Linking soil process and microbial ecology in freshwater wetland ecosystems

Soil microorganisms mediate many processes such as nitrification, denitrification, and methanogenesis that regulate ecosystem functioning and also feed back to influence atmospheric chemistry. These processes are of particular interest in freshwater wetland ecosystems where nutrient cycling is highly responsive to fluctuating hydrology and nutrients and soil gas releases may be sensitive to climate warming. In this review we briefly summarize research from process and taxonomic approaches to the study of wetland biogeochemistry and microbial ecology, and highlight areas where further research is needed to increase our mechanistic understanding of wetland system functioning. Research in wetland biogeochemistry has most often been focused on processes (e.g., methanogenesis), and less often on microbial communities or on populations of specific microorganisms of interest. Research on process has focused on controls over, and rates of, denitrification, methanogenesis, and methanotrophy. There has been some work on sulfate and iron transformations and wetland enzyme activities. Work to date indicates an important process level role for hydrology and soil nutrient status. The impact of plant species composition on processes is potentially critical, but is as yet poorly understood. Research on microbial communities in wetland soils has primarily focused on bacteria responsible for methanogenesis, denitrification, and sulfate reduction. There has been less work on taxonomic groups such as those responsible for nitrogen fixation, or aerobic processes such as nitrification. Work on general community composition and on wetland mycorrhizal fungi is particularly sparse. The general goal of microbial research has been to understand how microbial groups respond to the environment. There has been relatively little work done on the interactions among environmental controls over process rates, environmental constraints on microbial activities and community composition, and changes in processes at the ecosystem level. Finding ways to link process-based and biochemical or gene-based assays is becoming increasingly important as we seek a mechanistic understanding of the response of wetland ecosystems to current and future anthropogenic perturbations. We discuss the potential of new approaches, and highlight areas for further research.     

Redox and temperature-sensitive changes in microbial communities and soil chemistry dictate greenhouse gas loss from thawed permafrost

Shelf seas and their associated benthic habitats represent key systems in the global carbon cycle. However, the quantification of the related stocks and flows of carbon are often poorly constrained. To address benthic carbon storage in the North–West European continental shelf, we have spatially predicted the mass of particulate organic carbon (POC) stored in the top 10 cm of shelf sediments in parts of the North Sea, English Channel and Celtic Sea using a Random Forest model, POC measurements on surface sediments from those seas and relevant predictor variables. The presented model explains 78% of the variance in the data and we estimate that approximately 250 Mt of POC are stored in surficial sediments of the study area (633,000 km²). Upscaling to the North–West European continental shelf area (1,111,812 km²) yielded a range of 230–882 Mt of POC with the most likely estimate being on the order of 476 Mt. We demonstrate that the largest POC stocks are associated with coarse-grained sediments due to their wide-spread occurrence and high dry bulk densities. Our results also highlight the importance of coastal sediments for carbon storage and sequestration. Important predictors for POC include mud content in surficial sediments, annual average bottom temperature and distance to shoreline, with the latter possibly a proxy for terrestrial inputs. Now that key variables in determining the spatial distribution of POC have been identified, it is possible to predict future changes to the POC stock, with the presented maps providing an accurate baseline against which to assess predicted changes.     

Interactions between soil physicochemistry and belowground biomass production in a freshwater tidal marsh

Plant and Soil - The success of tidal freshwater wetland restoration is typically gauged by the re-establishment of characteristics found in reference marshes. Although plant species composition...     

Soil microbial diversity affects soil organic matter decomposition in a silty grassland soil

Soil microorganisms play a pivotal role in soil organic matter (SOM) turn-over and their diversity is discussed as a key to the function of soil ecosystems. However, the extent to which SOM dynamics may be linked to changes in soil microbial diversity remains largely unknown. We characterized SOM degradation along a microbial diversity gradient in a two month incubation experiment under controlled laboratory conditions. A microbial diversity gradient was created by diluting soil suspension of a silty grassland soil. Microcosms containing the same sterilized soil were re-inoculated with one of the created microbial diversities, and were amended with ¹³C labeled wheat in order to assess whether SOM decomposition is linked to soil microbial diversity or not. Structural composition of wheat was assessed by solid-state ¹³C nuclear magnetic resonance, sugar and lignin content was quantified and labeled wheat contribution was determined by ¹³C compound specific analyses. Results showed decreased wheat O-alkyl-C with increasing microbial diversity. Total non-cellulosic sugar-C derived from wheat was not significantly influenced by microbial diversity. Carbon from wheat sugars (arabinose-C and xylose-C), however, was highest when microbial diversity was low, indicating reduced wheat sugar decomposition at low microbial diversity. Xylose-C was significantly correlated with the Shannon diversity index of the bacterial community. Soil lignin-C decreased irrespective of microbial diversity. At low microbial diversity the oxidation state of vanillyl–lignin units was significantly reduced. We conclude that microbial diversity alters bulk chemical structure, the decomposition of plant litter sugars and influences the microbial oxidation of total vanillyl–lignins, thus changing SOM composition.     

