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Nutrient Cycles and Marine Microbes in a Co or collective redistirbution of any portion of this article by photocopy machine, reposting, or other means is permitted only with the approval of The approval portionthe ofwith any articlepermitted only photocopy by is of machine, reposting, this means or collective or other redistirbution This article has This been published in SPECIAL IssUE FEATURE Oceanography , Volume 22, Number 4, a quarterly journal of The 22, Number 4, a quarterly , Volume Nutrient Cycles and O ceanography Society. ceanography Marine Microbes in a © 2009 by The 2009 by CO -Enriched Ocean O 2 Society. ceanography BY DAVID A. HUTCHIns, MARGARET R. MULHOLLAnd, And FEIXUE FU O ceanography Society. Send all correspondence to: [email protected] or Th e [email protected] Send Society. ceanography to: correspondence all A ll rights reserved. P ermission is granted to copy this article for use in teaching and research. article for use research. and this copy in teaching to granted is ermission O ceanography Society, Society, ceanography PO Box 1931, R epublication, systemmatic reproduction, reproduction, systemmatic epublication, R ockville, MD 20849-1931, U S A . 128 Oceanography Vol.22, No.4 AbsTRACT The ocean carbon cycle is tightly linked with the cycles of the major nutrient elements CO2 using sunlight as an energy source, nitrogen, phosphorus, and silicon. It is therefore likely that enrichment of the ocean while chemoautotrophic bacteria and with anthropogenic CO2 and attendant acidification will have large consequences archaea do the same thing using chem- for marine nutrient biogeochemistry, and for the microbes that mediate many key ical sources of energy. Together, these nutrient transformations. The best available evidence suggests that the nitrogen cycle two broadly defined functional groups may respond strongly to higher CO2 through increases in global N2 fixation and provide the raw materials and energy possibly denitrification, as well as potential decreases in nitrification. These trends that fuel all of the ocean’s food webs. could cause nitrification to become a nitrogen cycle “bottleneck,” by increasing the For autotrophic groups that depend on flux of 2N fixed into ammonium while decreasing the fraction being oxidized to carbon fixation for a living, rising partial nitrite and nitrate. The consequences could include reduced supplies of oxidized pressure of CO2 (pCO2) in the ocean nitrogen substrates to denitrifiers, lower levels of nitrate-supported new primary may actually represent an opportunity production, and expansion of the regenerated production system accompanied by rather than a misfortune. The term shifts in current phytoplankton communities. The phosphorus and silicon cycles seem “ocean acidification” carries undeniably less likely to be directly affected by enhanced CO2 conditions, but will undoubtedly negative connotations, and indeed it is respond indirectly to changing carbon and nitrogen biogeochemistry. A review of hard to envision how most animals and culture experiments that examined the effects of increased CO2 on elemental ratios microbial heterotrophs could benefit of phytoplankton suggests that for most cyanobacteria and eukaryotes, C:N and N:P from lowered ocean pH. However, ratios will either remain at Redfield values or increase substantially. Natural plankton dissolved inorganic carbon enrich- community CO2 manipulation experiments show much more mixed outcomes, with ment is an equally accurate description both increases and decreases in C:N and N:P ratios reported at future CO2 levels. We of anthropogenic input of CO2 to the conclude our review with projections of overall trends in the cycles of nitrogen, phos- ocean, and this terminology evokes a phorus, and silicon over the next century as they respond to the steady accumulation much different image of how communi- of fossil-fuel-derived CO2 in a rapidly changing ocean. ties might respond. Much of our view of ocean acidification as an unmitigated stressor for marine life comes from InTRODUCTION nitrogen, phosphorus, and silicon. well-justified concern over its negative The accumulation of fossil-fuel-derived Consequently, the ongoing and accel- impacts on corals and other calcifying CO2 in the sea and consequent ocean erating enrichment of seawater with organisms (Kleypas et al., 1999; Feely acidification represents an unprec- anthropogenic CO2 will likely have far- et al., 2004; Fabry et al., 2008). It is edented human perturbation of ocean reaching effects not only on the carbon important to remember, though, that chemistry on a global scale. A funda- cycle, but also on the cycles of these for many of the autotrophs that power mental theme of modern oceanography biologically required nutrients. the cycles of carbon and nutrients