Burnham MB, Simon SJ, Lee DK, Kent AD, DeLucia EH, Yang WH. 2022. Intra- and inter-annual variability of nitrification in the rhizosphere of field-grown bioenergy sorghum. Global Change Biology - Bioenergy. DOI: 10.1111/gcbb.12917
Burnham MB, Christ MJ, Adams MB, Peterjohn WT. 2021. Assessing the linkages between tree species composition and stream water nitrate in a reference watershed in Central Appalachia. Forests, special issue on Responses of Forest Ecosystems to Nitrogen Deposition. DOI 10.3390/f12081116
Burnham MB, Adams MB, Peterjohn WT. 2019. Assessing tree ring δ15N of four temperate deciduous species as an indicator of N saturation using independent long-term records of N cycling and loss. Oecologia 191(4):971-981. DOI 10.1007/s00442-019-04528-4
Burnham MB, Cumming JR, Adams MB, Peterjohn WT. 2017. Soluble soil aluminum alters the relative uptake of mineral nitrogen forms by six mature temperate broadleaf tree species: Possible implications for watershed nitrate retention. Oecologia 185(3): 327-337. DOI 10.1007/s00442-017-3955-8.
Burnham MB, McNeil BE, Adams MB, Peterjohn WT. 2016. The response of tree ring δ15N to a whole-watershed fertilization with urea at the Fernow Experimental Forest, WV. Biogeochemistry 130(1): 133-145.
Agriculture has a huge environmental impact. The transformation of native perennial prairies and woodlands into conventional annual cropping systems visibly changes the landscape and diversity of terrestrial ecosystems, but there are also profound changes underground that are not necessarily obvious at a glance. For instance, the addition of fertilizer to support crop yield represents a major change in the nitrogen cycle that contributes to nitrate leaching, which pollutes groundwater and downstream waterways, and gaseous nitrogen loss (including nitrous oxide) into the atmosphere, which contributes to climate change and ozone depletion. My work furthers our mechanistic understanding of soil biogeochemical processes to better assess the viability of bioenergy as a sustainable energy source.
The rhizosphere is the soil directly adjacent to and affected by plant roots, and it is a hotspot for nutrient cycling, microbial activity, and plant-microbe interactions. Sorghum bicolor, an annual crop that is being developed for biofuel production, can exude compounds out of its roots that inhibit nitrification, the microbial production of nitrate from ammonium. We call this biological nitrification inhibition (BNI). Since nitrate is mobile in soil and can leach into groundwater and into waterways, the inhibition of nitrate production is a possible environmental benefit of sorghum as a crop. Currently, I'm studying the extent to which sorghum inhibits nitrification, how the microbial community changes in the sorghum rhizosphere, and if nitrification inhibition has any measurable effect on overall ecosystem nitrate losses.
During the 2018 and 2019 growing seasons, implemented two field trials to study the inhibition of nitrification in the sorghum rhizosphere relative to bulk soil, and if nitrification inhibition responded to fertilization. Since nitrification is the production of nitrate (a mobile N form) from ammonium (a relatively immobile N form in soil), I expected that increasing N availability through fertilization would reduce the difference between bulk and rhizosphere soil nitrification if the plants are exuding BNI compounds for the purpose of increasing N retention in soil.
In general, we found that nitrification was significantly inhibited in the sorghum rhizosphere. Mid-season, during the period of maximum plant growth rates (late-July, shown in the figure at left), the inhibition was strongest. In 2018, fertilizer addition reduced the BNI effect, but there was no fertilizer effect in 2019. It was also clear that BNI was stronger in 2019, and we think that's because it was a very dry year, causing hydrophilic metabolites that inhibit nitrification to be retained in rhizosphere soil rather than diffuse or leach away.
A manuscript about this work is currently under review for publication, so check back soon for an update on that paper!