Alteration of bacterial communities and organic matter in microbial fuel cells (MFCs) supplied with soil and organic fertilizer

The alteration of the organic matter (OM) and the composition of bacterial community in microbial fuel cells (MFCs) supplied with soil (S) and a composted organic fertilizer (A) was examined at the beginning and at the end of 3 weeks of incubation under current-producing as well as no-current-producing conditions. Denaturing gradient gel electrophoresis revealed a significant alteration of the microbial community structure in MFCs generating electricity as compared with no-current-producing MFCs. The genetic diversity of cultivable bacterial communities was assessed by random amplified polymorphic DNA (RAPD) analysis of 106 bacterial isolates obtained by using both generic and elective media. Sequencing of the 16S rRNA genes of the more representative RAPD groups indicated that over 50.4% of the isolates from MFCs fed with S were Proteobacteria, 25.1% Firmicutes, and 24.5% Actinobacteria, whereas in MFCs supplied with A 100% of the dominant species belonged to γ-Proteobacteria. The chemical analysis performed by fractioning the OM and using thermal analysis showed that the amount of total organic carbon contained in the soluble phase of the electrochemically active chambers significantly decreased as compared to the no-current-producing systems, whereas the OM of the solid phase became more humified and aromatic along with electricity generation, suggesting a significant stimulation of a humification process of the OM. These findings demonstrated that electroactive bacteria are commonly present in aerobic organic substrates such as soil or a fertilizer and that MFCs could represent a powerful tool for exploring the mineralization and humification processes of the soil OM.     

Links between plant community composition,soil organic matter quality and microbial communities in contrasting tundra habitats

Plant communities, soil organic matter and microbial communities are predicted to be interlinked and to exhibit concordant patterns along major environmental gradients. We investigated the relationships between plant functional type composition, soil organic matter quality and decomposer community composition, and how these are related to major environmental variation in non-acid and acid soils derived from calcareous versus siliceous bedrocks, respectively. We analysed vegetation, organic matter and microbial community compositions from five non-acidic and five acidic heath sites in alpine tundra in northern Europe. Sequential organic matter fractionation was used to characterize organic matter quality and phospholipid fatty acid analysis to detect major variation in decomposer communities. Non-acidic and acidic heaths differed substantially in vegetation composition, and these disparities were associated with congruent shifts in soil organic matter and microbial communities. A high proportion of forbs in the vegetation was positively associated with low C:N and high soluble N:phenolics ratios in soil organic matter, and a high proportion of bacteria in the microbial community. On the contrary, dwarf shrub-rich vegetation was associated with high C:N and low soluble N:phenolics ratios, and a high proportion of fungi in the microbial community. Our study demonstrates a strong link between the plant community composition, soil organic matter quality, and microbial community composition, and that differences in one compartment are paralleled by changes in others. Variation in the forb-shrub gradient of vegetation may largely dictate variations in the chemical quality of organic matter and decomposer communities in tundra ecosystems. Soil pH, through its direct and indirect effects on plant and microbial communities, seems to function as an ultimate environmental driver that gives rise to and amplifies the interactions between above- and belowground systems. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Enhanced removal of organic matter and ammoniacal-nitrogen in a column experiment of tidal flow constructed wetland system

A tidal flow constructed wetland system was investigated for the removal of organic matter and ammoniacal-nitrogen from diluted piggery wastewater. The results demonstrated that the operation of tidal flow enhanced the transfer of oxygen into wetland matrices. The supply of oxygen by the operation (473 gO2/m2d) matched the demand for wastewater treatment. The overall oxygen consumption rate in the system was considerably higher than the typical rate obtainable in conventional wetlands; most oxygen being used for the decomposition of organic matter. Compared with conventional systems, the tidal flow system demonstrated greater efficiency in the removal of organic matter. Significant nitrification did not take place, although 27-48% ammonia was removed from the wastewater. Immobilization by microbial cells and adsorption were the likely routes to remove ammonia under the specific experiment conditions. Percentage removals of BOD5, NH4-N and SS increased after effluent recirculation at a ratio of 1:1 was employed.     

