Nearly all of earth's plants respond to increases in the air's CO2 content by exhibiting increased rates of photosynthesis and biomass production. In addition, certain species that form symbiotic relationships with nitrogen-fixing bacteria find their ability to acquire nitrogen to be enhanced when exposed to CO2-enriched air. This phenomenon could increase the positive growth responses of these species to elevated CO2, as well as make more nitrogen available to co-occurring species and further enhance their positive growth responses to atmospheric CO2 enrichment. In this summary, therefore, we assemble and discuss the findings of some of the studies of these phenomena that have been conducted on aquatic plants in recent years, focusing on primary producers of marine environments.
Dupouy et al. (2000) note that marine biology may play a major role in regulating atmospheric CO2 over geologic time. They state, for example, that during interglacial periods, N2 fixation in the world's oceans is generally low, due to a low supply of iron compared to that of glacial periods. This state of affairs results in low surface productivity and little CO2 removal from the atmosphere. Hence, in an attempt to better understand where the world's oceans stand today in this regard, they describe some of their ongoing research projects geared to investigate this question.
The evidence the eight researchers have acquired to date suggests that marine N2 fixation may be much greater than what has generally been thought to be the case. In particular, they say that several Trichodesmium species of N2-fixing cyanobacteria have "a nearly ubiquitous distribution in the euphotic zone of tropical and subtropical seas and could play a major role in bringing new N to these oligotrophic systems." And this feat, in their words, "could play a significant role in enhancing new production."
The significance of these findings was presaged by the report of Pahlow and Riebesell (2000), who detected changes in deep-ocean Redfield ratios indicative of increasing nitrogen availability to the world's oceans over the last fifty years, as well as a concomitant increase in export production that appeared to be driving an increase in oceanic carbon sequestration. The latter investigators suggested that the growing supply of nitrogen needed to fuel this phenomenon had its origin in anthropogenic activities that release nitrous oxides to the air; but we speculated at the time of Dupouy et al.'s study that it may also be a consequence of the rising CO2 concentration of the atmosphere, by way of its potential to enhance aquatic productivity, including N2 fixation, as it does in the case of terrestrial productivity.
Further evidence for the possibility of an historical -- and still-ongoing -- CO2-induced enhancement of marine N2 fixation was provided by Lesser et al. (2004), who in their quest to determine the functions of certain bacteria associated with scleractinian corals, employed a number of techniques in a study of Montastraea cavernosa, including measurement of in vivo excitation/emission spectra, fluorescence lifetime analyses, epifluorescence microscopy, transmission electron microscopy, immunogold probing and ribosomal DNA sequencing. This array of investigative tools enabled them to identify "unicellular, nonheterocystis, symbiotic cyanobacteria within the host cells of the coral" that "coexist with the symbiotic dinoflagellates of the coral and express the nitrogen-fixing enzyme nitrogenase." They concluded that their results "clearly suggest that endosymbiotic cyanobacteria capable of fixing nitrogen are present in M. cavernosa and form a stable long-term association within host cells," noting that "this symbiont could potentially be a source of the limiting element nitrogen for the symbiosis through the release of fixed nitrogen products to the coral host."
The next "great leap forward" in the development of the concept of CO2-enhanced marine N2 fixation was taken by Levitan et al. (2007), who noted that "among the principal players contributing to global aquatic primary production, the nitrogen (N)-fixing organisms (diazotrophs) are important providers of new N to the oligotrophic areas of the oceans," citing several studies that demonstrate that "cyanobacterial (phototrophic) diazotrophs in particular fuel primary production and phytoplankton blooms which sustain oceanic food-webs and major economies and impact global carbon (C) and N cycling." These facts drove them to examine how the ongoing rise in the air's CO2 content might impact these relationships; and they began by exploring the response of the cyanobacterial diazotroph Trichodesmium to changes in the atmosphere's CO2 concentration, choosing this particular diazotroph because it dominates the world's tropical and sub-tropical oceans, contributing over 50% of total marine N fixation.
The eight Israeli and Czech researchers grew Trichodesmium stock cultures in YBCII medium (Chen et al., 1996) at 25°C and a 12-hour:12-hour light/dark cycle (with the light portion of the cycle in the range of 80-100 µmol photons m-2 s-1) in equilibrium with air of three different CO2 concentrations (250, 400 and 900 ppm, representing low, ambient and high concentrations, respectively), which was accomplished by continuously bubbling air of the three CO2 concentrations through the appropriate culture vessels throughout various experimental runs, each of which lasted a little over three weeks, during which time they periodically monitored a number of diazotrophic physiological processes and properties.
So what did the scientists learn? Levitan et al. report that Trichodesmium in the high CO2 treatment "displayed enhanced N fixation, longer trichomes, higher growth rates and biomass yields." In fact, they discovered that in the high CO2 treatment there was "a three- to four-fold increase in N fixation and a doubling of growth rates and biomass," and that the cultures in the low CO2 treatment reached a stationary growth phase after only five days, "while both ambient and high CO2 cultures exhibited exponential growth until day 15 before declining."
In discussing possible explanations for what they observed, the eight researchers suggested that "enhanced N fixation and growth in the high CO2 cultures occurs due to reallocation of energy and resources from carbon concentrating mechanisms required under low and ambient CO2." Consequently, they concluded, in their words, that "in oceanic regions, where light and nutrients such as P and Fe are not limiting, we expect the projected concentrations of CO2 to increase N fixation and growth of Trichodesmium," and that "other diazotrophs may be similarly affected, thereby enhancing inputs of new N and increasing primary productivity in the oceans." And to emphasize these points, they wrote in the concluding sentence of their paper that "Trichodesmium's dramatic response to elevated CO2 may consolidate its dominance in subtropical and tropical regions and its role in C and N cycling, fueling subsequent primary production, phytoplankton blooms, and sustaining oceanic food-webs."
