Search for: All records

Long-term anthropogenic nitrate (NO3−) enrichment is a serious threat to many coastal systems. Nitrate reduction coupled with the oxidation of reduced forms of sulfur is conducted by chemolithoautotrophic microbial populations in a process that decreases nitrogen (N) pollution. However, little is known about the diversity and distribution of microbes capable of carbon fixation within salt marsh sediment and how they respond to long-term NO3− loading. We used genome-resolved metagenomics to characterize the distribution, phylogenetic relationships, and adaptations important to microbial communities within NO3−-enriched sediment. We found NO3− reducing sulfur oxidizers became dominant members of the microbial community throughout the top 25 cm of the sediment following long-term NO3− enrichment. We also found that most of the chemolithoautotrophic genomes recovered contained striking metabolic versatility, including the potential for complete denitrification and evidence of mixotrophy. Phylogenetic reconstruction indicated that similar carbon fixation strategies and metabolic versatility can be found in several phylogenetic groups, but the genomes recovered here represent novel organisms. Our results suggest that the role of chemolithoautotrophy within NO3−-enriched salt marsh sediments may be quantitatively more important for retaining carbon and filtering NO3− than previously indicated and further inquiry is needed to explicitly measure their contribution to carbon turnover and removal of N pollution.

 

Abstract Excess reactive nitrogen (N) flows from agricultural, suburban, and urban systems to coasts, where it causes eutrophication. Coastal wetlands take up some of this N, thereby ameliorating the impacts on nearshore waters. Although the consequences of N on coastal wetlands have been extensively studied, the effect of the specific form of N is not often considered. Both oxidized N forms (nitrate, NO3−) and reduced forms (ammonium, NH4+) can relieve nutrient limitation and increase primary production. However, unlike NH4+, NO3− can also be used as an electron acceptor for microbial respiration. We present results demonstrating that, in salt marshes, microbes use NO3− to support organic matter decomposition and primary production is less stimulated than when enriched with reduced N. Understanding how different forms of N mediate the balance between primary production and decomposition is essential for managing coastal wetlands as N enrichment and sea level rise continue to assail our coasts. 

High‐throughput sequencing has enabled robust shotgun metagenomic sequencing that informs our understanding of the genetic basis of important biogeochemical processes. Slower to develop, however, are the application of these tools in a controlled experimental framework that pushes the field beyond exploratory analysis toward hypothesis‐driven research. We performed flow‐through reactor experiments to examine how salt marsh sediments from varying depths respond to nitrate addition and linked biogeochemical processes to this underlying genetic foundation. Understanding the mechanistic basis of carbon and nitrogen cycling in salt marsh sediments is critical for predicting how important ecosystem services provided by marshes, including carbon storage and nutrient removal, will respond to global change. Prior to the addition of nitrate, we used metagenomics to examine the functional potential of the sediment microbial community that occurred along a depth gradient, where organic matter reactivity changes due to decomposition. Metagenomic data indicated that genes encoding enzymes involved in respiration, including denitrification, were higher in shallow sediments, and genes indicative of resource limitation were greatest at depth. After 92 d of nitrate enrichment, we measured cumulative increases in dissolved inorganic carbon production, denitrification, and dissimilatory nitrate reduction to ammonium; these rates correlated strongly with genes that encode essential enzymes in these important pathways. Our results highlight the importance of controlled experiments in linking biogeochemical rates to underlying genetic pathways. Furthermore, they indicate the importance of nitrate as an electron acceptor in fueling microbial respiration, which has consequences for carbon and nitrogen cycling and fate in coastal marine systems.

 

Salt marshes sequester carbon at rates more than an order of magnitude greater than their terrestrial counterparts, helping to mitigate climate change. As nitrogen loading to coastal waters continues, primarily in the form of nitrate, it is unclear what effect it will have on carbon storage capacity of these highly productive systems. This uncertainty is largely driven by the dual role nitrate can play in biological processes, where it can serve as a nutrient‐stimulating primary production or a thermodynamically favorable electron acceptor fueling heterotrophic metabolism. Here, we used a controlled flow‐through reactor experiment to test the role of nitrate as an electron acceptor, and its effect on organic matter decomposition and the associated microbial community in salt marsh sediments. Organic matter decomposition significantly increased in response to nitrate, even at sediment depths typically considered resistant to decomposition. The use of isotope tracers suggests that this pattern was largely driven by stimulated denitrification. Nitrate addition also significantly altered the microbial community and decreased alpha diversity, selecting for taxa belonging to groups known to reduce nitrate and oxidize more complex forms of organic matter. Fourier Transform‐Infrared Spectroscopy further supported these results, suggesting that nitrate facilitated decomposition of complex organic matter compounds into more bioavailable forms. Taken together, these results suggest the existence of organic matter pools that only become accessible with nitrate and would otherwise remain stabilized in the sediment. The existence of such pools could have important implications for carbon storage, since greater decomposition rates as N loading increases may result in less overall burial of organic‐rich sediment. Given the extent of nitrogen loading along our coastlines, it is imperative that we better understand the resilience of salt marsh systems to nutrient enrichment, especially if we hope to rely on salt marshes, and other blue carbon systems, for long‐term carbon storage.