3 Carbon fixation
Global estimates of carbon fixation by marine diazotrophs based on direct measurements have not been attempted to the author’s knowledge. There are few published estimates of carbon fixation (compared to N2 fixation) by Trichodesmium and global carbon fixation by this genus is generally estimated by multiplying the nitrogen fixation rate by some average C:N for Trichodesmium biomass. Modeling results assume N2 fixation equals denitrification, which corresponds to 480–960 Tg C year-1 (Mahaffey et al., 2005). Fortunately, the C:N ratio of Trichodesmium biomass, unlike the N:P ratios, falls within a narrow range (4.7 to 7.3; LaRoche and Breitbarth, 2005) with an average value of 6.3, very near the Redfield ratio (6.6). Unfortunately, as for N2 fixation, direct rate measurements of carbon fixation and carbon specific turnover times by Trichodesmium vary by orders of magnitude (Mulholland et al., 2006). Further, there is no consistent stoichiometric relationship between the ratio of C to N2 fixation (Table 3). Available paired estimates of N2 and C fixation suggest that in general, C:N fixation ratios far exceed the C:N ratio of cells (see also Mulholland et al., 2006). Consequently, geochemical estimates that rely on elemental stoichiometry to extrapolate N2 fixation from observations of carbon drawdown or the carbon cycle in general may be grossly in error (Mahaffey et al., 2005). For example, at the Bermuda Atlantic Time-Series Study (BATS) site, the observed rates of C drawdown were much higher than that which can be accounted for based on the observed rates of N2 fixation and Redfield stoichiometry. However, when the average observed ratio of carbon to N2 fixation rates measured at BATS (C:N2 fixation rates of 128) were used, the observed low rates of N2 fixation could indeed account for the observed carbon drawdown at BATS (Orcutt et al., 2001). Interestingly, the extrapolation of N2 fixation rates necessary to close C budgets may be seriously biased (overestimated) if the actual rate relationships between N2 and carbon fixation are NOT considered. The relationship between N and P may be even more complex.
There are a variety of reasons why there may be higherthan- stoichiometrically-expected carbon to N2 fixation ratios in nature. These include: factors resulting in underestimates of N2 fixation rates and rationalizations as to why Trichodesmium may have unusually high carbon fixation rates. Regarding the former, gross N2 fixation rates can be underestimated in 15N2 incubations if there is substantial N release (Glibert and Bronk, 1994; Mulholland et al., 2004a, 2006; see Sect. 4 below) or gross N utilization may be underestimated if alternative N sources are taken up (Mulholland and Capone, 1999; Mulholland et al., 1999a, b). On the other hand, carbon fixation rates may be stoichiometrically higher than expected, based on the elemental ratio of cells, if carbon is used as ballast for vertical migration (Villareal and Carpenter, 1990; Romans et al., 1994; Gallon et al., 1996), if substantial carbon is excreted as mucilage or extracellular polymeric substances (Stal, 1995; Sellner, 1997), to support the high observed respiration rates by Trichodesmium (Kana, 1993; Carpenter and Roenneberg, 1995), or if cells “overfix” carbon to support Mehler reactions to reduce cellular oxygen concentrations or support the production of ATP (Kana, 1992, 1993). Kana (1993) estimated that 48% of gross photosynthetic electron flow went to oxygen reduction. Trichodesmium also make poly-beta-hydroxybutyric acid as a storage product (Siddiqui et al., 1992) and this may be important in carbohydrate ballasting (Romans et al., 1994) but would require additional cellular carbon reserves. In addition to these physiological reasons why carbon might be “overfixed” relative to nitrogen, active release of carbon compounds and photosynthate has been observed and will be discussed below in Sect. 5. Alternatively, N and C uptake may not be tightly coupled in diazotrophic cyanobacteria (Gallon et al., 2002).
An interesting genomic finding is that Trichodesmium erythraeum is unusual among cyanobacteria in that it lacks any genes encoding known high-affinity carbon concentrating mechanisms (Badger and Price, 2003). While it is not clear how this affects photosynthetic C acquisition by Trichodesmium, it suggests this species is vulnerable to C limitation. Continuous carbon fixation or storage of fixed carbon compounds, even in excess of their growth requirements, may protect them from carbon limitation in nature. Although carbon limitation has not been demonstrated for these species in nature, the interiors of Trichodesmium colonies have been shown to exhibit oxygen dynamics that may be important for aerobic N2 fixation (Paerl and Bebout, 1988; Carpenter et al., 1990; Gallon, 1992).
Although the ultimate biogeochemical fate of Trichodesmium-fixed elements is not fully understood (Mahaffey et al., 2005; Mulholland et al., 2006), any fraction of new production from diazotrophy that is exported (e.g., Eppley and Peterson, 1979) to underlying waters will contribute to sequestering atmospheric carbon and so it is important that we gain a better understanding of the coupled N and C cycles for these organisms.