A new source of 'new' nitrogen in the sea

David M. Karl

School of Ocean and Earth Science and Technology, Department of Oceanography, University of Hawaii, Honolulu, Hawaii 96822

Open-ocean ecosystems on Earth are characterized by low concentrations of fixed, bioavailable nitrogen (N), which would appear to make them a suitable niche for the proliferation of N₂-fixing prokaryotes. However, N₂-fixing prokaryotes also prefer environmental conditions defined by high phosphorus (P), high iron (Fe) and low oxygen (O₂); near-surface open-ocean habitats are chronically depleted in P and Fe and, typically, are well oxygenated (e.g. O₂ = 200-250 µm).

Historical investigations conducted in candidate tropical and subtropical habitats of the world's oceans have generally failed to support the ecological prediction of N₂-fixing microorganism dominance. Existing conceptual and mathematical models of biogeochemical cycling in the ocean therefore generally ignore N₂ fixation as a key metabolic process.

In their now-classic treatise on nutrient dynamics in the sea, Dugdale and Goering¹ introduced the unifying concept of 'new' (i.e. nutrients imported to the local environment from surrounding regions) vs 'regenerated' (i.e. nutrients that are locally remineralized) forms of nitrogen. They were careful to emphasize that there were several potential sources of new N for the euphoric zone, each of equal value but with potentially different ecological consequences. As there were few data on N₂-fixation rates when their paper was published, importation of nitrate from below the euphoric zone was considered to provide the majority of new N in the sea.

Now, thirty years after the new production concept was introduced, there is increasing evidence that rates of oceanic N₂ fixation could have been systematically underestimated or, perhaps, have increased in relative importance over time. This new evidence comes from several independent lines of investigation. One of the most interesting and provocative modern data sets is that derived from the application of novel molecular methods to detect the presence and abundance of N₂-fixing microorganisms either by hybridization or amplification of nitrogenase genes (nif; the enzyme system used to reduce N₂ to ammonia), as described by Zehr et al. in the February 2000 issue of this journal². Application of these methods to open-ocean biomes in the North Atlantic and North Pacific Oceans has revealed a spectrum of previously uncharacterized nif gene phylotypes. Furthermore, significant nif phylotype diversity was apparent both within and between open-ocean ecosystems. These novel data sets, when considered in concert with other recent reports of high rates of oceanic N₂ fixation, support the hypothesis that N₂ fixation is a major source of new N over vast regions of the world's oceans. It now appears that up to 50% of ecosystem new N could be derived from N₂ fixation^3-6 (D.M. Karl et al., unpublished). Dugdale and Goering¹ were careful to warn initially that if N₂ fixation was (later) found to be a quantitatively important pathway for nutrient supply, then a revision of the new vs recycled N conceptual framework would be necessary.

I submit that the time has come for a reconsideration of the new production paradigm. There is much at stake in this re-assessment. First, the net rate of carbon dioxide sequestration into the interior portion of the ocean is directly controlled by the source(s) of new N. If the nitrate flux dominates, there will be no net carbon sequestration because the bidirectional mass fluxes of C and N would be nearly in balance, as predicted by the new production-export production model⁷. Alternatively, if N₂ fixation sustains a significant amount of new and export production in open-ocean ecosystems, then net carbon dioxide will be sequestered. Furthermore, N₂ fixation in the world's oceans could be controlled by the atmospheric deposition of Fe, which itself is a variable, climate-sensitive parameter. Total atmospheric dust transport is also affected by humankind, including population demographics, global economies and land-use patterns. These complex natural and anthropogenic interactions, with multiple potential feedback loops, provide a mechanism for biogeochemical variability in otherwise 'stable and homogeneous' biomes. In this regard, the seascape might be a slave to the landscape, and there is no question that the latter has changed significantly over the past 250 years.

If the conceptual framework of new and regenerated production is discarded, it could take many years for it to be replaced with a new, ecumenical theory of nutrient dynamics in the sea. There is no doubt in my mind that additional, important discoveries of novel unexpected marine microorganisms will be made as we continue to explore our planet and these future discoveries might also challenge existing dogmas. One immediate and major task before us is to isolate and identify these recently discovered 'virtual' N₂-fixing microorganisms in order to move forward towards the much larger challenge of in situ processes. As Tom Brock correctly stated nearly 40 years ago, 'Ecology is physiology under the worst possible conditions'. The report by Zehr et al.² brings us a step closer to a more complete ecological understanding of Earth's largest biome.

References

¹ Dugdale, R.C. and Goering, J.J. (1967) Uptake of new and regenerated forms of nitrogen in primary productivity. Limnol. Oceanogr. 12, 196-206

² Zehr, J.P. et al. (2000) New perspectives on nitrogen-fixing microorganisms in tropical and subtropical oceans. Trends Microbiol. 8, 68-73

³ Michaels, A.F. et al. (1996) Inputs, losses and transformations of nitrogen and phosphorus in the pelagic North Atlantic Ocean. Biogeochem. 35, 181-226

⁴ Gruber, N. and Sarmiento, J.L. (1997) Global patterns of marine nitrogen fixation and denitrification. Global Biogeochem. Cycles 11, 235-266

⁵ Karl, D. et al. (1997) The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean. Nature 388, 533-538

⁶ Capone, D.G. and Carpenter, E.J. (1999) Nitrogen fixation by marine cyanobacteria: historical and global perspectives. Bull. Inst. Oceanogr. Monaco 19, 235-256

⁷ Eppley, R.W. and Peterson, B.J. (1979) Particulate organic matter flux and planktonic new production in the deep ocean. Nature 282, 677-680