sci. USA, 102, 14683–14688, 2005.
Galán, A., Molina, V., Thamdrup, B., Woebken, D., Lavik, G., Kuypers, M. M. M., and Ulloa, O.: Anammox bacteria and the anaerobic oxidation of ammonium in the oxygen minimum zone off northern Chile, Deep Sea Res. Part II Top. Stud. Oceanogr., 56, 1021–1031, 2009
Gruber, N. and Galloway, J. N.: An Earth-system perspective of the global nitrogen cycle, Nature, 451, 293–6, 2008.
Karl, D., Letelier, R., Tupas, L., Dore, J., Christian, J., and Hebel, D.: The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean, Nature, 388, 533–538, 1997
Karner, M. B., DeLong, E. F., and Karl, D. M.: Archaeal dominance in the mesopelagic zone of the Pacific Ocean, Nature, 409, 507– 10, 2001.
Könneke, M., Bernhard, A. E., de la Torre, J. R., Walker, C. B., Waterbury, J. B., and Stahl, D. A.: Isolation of an autotrophic ammonia-oxidizing marine archaeon, Nature, 437, 543–6, 2005.
Kuypers, M. M. M., Lavik, G., Woebken, D., Schmid, M., Fuchs, B. M., Amann, R., Jørgensen, B. B., and Jetten, M. S. M.: Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation, Proc. Natl. Acad. Sci. USA, 102, 6478–83, 2005.
Lam, P. and Kuypers, M. M. M.: Microbial nitrogen cycling processes in oxygen minimum zones, Ann. Rev. Mar. Sci., 3, 317– 345, 2011.
Lam, P., Lavik, G., Jensen, M. M., van de Vossenberg, J., Schmid, M., Woebken, D., Gutiérrez, D., Amann, R., Jetten, M. S. M., and Kuypers, M. M. M.: Revising the nitrogen cycle in the Peruvian oxygen minimum zone, Proc. Natl. Acad. Sci. USA, 106, 4752– 4757, 2009.
Lam, P., Jensen, M. M., Lavik, G., McGinnis, D. F., Müller, B., Schubert, C. J., Amann, R., Thamdrup, B., and Kuypers, M. M. M.: Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea, Proc. Natl. Acad. Sci. USA, 104, 7104–7109, 2007.
Martens-Habbena, W., Berube, P. M., Urakawa, H., de la Torre, J. R., and Stahl, D. A.: Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria., Nature, 461, 976–979, 2009.
Park, B.-J., Park, S.-J., Yoon, D.-N., Schouten, S., Sinninghe Damsté, J. S., and Rhee, S.-K.: Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in coculture with sulfur-oxidizing bacteria, Appl. Environ. Microbiol., 76, 7575–87, 2010.
Pester, M., Schleper, C., and Wagner, M.: The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology, Curr. Opin. Microbiol., 14, 300–306, 2011.
Pitcher, A., Villanueva, L., Hopmans, E. C., Schouten, S., Reichart, G.-J., and Sinninghe Damsté, J. S.: Niche segregation of ammonia-oxidizing archaea and anammox bacteria in the Arabian Sea oxygen minimum zone, ISME J., 5, 1896–904, 2011b.
Qin, W., Amin, S. A., Martens-Habbena, W., Walker, C. B., Urakawa, H., Devol, A. H., Ingalls, A. E., Moffett, J. W., Armbrust, E. V., and Stahl, D. A.: Marine ammonia-oxidizing archaeal isolates display obligate mixotrophy and wide ecotypic variation, Proc. Natl. Acad. Sci., 111, 12504–12509, 2014.
Schmidt, I. and Bock, E.: Anaerobic ammonia oxidation with nitrogen dioxide by Nitrosomonas eutropha, Arch. Microbiol., 167, 106–111, 1997.
Sinninghe Damsté, J. S., Strous, M., Rijpstra, W. I. C., Hopmans, E. C., Geenevasen, J. A. J., van Duin, A. C. T., van Niftrik, L., and Jetten, M. S. M.: Linearly concatenated cyclobutane lipids form a dense bacterial membrane, Nature, 419, 708–712, 2002c.
Spang, A., Hatzenpichler, R., Brochier-Armanet, C., Rattei, T., Tischler, P., Spieck, E., Streit, W., Stahl, D. A., Wagner, M., and Schleper, C.: Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota, Trends Microbiol., 18, 331–40, 2010.
Strous, M., Fuerst, J., Kramer, E. H. M., Logemann, S., Muyzer, G., van de Pas-Schoonen, K., Webb, R., Kuenen, J. G., and Jetten, M. S. M.: Missing lithotroph identified as new planctomycete, Nature, 400, 446–449, 1999.
Thamdrup, B., Dalsgaard, T., Jensen, M. M., Ulloa, O., Farías, L., and Escribano, R.: Anaerobic ammonium oxidation in the oxygen-deficient waters off northern Chile, Limnol. Oceanogr., 51, 2145–2156, 2006.
Thamdrup, B. and Dalsgaard, T.: Production of N2 through Anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments, Appl. Environ. Microbiol., 68, 1312–1318, 2002.
Van de Graaf, A. A., Mulder, A., de Bruijn, P., Jetten, M. S. M., Robertson, L. A., and Kuenen, J. G.: Anaerobic oxidation of ammonium is a biologically mediated process, Appl. Environ. Microbiol., 61, 1246–1251, 1995.
Venter, J. C., Remington, K., Heidelberg, J. F., Halpern, A. L., Rusch, D., Eisen, J. A., Wu, D., Paulsen, I., Nelson, K. E., Nelson, W., Fouts, D. E., Levy, S., Knap, A. H., Lomas, M. W., Nealson, K., White, O., Peterson, J., Hoffman, J., Parsons, R., Baden-Tillson, H., Pfannkoch, C., Rogers, Y.-H., and Smith, H. O.: Environmental genome shotgun sequencing of the Sargasso Sea., Science, 304, 66–74, 2004.
Woebken, D., Fuchs, B. M., Kuypers, M. M. M., and Amann, R.: Potential interactions of particle-associated anammox bacteria with bacterial and archaeal partners in the Namibian upwelling system, Appl. Environ. Microbiol., 73, 4648–4657, 2007.
Wuchter, C., Abbas, B., Coolen, M. J. L., Herfort, L., van Bleijswijk, J., Timmers, P., Strous, M., Teira, E., Herndl, G. J., Middelburg, J. J., Schouten, S., and Sinninghe Damsté, J. S.: Archaeal nitrification in the ocean, Proc. Natl. Acad. Sci. USA, 103, 12317–12322, 2006.
Yan, J., Haaijer, S. C. M., Op den Camp, H. J. M., van Niftrik, L., Stahl, D. A., Könneke, M., Rush, D., Sinninghe Damsté, J. S., Hu, Y. Y., and Jetten, M. S. M.: Mimicking the oxygen minimum zones: stimulating interaction of aerobic archaeal and anaerobic bacterial ammonia oxidizers in a laboratory-scale model system, Environ. Microbiol., 14, 3146–3158, 2012.
Excerpted from:
Sollai, M., Hopmans, E. C., Schouten, S., Keil, R. G., and Sinninghe Damsté, J. S.: Intact polar lipids of Thaumarchaeota and anammox bacteria as indicators of N cycling in the eastern tropical North Pacific oxygen-deficient zone, Biogeosciences, 12, 4725–4737, Accessed December 2023 at https://doi.org/10.5194/bg-12-4725-2015, 2015 . CC-BY-4.0