In a second field trial in 2019, we planted sorghum that was genetically modified by Tom Clemente's lab group at the University of Nebraska to reduce the production of one of the major hydrophobic BNI compounds, sorgoleone. We then compared rhizosphere BNI of this transgenic to its genetic background wild-type grain sorghum and also to hybrid maize. Interestingly, the transgenic sorghum inhibited nitrification to the same extent as the wild-type, and so we expect that two other BNI compounds, both of which are hydrophilic, play a significant role that is exaggerated even more during dry seasons like 2019. As expected, sorghum inhibited nitrification more than maize, especially mid-season.
From our work on sorghum BNI so far, we've learned that the plant does indeed inhibit nitrification in the field setting, which is an important advancement for BNI research. However, our field results show that BNI is much more complicated than laboratory or even greenhouse studies indicate, since plant phenology and interactions with climate, particularly precipitation and soil moisture, exert substantial control over the expression of BNI. Thus, in addition to scaling BNI effects to the ecosystem level, we are also evaluating different mechanisms of nitrification inhibition, including:
direct inhibition of ammonium oxidation (direct BNI)
suppression of nitrifier abundance by root exudates
direct competition for ammonium by heterotrophic microbes in the carbon-rich rhizosphere ecosystem
direct competition for ammonium by plant roots
When we talk about bioenergy, the first thing that usually comes to mind is how it is a renewable fuel source that could be more carbon-neutral than fossil fuels. However, farming also impacts the nitrogen cycle, causing nitrate leaching into groundwater and nitrous oxide emissions into the atmosphere. Nitrate is a pollutant that can cause methemoglobinemia (mostly in the developing world now) and contributes to algal blooms and the resulting aquatic and marine dead zones worldwide. Nitrous oxide is a potent greenhouse gas (~300-times as strong as carbon dioxide) and ozone-depleting compound. As such, we have to account for changes in the nitrogen cycle to fully understand the environmental sustainability of bioenergy feedstocks.
One of our initial findings in 2018 was that sorghum fields appear to be "leakier" than corn fields, meaning that despite being fertilized about half as much, sorghum loses just as much nitrous oxide as maize. It also appears that sorghum fields leach about the same amount of nitrate. As part of my work on biological nitrification inhibition, I also found that sorghum stimulated denitrification in the rhizosphere. Since soil moisture and soil dissolved organic carbon (DOC) heavily influence denitrification, we're taking thorough measurements of those factors in the 2020 growing season.
Compared to annual crop rotations, perennial bioenergy feedstocks require lower nitrogen fertilization, and thus exhibit lower rates of nitrate leaching and nitrogen gaseous losses. Despite the lack of fertilization, Miscanthus x giganteus maintains high yield through time, making it an environmentally desirable perennial feedstock for bioenergy production. By growing Miscanthus at the University of Illinois for ~10 years, we know that the amount of nitrogen harvested each year exceeds the supply of nitrogen through fertilization and deposition. So, the crop must be making up for this gap from some other source. Two potential avenues are nitrogen fixation, which is the microbial conversion of atmospheric nitrogen gas into organic nitrogen, or nitrogen mineralization, which is the transformation of organic nitrogen into ammonium.
We are studying nitrogen mineralization through time in Miscanthus stands of various ages (1, 3, and 10 years old), at the University of Illinois Energy Farm and the Iowa State University LAMPS field study. Early results show high mineralization rates in these crops, slightly declining nitrogen stocks, and increasing nitrogen isotope values through the soil profile, which could all be evidence of mining of soil nitrogen by Miscanthus. We are continuing to expand this work to determine if Miscanthus stimulates mineralization, if nitrogen fertilization reduces these effects, and how long Miscanthus crops could sustain high yield without fertilization.
My dissertation research focused on plant- to ecosystem-scale nitrogen dynamics in the temperate deciduous forests of central Appalachia.
For more info, check out my dissertation, my Oecologia paper on how aluminum affects nitrate uptake, my Biogeochemistry paper and Oecologia paper on using tree ring N isotopes to track past disturbances in the N cycle, and my Forests paper on linking watershed species composition to stream water nitrate export!