Exploring anaerobic CO2 production response to elevated nitrate levels in Gulf of Mexico coastal wetlands: Phenomena and relationships
Graphical abstract
Introduction
Wetlands play an important role on carbon (C) cycling in nature (Zhang et al., 2002). Despite being only about 6.4% of the terrestrial surface, wetlands account for 20–25% of the global organic C (OC) reservoir (Stocker et al., 2013). From a global warming perspective, wetland participates in C interactions between terrestrial ecosystem and atmosphere by serving as both a sink of atmospheric carbon dioxide (CO2) and an emitting source of methane (CH4) (Mitsch and Gosselink, 2007; Lenart, 2009; Junk et al., 2013; Meng et al., 2016). Carbon dioxide as the primary greenhouse gas (GHG), releases to atmosphere when wetland is under drainage (aerobic) or disturbed conditions (Page and Dalal, 2011) and CO2 efflux from saltwater wetland soils is a significant component of the global C budget (Alongi et al., 2004; Donato et al., 2011). Many factors affect C mineralization, including vegetation type (Neff and Hooper, 2002; Kandel et al., 2013), nutrient availability (Bridgham et al., 1998), microbial activity (Das et al., 2017), salinity (Weston et al., 2011; Wang et al., 2017), pH (Goodwin and Zeikus, 1987), and climate change (Keller et al., 2004). In particular, the CO2 production is closely related to the activity of decomposers in wetlands under anaerobic condition (Bridgham and Richardson, 1992), which depends on the availability of C sources (Qiu et al., 2015) as well as specific electron acceptors as a replacement of O2 to decompose organic matter in soil and oxidize the latter to CO2 (Ponnamperuma, 1972; Patrick and Reddy, 1978; Zehnder and Stumm, 1988). Nitrate (NO3−), which is a dominant and most preferred terminal electron acceptor based on its thermodynamic potency, can oxidize organic C in anoxic natural wetland soil (Kaplan et al., 1979; Seitzinger, 1988; Hamersley and Howes, 2005).
However, while the effects of exogenous NO3− on wetland CH4 emission is well known to be inhibitory, its effect on anaerobic CO2 production has been in debate (Dodla et al., 2009). Many studies have found that NO3− promotes CO2 production by increasing nutrient availability, which in turn enhances the microbial C demand with increased microbial activity in ecosystems (Treseder, 2008; Bridgham and Richardson, 2003). Positive correlations between NO3− availability and CO2 production were also found in several wetland soils (Swerts et al., 1996; Basiliko et al., 2005; Dettling et al., 2006). In contrast, there are also studies observing that added electron acceptors, including NO3−, SO42−, and Fe(III) in wetland soils did not cause an increase in CO2 production (D'Angelo and Reddy, 1999; Chidthaisong and Conrad, 2000; Vile et al., 2003). In a previous study, Dodla et al. (2009) reported a suppressive effect of NO3− on C mineralization in Louisiana coastal freshwater marsh soil. However, the extent of such phenomenon occurrence in the wide range spectrum of wetland ecosystems is unknown. There has been no systematical study to investigate such effects among different wetland ecosystems separated by a natural salinity gradient.
Wetland systems in Louisiana Gulf coastal area are characterized by various geographic distribution and are among the largest in the United States, stretching over 11,000 km2 from Vermillion Bay east to the Chandeluleur Islands (Wang et al., 2015). Part of these wetlands are subjected to disparate influence of NO3− brought in from Mississippi River diversion (Day et al., 2012). The NO3− is thought to be primarily originated from upstreams of both point and non-point sources such as wastewater treatment facilities and runoff of agriculture lands with irregular amount and frequency (David et al., 2010; Mitsch et al., 2001). On the other hand, some part of these wetlands has been affected by NO3− form direct discharge of secondarily treated disinfected, non-toxic municipal effluent from local processing facility for assimilation of nutrients (Hunter et al., 2018). The denitrification of these NO3− potentially cause destabilization of the marsh soils based on the fact that denitrification is coupled to the oxidation of organic matter (Bodker et al., 2015) and is influenced by degree of NO3− exposure (Day et al., 2018). In addition, Louisiana Gulf coastal wetlands are dominated with vegetation and salinity differences, such as swamp, freshwater, and saline marshes. Previous studies have observed different levels of major C gas fluxes between saline and freshwater marshes in Louisiana coastal wetlands (DeLaune and Smith, 1984). Thus, understanding the NO3− impacts on anaerobic CO2 production in these coastal wetlands of a natural salinity gradient is especially important for managing and utilizing these valuable wetland resources.
