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The authors thank Dr X. Zhou for her support in maintaining the laboratory and field sites, S. Leibovitch for assistance in HPLC techniques and general cooperation from Bios Agriculture Inc., G. Stacey for provision of LCO samples to act as standards for our HPLC work, and R. Carlson for provision of artificial LCOs.
WHY DO LEGUME NODULES EVOLVE HYDROGEN GAS?
'Dept of Biology, Saint Mary's University, Halifax, NS, B3H 3C3 Canada
2Dept of Biology, Queen's University, Kingston, ON, K7L 3N6 Canada
1. H2 Evolution from ^-Fixation Systems
Hydrogen (H2) gas is an obligate byproduct of the N2-fixing enzyme, nitrogenase, claiming about 33% of the reducing power and ATP that flows to the enzyme. In some legume symbioses, the bacteria also produce an uptake hydrogenase (HUP) that is able to oxidize the H2 and thereby recover the reducing power used in H2 production. However, many N2 fixing legume nodules evolve H2 due to the absence (HUP") or low activity of the uptake hydrogenase (Arp 1992). In a HUP" symbiosis, large amounts of H2 can diffuse out of the nodule into the soil. For example, at peak growth every hectare of a N2-fixing soybean field will produce about 5000 L H2 d"1. This hydrogen evolution represents an energy equivalent to about 5% of the crop's net photosynthetic C gain for that day (Dong, Layzell 2001). It is interesting to note that the majority (>75%) of the rhizobia strains isolated from major soybean production areas in United States are HUP" (Uratsu et al. 1982). Also, all known clover and alfalfa symbioses are HUP".
The existence of HUP has been considered to be beneficial since it makes it possible for the symbiosis to recover at least a portion of the energy used for H2 production (Postgate 1998). Some laboratory studies have shown that HUP+ symbioses support a higher N content and enhanced legume growth (Albrecht et al. 1979; Bergersen et al. 1995), and many attempts have been made to introduce the HUP genes into endemic HUP" strains (Uratsu et al. 1982; Arp 1992). However, the expected benefits from HUP+ were not always apparent, especially in field studies and some studies showed negative effects of HUP on yield (Arp 1992).
Soil is a major sink for the H2 produced by legume nodules (Conrad et al. 1980). In fact, most soils are able to remove H2 from the atmosphere where it exists at a level of only 0.55 ppm H2. However, if a nodulated root system of a HUP" symbiosis is transplanted into non-legume soil, the If? produced by the nodules can be measured readily as a net evolution from the soil surface (Layzell, Atkins, Smith, Zhang, unpublished). In contrast, no H2 evolution can be detected from the surface of a soil that has supported the growth of a HUP" legume symbiosis.
La Favre et al. (1983) showed that H2 production from legume nodules induced H2 oxidation capacity of the soil, and that this capacity and the number of H2 oxidizing bacteria decreased exponentially with distance from the nodule. Soil microorganisms within a few cm of the legume nodules rapidly oxidized the H2. Popelier et al. (1985) found a highly significant positive correlation between the microbial biomass of the soil and the soil H2 uptake rate. Despite numerous attempts (Conrad et al. 1979a, 1979b, 1983; Haring, Conrad 1994; Haring et al. 1994; Kluber et al. 1995; Lechner, Conrad 1997), the microorganisms responsible for H2 oxidation in soils have yet to be identified and Conrad (1988) even questioned whether the H2 oxidation was, in fact, biological or chemical.
The H2 exposure rate of soil within a few cm of N2-fixing nodules has been calculated to be 30-250 nmoles cm"3 h"1 (Dong, Layzell 2001). A similar H2 exposure rate was used to treat a large volume of field soil (300 mL to 70 L) held within a plastic container. After 7 to 10 d of exposure, the H2 uptake rate of soil increased rapidly. After 3 weeks of H2 treatment, the apparent Km(H2) of soil had increased from 40.2 to 1028 ppm H2, and the Vmax of the treated soil increased from 4.35 to 836 nmoles H2 cm"3 h"1 (Dong, Layzell 2001). Similar results have also been reported in field soils adjacent to H2 evolving legume nodules (Conrad, Seiler 1979). These data suggest that the H2 treatment enhances the growth and hydrogenase activity of certain soil microorganisms.
The reducing power from H2 could be used in a number of biological reactions in soil, including ATP formation, lipid production, or the reduction of CO2 or N2. To assess the fate of the reducing power from H2, the exchange rates of CO2, O2 and H2, were measured simultaneously as a pretreated soil was provided with a range of H2 exposure rates (Dong, Layzell 2001). When the soil received an H2 exposure rate equivalent to that used in its pretreatment (147 nmoles H2 cm"3 h"1), 60% of the electrons from H2 were passed to O2 and 40% were used in CO2 fixation. At H2 exposure rates greater than this, net CO2 fixation was measured. This observation was consistent with higher C content following cultivation of HUP" legumes (Popelier et al. 1985), and in alfalfa-based rotation fields than the monoculture maize fields (Gregorich et al. 2001).
The additional microbial activity in the H2 treated soil was frequently associated with a greatly increased population of springtails, small insects of the order Collembola that feed on soil bacteria and fungi. Also, in field studies in which H2 was provided to soils, an increase in the nematode and earthworm populations were observed (Dong, Zhang, Layzell, unpublished).
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