Polishing domestic wastewater on a subsurface flow constructed wetland: organic matter removal and microbial monitoring

Microbial monitoring of constructed wetlands (CWs) treating domestic wastewater is generally scarce, despite the need of more knowledge about its biocenosis. The sanitation quality of a wastewater treated in a CW is a crucial aspect, mainly when the receiving water body is used as a swimming and/or recreation area. The present study was carried out in a horizontal subsurface flow CWplanted with Phragmites australis receiving pre-treated domestic wastewater (mean flow 50 m3 day(-1)), from a population of about 300 inhabitants. The monitoring programme undertaken during the first year operation, revealed removal efficiencies of 61% BOD5, 44% COD, and 65% TSS for inlet water with ca. 90 mg L(-1) BOD5, 157 mg L(-1) COD, and 17 mg L(-1) TSS. Total Coliform (TC) and Faecal Coliform (FC) bacteria were removed from wastewater (mean inlet values of 5 x 10(6) CFU 100 mL(-1) TC and of 9 x 10(5) CFU 100 mL(-1) FC), with efficiencies of 92 and 97%, respectively. The dynamics of microbial communities established in the system assessed by polymerase chain reaction-denaturing gradient gel electrophoresis (PCR-DGGE), had revealed a high bacterial diversity within the system, with no relevant differences in composition at the CW inlet and outlet but exhibiting temporal differences in bacterial communities.     

The variability of soil microbial community composition of different types of tidal wetland in Chongming Dongtan and its effect on soil microbial respiration

Previous studies have shown that the soil enzyme activity and microbial respiration intensities varied in two different types of tidal wetland in Chongming Dongtan, the first a sandy soil in a scouring bank with Phragmites australis and the second a saline-alkali clay soil in silting bank with P. australis/Spartina alterniflora/Scirpus mariqueter, resulting in different organic carbon reservation capabilities; however, their microbial biomass did not differ significantly. To clarify the microbial mechanism that explains the variability of soil respiration among different wetland areas, the community structure and abundance of soil microorganisms in different types of wetland were investigated using denaturing gradient gel electrophoresis (DGGE) plus real-time quantitative polymerase chain reaction (PCR) technologies, and the relationship between soil environmental factors and the microbial community structure and the soil respiration intensity was elucidated. The results revealed that the soil microbial diversity and community structure differed between the two typical wetland areas. The common population was uncultured bacterium in both areas, and the most abundant community was α-, β-, γ-Proteobacteria, which play an important role in the cycling of carbon in soil. However, the abundance of α-Proteobacteria in Area A was 18.2% of that in Area B (P <0.05), while the β-Proteobacteria in Area A was 3.23 times higher than that in Area B (P <0.05). In addition, one cellulose-degrading bacteria, uncultured Bacilli, was detected in Area A. PCA (Principal component analysis) revealed that γ-Proteobacteria and β-Proteobacteria had the greatest impact on soil respiration intensity. Both soil water content and salinity depressed the propagation of β-Proteobacteria. Considering the similar microbial biomass and abundance of γ-Proteobacteria between the two areas, the lower level of β-Proteobacteria, uncultured Bacilli bacterium in Area B might be important factors involved in the lower soil respiration, and hence the higher soil organic carbon reservation capability in Area B.     

Endogeic earthworms shape bacterial functional communities and affect organic matter mineralization in a tropical soil

Priming effect (PE) is defined as a stimulation of the mineralization of soil organic matter (SOM) following a supply of fresh organic matter. This process can have important consequences on the fate of SOM and on the management of residues in agricultural soils, especially in tropical regions where soil fertility is essentially based on the management of organic matter. Earthworms are ecosystem engineers known to affect the dynamics of SOM. Endogeic earthworms ingest large amounts of soil and assimilate a part of organic matter it contains. During gut transit, microorganisms are transported to new substrates and their activity is stimulated by (i) the production of readily assimilable organic matter (mucus) and (ii) the possible presence of fresh organic residues in the ingested soil. The objective of our study was to see (i) whether earthworms impact the PE intensity when a fresh residue is added to a tropical soil and (ii) whether this impact is linked to a stimulation/inhibition of bacterial taxa, and which taxa are affected. A tropical soil from Madagascar was incubated in the laboratory, with a ¹³C wheat straw residue, in the presence or absence of a peregrine endogeic tropical earthworm, Pontoscolex corethrurus. Emissions of ¹²CO₂ and ¹³CO₂ were followed during 16 days. The coupling between DNA-SIP (stable isotope probing) and pyrosequencing showed that stimulation of both the mineralization of wheat residues and the PE can be linked to the stimulation of several groups especially belonging to the Bacteroidetes phylum.     