In this study, the soil CO2 respiration responses of Louisiana Gulf coastal wetland ecosystems (swamp and marshes) along a salinity gradient to elevated NO3− levels was investigated in a microcosm experiment. We also compared molecular composition of soil organic matter (SOM) and soil microbial community between the wetlands. It was hypothesized that the influence of NO3− on CO2 production would be determined by the intrinsic nutrient dynamics, organic C characteristics and associated soil microbiological properties within each of these wetland ecosystems. The overall objective was to explore and evaluate the links among soil CO2 respiration, organic matter chemistry, and microbial community in responding to NO3− levels in different anaerobic wetland ecosystems.
Section snippets
Soil sampling
Three wetland ecosystems, forest swamp (FS), freshwater marsh (FM), and saline marsh (SM) along a natural salinity gradient from the Barataria Basin of the Louisiana Gulf coast were selected for this study. Composite samples of 10 soil cores from top 0 to 25 cm depth at each site were collected. Samples were placed into zip-lock bags and transported to the lab on ice. Visible plant parts were removed and samples were thoroughly mixed before being used for the analysis. The major vegetation
Basic soil properties of study sites
Soil bulk density (BD) of the FS was much higher than those of marshes with similar BD between FM and SM soils (Table 1). The texture of FS soil was dominated by clay as compared to that of FM and SM soils. Saline marsh soil generally had a higher pH than the FM and FS soil. Soil electric conductivity (EC) differed among the three sites with a maximum of 38.9 dS m−1 in SM soil followed by FM soil (2.7 dS m−1) and FS (1.1 dS m−1). Among the three ecosystems, FM soil contained the highest TOC
Conclusion
This study confirmed different response of soils of forest swamp and marsh ecosystems to elevated NO3−. Addition of NO3− promoted CO2 production in forest swamp soil while it reduced CO2 respiration in marsh soils regardless of salinity variation. Further analysis indicated that the different response was due to underline inherent variation in soil DOM composition characteristics and microbial community structure between these wetlands. Specifically, swamp soil contained more polysaccharides,
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
The work was, in part, supported by the USDA National Institute of Food and Agriculture (NIFA)-Agricultural and Food Research Initiative (AFRI) Grant #2009-65102-05975 and the USDA National Institute of Food and Agriculture Hatch Project #10138880.
References (98)
- et al.
Sediment accumulation and organic material flux in a managed mangrove ecosystem: Estimates of land-ocean-atmosphere exchange in peninsular Malaysia
Mar. Geol.
(2004) - et al.
Nutrient-enhanced decomposition of plant biomass in a freshwater wetland
Aquat. Bot.
(2015) - et al.
Dissolved organic matter: biogeochemistry, dynamics, and environmental significance in soils
Adv. Agron.
(2011) - et al.
Mechanisms controlling soil respiration (CO2 and CH4) in southern peatlands
Soil Biol. Biochem.
(1992) - et al.
Turnover of glucose and acetate coupled to reduction of nitrate, ferric iron and sulfate and to methanogenesis in anoxic rice field soil
FEMS Microbiol. Ecol.
(2000) - et al.
Regulators of heterotrophic microbial potentials in wetland soils
Soil Biol. Biochem.
(1999) - et al.
Ecological response of forested wetlands with and without Large-Scale Mississippi River input: implications for management
Ecol. Eng.
(2012) - et al.
Can denitrification explain coastal wetland loss: a review of case studies in the Mississippi Delta and New England
Estuar. Coast. Shelf Sci.
(2018) - et al.
Denitrification potential and its relation to organic carbon quality in three coastal wetland soils
Sci. Total Environ.
(2008) - et al.
Carbon gas production under different electron acceptors in a freshwater marsh soil
Chemosphere
(2009)
Phospholipid fatty acid and infra-red spectroscopic analysis of a sulphate-reducing consortium
FEMS Microbiol. Lett.
Extractable and lipopolysaccharide fatty acid and hydroxy acid profiles from Desulfovibrio species
J. Lipid Res.
Influence of balsam poplar tannin fractions on carbon and nitrogen dynamics in Alaskan taiga floodplain soils
Soil Biol. Biochem.
Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests
For. Ecol. Manag.
Shifts in the structure of soil microbial communities in limed forests as revealed by phospholipid fatty acid analysis
Soil Biol. Biochem.
Characterization of the saccharide composition of heteropolysaccharides by pyrolysis-capillary gas chromatography-mass spectrometry
J. Anal. Appl. Pyrolysis
Fundamental and molecular composition characteristics of biochars produced from sugarcane and rice crop residues and by-products
Chemosphere
Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil
Soil Biol. Biochem.
Uncertain climate thresholds and optimal economic growth
J. Environ. Econ. Manag.
Contribution of lignin and polysaccharides to the refractory carbon pool in C-depleted arable soils
Soil Biol. Biochem.
Comparison of phylogenetic relationships based on phospholipid fatty acid profiles and ribosomal RNA sequence similarities among dissimilatory sulfate-reducing bacteria
FEMS Microbiol. Lett.
Organic matter turnover in soil physical fractions following woody plant invasion of grassland: evidence from natural 13C and 15N
Soil Biol. Biochem.
Use of fatty acids for identification of AM fungi and estimation of the biomass of AM spores in soil
Soil Biol. Biochem.
Humic-rich peat extracts inhibit sulfate reduction, methanogenesis, and anaerobic respiration but not acetogenesis in peat soils of a temperate bog
Soil Biol. Biochem.
Nitrogen and phosphorus fertilization of Sparganium eurycarpum Engelm. and Typha glauca Godr. Stands. I. Emergent plant production
Aquat. Bot.
The impact of farming practice on soil microorganisms and arbuscular mycorrhizal fungi: crop type versus long-term mineral and organic fertilization
Appl. Soil Ecol.
The chemistry of submerged soils
Adv. Agron.
Effects of plant-derived dissolved organic matter (DOM) on soil CO<inf>2</inf> and N<inf>2</inf>O emissions and soil carbon and nitrogen sequestrations
Appl. Soil Ecol.
Electron donors and acceptors influence anaerobic soil organic matter mineralization in tidal marshes
Soil Biol. Biochem.
Cellular fatty acid composition of Desulfovibrio species and its use in classification of sulfate-reducing bacteria
Syst. Appl. Microbiol.
An extraction method for measuring soil microbial biomass C
Soil Biol. Biochem.
Participation of iron in denitrification in waterlogged soil
Soil Biol. Biochem.
Signature fatty acids in phospholipids and lipopolysaccharides as indicators of microbial biomass and community structure in agricultural soils
Soil Biol. Biochem.
Changes in soil microbial community structure in a tallgrass prairie chronosequence
Soil Sci. Soc. Am. J.
The role of root exudates in rhizosphere interactions with plants and other organisms
Annu. Rev. Plant Biol.
Seasonal and inter-annual decomposition, microbial biomass, and nitrogen dynamics in a Canadian bog
Soil Sci.
Carbon sources for bacterial denitrification
A rapid method of total lipid extraction and purification
Can. J. Biochem. Physiol.
Endogenous versus exogenous nutrient control over decomposition and mineralization in North Carolina peatlands
Biogeochemistry
Carbon, nitrogen, and phosphorus mineralization in northern wetlands
Ecology
Microbial activity determining soil CO\textlessinf\textgreater2\textless/inf\textgreateremission in the Sundarban mangrove forest, India
Trop. Ecol.
Sources of nitrate yields in the Mississippi River Basin
J. Environ. Qual.
The carbon cycle and the rate of vertical accumulation of peat in the Mississippi River Deltaic Plain
Southeast. Geol.
Control of organic carbon mineralization by alternative electron acceptors in four peatlands, central New York state, USA
Wetlands
Molecular composition of humic acids from coastal wetland soils along a salinity gradient
Soil Sci. Soc. Am. J.
Mangroves among the most carbon-rich forests in the tropics
Nat. Geosci.
The variation of soil microbial respiration with depth in relation to soil carbon composition
Plant Soil
Pyrolysis-gas chromatography/mass spectrometry of soil organic matter extracted from a Brazilian mangrove and Spanish salt marshes
Soil Sci. Soc. Am. J.
Ecology of actinomycetes
Annu. Rev. Microbiol.
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