Hydrogen emission from nodulated soybeans [Glycine max (L.) Merr.] and consequences for the productivity of a subsequent maize (Zea mays L.) crop

Abstract

Hydrogen (H 2 ) is a by-product of the symbiotic nitrogen fixation (N 2 fixation) between legumes and root-nodule bacteria (rhizobia). Some rhizobial strains have an uptake hydrogenase enzyme (commonly referred to as Hup + ) that recycles H 2 within the nodules. Other rhizobia, described as Hup − , do not have the enzyme and the H 2 produced diffuses from the nodules into the soil where it is consumed by microorganisms. The effect of this phenomenon on the soil biota and on the soil itself, and consequent stimulation of plant growth, has been demonstrated previously. Soybeans [Glycine max (L.) Merr.] cv. Leichhardt, inoculated with either a Hup + strain (CB1809) or one of two Hup − strains (USDA442 or USDA16) of Bradyrhizobium japonicum and uninoculated soybeans, plus a non-legume control [capsicum (Capsicum annuum L.)] were grown in the field at Ayr, North Queensland, Australia. The objectives were to examine (1) relationships between N 2 fixation and H 2 emission, and (2) the influence H 2 -induced changes in soil might have during the legume phase and/or on the performance of a following crop. Strains CB1809 and USDA442 were highly effective in N 2 fixation ("good" fixers); USDA16 was partly effective ("poor" fixer). The soil had a large but nonuniformly distributed naturalised population of B. japonicum and most uninoculated control plants formed nodules that fixed some N 2 . These naturalised strains were classified as "poor fixers" of N 2 and were Hup + . H 2 emissions from nodules were assessed for all treatments when the soybean crop was 62 days old. Other parameters of symbiotic N 2 fixation and plant productivity were measured when the crop was 62 and 96 days old and at crop maturity. Immediately after final harvest, the land was sown to a crop of maize (Zea mays L.) in order to determine the consequences of H 2 emission from the soybean crop on maize growth. It was estimated that soybeans inoculated with USDA442, the highly effective Hupstrain of B. japonicum, fixed 117 kg shoot N/ha (or about 195 kg total N/ha if the fixed N associated with roots and nodules was taken into account), and contributed about 215,000 l H 2 gas per hectare to the ecosystem over the life of the crop. The volume of H 2 evolved from soybeans nodulated by the Hup + strain CB1809 was only 6% of that emitted by the USDA442 treatment, but there was no indication that soybean inoculated with USDA442 benefited from the additional H 2 input. The shoot biomass, grain yield, and amounts of N fixed (105 kg shoot N/ha, Plant Soil (175 kg total N/ha) by the CB1809 treatment were little less than for USDA442 plants. Three days after the soybean crop was harvested, the plots were oversown with maize along the same row lines in which the soybeans had grown. This procedure exposed the maize roots to whatever influence soybean H 2 emission might have had on the soil and/or the soil microflora immediately surrounding soybean nodules. The evidence for a positive effect of soybean H 2 emission on maize production was equivocal. While the consiste...

Detection of a Reproducible, Single-Member Shift in Soil Bacterial Communities Exposed to Low Levels of Hydrogen

“…Soil surrounding the roots of uninoculated soybean was also examined. Field measurements of H 2 emission from excavated nodulated root systems undertaken during early reproduction confirmed the relative Hup status of the inoculated B. japonicum strains (7.7 and 119.5 liters H 2 per hectare per hour for plants with nodules formed by CB1809 and USDA442, respectively [28]). The bacterial communities from the nodule surface, proximal soil (within 5 mm), and distant soil (greater than 5 cm from the nodules and roots) from the root systems, analyzed 62 and 96 days after sowing, did not group by either inoculant type or sampling time in a consensus dendrogram generated from the T-RFLP profiles (data not shown).…”

“…The QRS site is located at Ayr (147°23ЈE, 19°37ЈS), 90 km north of Townsville in the Burdekin Delta in tropical north Queensland with a mean annual precipitation of 950 mm. Descriptions of the soil physical and chemical characteristics at both locations can be found in previous publications (28,37).…”

“…Most of the H 2 emitted from legume root nodules is taken up by the surrounding soil, within a few centimeters of the nodule surface, and is not released to the atmosphere (20). Although the H 2 emitted by the rhizobial symbionts costs the legume approximately 5% of its daily photosynthate and "represents a significant investment by the plant" (9), there is growing evidence to suggest that soil exposed to H 2 is beneficial to plant growth, separate from the benefits derived from N 2 fixation (8,10,28). Previously, La Favre and Focht have hypothesized that "the hydrogen which is evolved during N 2 fixation represents an additional energy input into the plant-soil ecosystem .…”

“…A number of studies have found that when H 2 is taken up by soil, net CO 2 fixation occurs at the rate of 7 to 8 nmol CO 2 per g of soil per h (22,34). For a legume fixing 200 kg of atmospheric N 2 per hectare, over 200,000 liters of H 2 could be released into the legume's rhizosphere over the duration of the growing season and CO 2 fixation could result in an extra 25 kg of soil carbon fixed per hectare (9,10,28).…”

“…The soybean seeds were uninoculated or inoculated with either Bradyrhizobium japonicum strain CB1809, which possesses a hydrogenase uptake enzyme (designated Hup ϩ ) and recycles much of the H 2 generated during N 2 fixation, or strain USDA442, which lacks the hydrogenase uptake system (Hup Ϫ ) and emits H 2 from the root nodules (13). Full details of this field trial have been described previously (28).…”