Hard on the heels of Levitan et al.'s study came the report of Barcelos e Ramos et al. (2007), who reiterated that "Trichodesmium, a colony-forming cyanobacerium, fixes nitrogen in an area corresponding to almost half of earth's surface (Davis and McGillicuddy, 2006) and is estimated to account for more than half of the new production in parts of the oligotrophic tropical and subtropoical oceans (Capone et al., 2005; Mahaffey et al., 2005)," making it "the single most important nitrogen fixer in today's ocean."
Semi-continuous batch cultures of this all-important N2-fixing cyanobacterium were maintained for approximately two months in the exponential growth phase (by means of repeated sampling and dilution) throughout a range of conditions corresponding to atmospheric CO2 concentrations stretching from 140 to 850 ppm, while a number of the organism's physical, chemical and physiological characteristics were repeatedly measured. This protocol revealed, in the words of the five German researchers who conducted the work, that "over the experimental CO2 range (140 to 850 ppm), cell division rate of Trichodesmium increased about twofold," while "nitrogen fixation rate normalized to cellular phosphorus quota and chlorophyll a content increased threefold," which "corresponds to a 50% increase in P-normalized N2 fixation for atmospheric CO2 increasing from its present value (380 ppm) to that projected for 2100 (750 ppm) assuming a business as usual CO2 emission scenario."
In discussing their findings, Barcelos e Ramos et al. say their work shows that "not only Trichodesmium responds to rising CO2, but as one of the oldest life forms on planet earth, it is more sensitive than other groups previously considered (e.g., coccolithophores and diatoms)," and that "if the observed effect on Trichodesmium is a general phenomenon in diazotrophic cyanobacteria, our results would predict an increase in global ocean N2 fixation at CO2 levels expected for the future ocean," and that "this in turn, would increase the nitrogen inventory, resulting in increased future primary productivity and oceanic carbon sequestration," which "could thereby provide a strong negative feedback to atmospheric CO2 increase."
Most recently, Hutchins et al. (2007) have also reminded us that Trichodesmium species and other diazotrophic cyanobacteria support a large fraction of the total biological productivity of earth's tropical and subtropical seas, and that they exert a significant influence on the planet's carbon cycle by supplying much of the nitrogen that enables marine phytoplankton to maintain a level of productivity that removes vast amounts of CO2 from the atmosphere. Hence, they speculate that if either an increase in the air's CO2 content or its temperature would lead to an increase in oceanic N2 fixation, it would also lead to the biological extraction of more CO2 from the atmosphere and a tempering of the CO2 greenhouse effect via this negative feedback process.
To explore this intriguing possibility, the eight researchers grew cultures of both Pacific and Atlantic Ocean isolates of Trichodesmium ecotypes across a range of atmospheric CO2 concentrations characteristic of earth's past (150 ppm), its current state (380 ppm) and possible future conditions (750, 1250 and 1500 ppm) at two temperatures (25 and 29°C) and at sufficient and limiting phosphorus concentrations (20 and 0.2 µmol L-1 of phosphate, respectively), in situations where the carbonate buffer system parameters in their artificial seawater culture media were "virtually identical to those found in natural seawater across the relevant range of CO2 values."
As Hutchins et al. describe it, their work revealed that at atmospheric CO2 concentrations projected for the year 2100 (750 ppm), "N2 fixation rates of Pacific and Atlantic isolates increased 35-100%, and CO2 fixation rates increased 15-128% relative to present day CO2 conditions (380 ppm)." And in what they call one of their "most striking results," they found that "increased CO2 enhanced N2 and CO2 fixation and growth rates even under severely phosphorus-limited steady-state growth conditions [our italics]." They also report that "neither isolate could grow at 150 ppm CO2," but that "N2 and CO2 fixation rates, growth rates, and nitrogen:phosophorus ratios all increased significantly between 380 and 1500 ppm," and that "in contrast, these parameters were affected only minimally or not at all by a 4°C temperature change."
In discussing the implications of their findings, Hutchins et al. note that current global estimates of N2 fixation by Trichodesmium are about 60 x 109 kg N yr-1, and that if their experimental results can be extrapolated to the world's oceans, by 2100 this amount could increase to 81-120 x 109 kg N yr-1. In addition, they say that "if these estimates are coupled with modeling predictions of a 27% warming-induced expansion of suitable habitat (Boyd and Doney, 2002), calculations suggest that global N2 fixation by Trichodesmium alone could range from 103-152 x 109 kg N yr-1 by the end of this century," which is to be compared to recent estimates for total pelagic N2 fixation of 100-200 x 109 kg N yr-1 (Galloway et al., 2004). What is more, they note that free-living unicellular cyanobacteria in the ocean are believed to fix at least as much nitrogen as Trichodesmium (Montoya et al., 2004), and that endosymbiotic cyanobacteria also contribute substantially to N2 fixation. Hence, they conclude that "if N2 fixation rates in these groups show commensurate increases with rising CO2, the cumulative effect on the global nitrogen cycle could be considerably larger (e.g., a doubling)." In addition, they say their results suggest that "like N2 fixation, CO2 fixation by Trichodesmium should also increase dramatically in the future because of CO2 enrichment."
In light of these several observations, Hutchins et al. state in their concluding sentence that "many of our current concepts describing the interactions between oceanic nitrogen fixation, atmospheric CO2, nutrient biogeochemistry, and global climate may need re-evaluation to take into account these previously unrecognized feedback mechanisms between atmospheric composition and ocean biology."
How right they are!
References
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Last updated 19 March 2008