Trace metal availability affects greenhouse gas emissions and microbial functional group abundance in freshwater wetland sediments

Abstract

We investigated the effects of trace metal additions on microbial nitrogen and carbon cycling using freshwater wetland sediment microcosms amended with μM concentrations of copper (Cu), molybdenum (Mo), iron (Fe), and all combinations. In addition to monitoring inorganic nitrogen transformations (NO3−, NO2−, N2O, NH4+) and carbon mineralization (CO2, CH4), we tracked changes in functional gene abundance associated with denitrification (nirS, nirK, nosZ), DNRA (nrfA), and methanogenesis (mcrA). Greater availability of Cu led to more complete denitrification (i.e., less N2O accumulation) and a higher abundance of the nirK and nosZ genes, which encode for Cu-dependent reductases. We found sparse evidence of DNRA activity and no consistent effect on CO2 production. Contrary, net CH4 production was stimulated by the trace metal amendments and the Mo additions, in particular, led to increased mcrA gene abundance. Taken together, these findings demonstrate that trace metal effects on microbial physiology, which have heretofore only been studied in pure culture, can impact community-level function. We observed direct and indirect effects on both nitrogen and carbon biogeochemistry that culminated in increased production of greenhouse gasses, and the shifts in functional group abundance that we documented suggest these responses may have been mediated through changes in microbial community composition. Overall, this work supports a more holistic consideration of metal effects on environmental microbial communities that recognizes the key role that metal limitation plays in microbial physiology.

Copper availability governs nitrous oxide accumulation in wetland soils and stream sediments

“…The limited set of studies on natural aquatic systems containing Cu at concentrations less than or equal to crustal abundances (441±63 nmol g -1 ) support our major finding that increased Cu concentrations can increase the extent of conversion of N2O to N2. At 26 µM dissolved Cu, Giannopoulos et al (2020) concluded that greater availability of Cu led to less N2O accumulation and higher abundance of Cu-dependent enzymes in wetland soils. A study on agricultural soils indicated that the application of organic fertilizer modified with 130 mM CuSO4 decreased N2O emissions substantially (Shen et al, 2020).…”

“…A recent study of freshwater wetland sediments that initially had 37.8 µg g -1 Cu and were amended with CuSO4 to have 26 µM dissolved Cu showed an increased abundance of nitrite and nitrous oxide reductase genes that enhanced the conversion of N2O to N2 (Giannopoulos et al, 2020). Similarly, a study of freshwater sediments collected from central Indiana also showed that N2O accumulation decreased when the sediments were amended with 50-100 µg g -1 Cu (Jacinthe and Tedesco, 2009).…”

“…The effects of redox conditions, substrate availability, temperature, and pH on denitrification have been widely studied (Nowicki, 1994;Koponen et al, 2004;Baeseman et al, 2006;Nag et al, 2017). There has also been significant progress in understanding the toxic effects of elevated Cu levels on the denitrification pathway, but only limited studies have investigated the effect of Cu availability on N2O accumulation in uncontaminated aquatic systems (Twining et al, 2007;Giannopoulos et al, 2020). A broader understanding of how Cu affects N-cycling in natural systems can improve the accuracy of ecosystem models, such as the Dynamic Land Ecosystem Model (DLEM) (Tian et al, 2020), used to estimate N2O emissions.…”

Trace Metal Availability Affects Greenhouse Gas Emissions and Microbial Functional Group Abundance in Freshwater Wetland Sediments

“…We also thank Colin McKenny for assistance in field and lab, Gabriella Balasa and Renia Passie for assistance with qPCR, Olivia De Meo for setting up the GC and HPLC procedures, and Dr. Scott Neubauer for GC and HPLC equipment access. This manuscript has been released as a pre-print at bioRxiv (#515809) (Giannopoulos et al, 2019).…”