Evaluation of a lab-scale tidal flow constructed wetland performance: Oxygen transfer capacity, organic matter and ammonium removal

Oxygen transfer capacity and removal of ammonium and organic matter were investigated in this study to evaluate the performance of a lab-scale tidal flow constructed wetland. Average oxygen supply under tidal operation (350 g m⁻² d⁻¹) was much higher than in conventional constructed wetlands (<100 g m⁻² d⁻¹), resulting in enhanced removal of BOD₅ and NH₄⁺. Theoretical oxygen demand from BOD₅ removal and nitrification was approximately matched by the measured oxygen supply, which indicated aerobic consumption of BOD₅ and NH₄⁺ under tidal operation. When BOD₅ removal increased from 148 g m⁻² d⁻¹ to 294 g m⁻² d⁻¹, neither exhausted oxygen from the aggregate matrix during feeding period (111 g m⁻² d⁻¹) nor effluent dissolved oxygen (DO) concentration (2.8 mg/L) changed significantly, demonstrating that the oxygen transfer potential of the treatment system had not been exceeded. However, even though DO had not been exhausted, inhibition of nitrification was observed under high BOD loading. The loss of nitrification was attributed to excessive heterotrophic biofilm growth believed to induce oxygen transfer limitations or oxygen competition in thickened biofilms.     

Catabolic diversity of periphyton and detritus microbial communities in a subtropical wetland

The catabolic diversity of wetland microbial communities may be a sensitive indicator of nutrient loading or changes in environmental conditions. The objectives of this study were to assess the response of periphyton and microbial communities in water conservation area-2a (WCA-2a) of the Everglades to additions of C-substrates and inorganic nutrients. Carbon dioxide and CH₄ production rates were measured using 14 days incubation for periphyton, which typifies oligotrophic areas, and detritus, which is prevalent at P-impacted areas of WCA-2a. The wetland was characterized by decreasing P levels from peripheral to interior, oligotrophic areas. Microbial biomass and N mineralization rates were higher for oligotrophic periphyton than detritus. Methane production rates were also higher for unamended periphyton (80 mg CH₄-C kg⁻¹ d⁻¹) than detritus (22 mg CH₄-C kg⁻¹ d⁻¹), even though the organic matter content was higher for detritus (80%) than periphyton (69%). Carbon dioxide production for unamended periphyton (222 mg CO₂-C kg⁻¹ d⁻¹) was significantly greater than unamended detritus (84 mg CO₂-C kg⁻¹ d⁻¹). The response of the heterotrophic microbial community to added C-substrates was related to the nutrient status of the wetland, as substrate-induced respiration (SIR) was higher for detritus than periphyton. Amides and polysaccharides stimulated SIR more than other C-substrates, and methanogenesis was greater contributor to SIR for periphyton than detritus. Inorganic P addition stimulated CO₂ and CH₄ production for periphyton but not detritus, indicating a P limitation in the interior areas of WCA-2a. Continued nutrient loading into oligotrophic areas of WCA-2a or enhanced internal nutrient cycling may stimulate organic matter decomposition and further contribute to undesirable changes to the Everglades ecosystem caused by nutrient enrichment.     

The freshwater tidal wetland Liberty Island,CA was both a source and sink of inorganic and organic material to the San Francisco Estuary

It is hypothesized that perennial freshwater tidal wetland habitat exports inorganic and organic material needed to support the estuarine food web and to create favorable habitat for aquatic organisms in San Francisco Estuary. It is also hypothesized that most of the material flux in this river-dominated region is controlled by river flow. The production and export of material by Liberty Island were measured and compared using discrete monthly and continuous (15 min) measurements of a suite of inorganic and organic materials and flow between 2004 and 2005. Seasonal material flux was estimated from monthly discrete data for inorganic nutrients, suspended solids and salts, organic carbon and nitrogen and phytoplankton and zooplankton group carbon and chlorophyll a and pheophytin pigment. Estimates of material flux from monthly values were compared with measured daily material flux values for chlorophyll a concentration, salt and suspended solids obtained from continuous measurements (15 min) using YSI water quality sondes. Phytoplankton carbon produced within the wetland was estimated by in situ primary productivity. Most inorganic and organic materials were exported from the wetland on an annual basis, but the magnitude and direction varied seasonally. Dissolved inorganic nutrients such as nitrate, soluble phosphorus, total phosphorus and silica as well as total suspended solids were exported in the summer while total and dissolved organic carbon were exported in the winter. Salts like chloride and bromide were exported in the fall. Chlorophyll a and pheophytin were exported in the fall and associated with diatom and cyanobacteria carbon. Mesozooplankton carbon was dominated by calanoid copepods and exported most of the year except summer. Continuous sampling revealed high hourly and daily variation in chlorophyll a, salt and total suspended solids flux due to high frequency changes in concentration and tidal flow. In fact, tidal flow rather than river discharge was responsible for 90% or more of the material flux of the wetland. These studies indicate that freshwater tidal wetlands can be a source of inorganic and organic material but the export of material is highly variable spatially and temporally, varies most closely with tidal flow and requires high frequency measurements of both tidal flow and material concentration for accurate estimates.     