in the that dates back to the classic work of Many of the key pathways and ocean and support virtually all marine Redfield (1958) is a recognition of the transformations in ocean nutrient biological productivity, the term “CO2 intimate interweaving of the marine cycles are mediated by autotrophs. fertilization” may be more appropriate. biogeochemical cycle of carbon with the Photoautotrophs, including cyanobac- There are several comprehensive recent cycles of the major nutrient elements teria and eukaryotic phytoplankton, fix reviews on the effects of changing pCO2 Oceanography December 2009 129 THE MARINE NITROGEN CYCLE – on phytoplankton physiology, including +5 NO3 Riebesell (2004) and Rost et al. (2008). +4 tion In this article we explore what is n currently known about the implica- +3 – Nitrica NO2 tions of ocean acidification and CO2 Assimilation e fertilization for the biogeochemical +2 DenitricatioNO cycles of nitrogen, phosphorus, and Assimilation silicon, and for the keystone marine +1 N2O organisms that mediate them, including photoautotrophs, chemoautotrophs, and 0 N2 Anammox Oxidation Stat Oxidation heterotrophs. Along with the rapidly -1 Nitrication mounting concern about ocean acidifi- N 2 F ixation cation, the marine science community -2 has produced a flood of new informa- Assimilation tion from experimental studies in both Organic -3 NH3 the laboratory and the field. These + Nitrogen NH 4 Degradation novel results are helping to provide the perspective we need to make educated Figure 1. Major chemical forms and transformations of nitrogen in the ocean. The guesses in response to such questions as: various chemical forms of nitrogen are plotted versus their oxidation states. Here, we consider the potential effects of increased oceanp CO2 on three of the critical How will crucial processes in the marine transformations within the N cycle: N2 fixation (red arrow), nitrification (blue nitrogen cycle, including nitrogen fixa- arrows), and denitrification (green arrow). tion, nitrification, and denitrification, respond to ocean acidification? Will the cycles of phosphorus and silicon change in response to anthropogenic CO2 CO2 enrichment and concomitant ocean physiology and biological community inputs, and if so, how? How will elevated acidification. We acknowledge that our structure could have major impacts on pCO2 affect the C:N:P stoichiometry of projections are speculative, as we recog- ocean biogeochemical cycles. phytoplankton in the ocean? Finally, we nize that many large gaps remain in this New nitrogen enters the ocean conclude this review with a projection developing picture, and there is a need through the fixation of atmospheric of how nutrient biogeochemistry might for additional work to fill these gaps. dinitrogen (N2) by marine N2 fixers, be altered in the future in response to also known as diazotrophs (Figure 1, ThE NITROGEN CYCLE red arrow). Nitrogen losses from the David A. Hutchins ([email protected]) The potential for ocean acidification ocean are through organisms that – is Professor of Marine Environmental to affect multiple processes within reduce oxidized N (primarily NO3) to Biology, Department of Biological the marine nitrogen cycle is obvious, N2 through classical denitrification, Sciences, University of Southern because this complex cycle involves an anaerobic process (Figure 1, green California, Los Angeles, CA, USA. compounds that are stable across eight arrow). Further losses of fixed N from the Margaret R. Mulholland is Associate oxidation states (Figure 1). Microbes ocean occur through anaerobic ammo- + Professor, Department of Ocean, Earth, are the primary mediators of the cycling nium (NH4) oxidation via so-called and Atmospheric Sciences, Old Dominion of nitrogen between compounds, and “anammox.” Once input into the ocean, University, Norfolk, VA, USA. Feixue Fu is through their metabolisms the nitrogen nitrogen is cycled through microbial and Research Assistant Professor, Department and carbon cycles are inextricably food web interactions. Nitrogen taken up of Biological Sciences, University of linked. Consequently, CO2 enrichment into particulate material and microbial Southern California, Los Angeles, CA, USA. or acidification-related shifts in both cell biomass is released and regenerated 130 Oceanography Vol.22, No.4 a as ammonium and dissolved organic 120 compounds. In aerobic waters, nitrifying bacteria and archaea can then oxidize tes (%) 100 ammonium, producing first nitrite Ra – – 80 (NO2) and then nitrate (NO3) (Figure 1, blue arrows). Here, we evaluate the state ixation F 60 of our current knowledge about how 2 N ocean uptake of anthropogenic CO2 40 and attendant acidification could affect three of the fundamental nitrogen cycle 20 Increase in processes shown in Figure 1: N2
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