An oxygen-mediated positive feedback between elevated carbon dioxide and soil organic matter decomposition in a simulated anaerobic wetland

We examined the effects of elevated atmospheric CO₂ on soil carbon decomposition in an experimental anaerobic wetland system. Pots containing either bare C₄‐derived soil or the C₃ sedge Scirpus olneyi planted in C₄‐derived soil were incubated in greenhouse chambers at either ambient or twice‐ambient atmospheric CO₂. We measured CO₂ flux from each pot, quantified soil organic matter (SOM) mineralization using δ¹³C, and determined root and shoot biomass. SOM mineralization increased in response to elevated CO₂ by 83–218% (P<0.0001). In addition, soil redox potential was significantly and positively correlated with root biomass (P= 0.003). Our results (1) show that there is a positive feedback between elevated atmospheric CO₂ concentrations and wetland SOM decomposition and (2) suggest that this process is mediated by the release of oxygen from the roots of wetland plants. Because this feedback may occur in any wetland system, including peatlands, these results suggest a limitation on the size of the carbon sink presented by anaerobic wetland soils in a future elevated‐CO₂ atmosphere.     

Biological indicators of soil quality and soil organic matter characteristics in an agricultural management continuum

Relationships among biological indicators of soil quality and organic matter characteristics were evaluated across a continuum of long-term agricultural practices in Missouri, USA. In addition to chemical and physical soil quality indicators, dehydrogenase and phenol oxidase activity were measured, ¹³C nuclear magnetic resonance (¹³C NMR) and diffuse reflectance Fourier transform (DRIFT) spectra of soil organic matter were collected, and visible, near-infrared reflectance (VNIR) spectra of whole soil were collected. Enzyme activities were positively correlated with several soil quality indicators and labile fractions of soil organic matter (r = 0.58–0.92), and were negatively correlated with DRIFT indices of decomposition stage and recalcitrance (r = ?0.62 to ?0.76). A comparison of vegetative and land management practices was scored using the soil management assessment framework (SMAF)—a soil quality index. Perennial vegetation (i.e., native prairie, restored prairie, and timothy) plots exhibited the greatest soil quality (SMAF scores 93.6–98.6 out of 100), followed by no-till and conventionally cultivated plots, with wheat outranking corn. Among fertilization practices, soil quality followed the order: manure > inorganic fertilizer > unamended soil. Finally, in the estimation of soil properties, VNIR spectra generally outperformed DRIFT spectra using partial least squares regression (PLSR) and multiple, linear regression (MLR). The strongest estimates of dehydrogenase and phenol oxidase activity were found using MLR models of VNIR spectra (R² > 0.78, RPD > 2.20). Overall, this study demonstrates the potential utility and versatility of enzymes in modeling and assessing changes in soil organic carbon fractions and soil quality, and emphasizes the benefits of maintaining long-term agricultural experiments.     

Effects of floating vegetation on denitrification,nitrogen retention,and greenhouse gas production in wetland microcosms

Wetlands are biogeochemical hotspots that have been identified as important sites for both nitrogen (N) removal from surface waters and greenhouse gas (GHG) production. Floating vegetation (FV) commonly occurs in natural and constructed wetlands, but the effects of such vegetation on denitrification, N retention, and GHG production are unknown. To address this knowledge gap, we used microcosm experiments to examine how FV affects N and GHG dynamics. Denitrification and N retention rates were significantly higher in microcosms with FV (302 μmol N m^?2 h^?1 and 203 μmol N m^?2 h^?1, respectively) than in those without (63 μmol N m^?2 h^?1 and 170 μmol N m^?2 h^?1, respectively). GHG production rates were not significantly different between the two treatments. Denitrification rates were likely elevated due to decreased dissolved oxygen (DO) in microcosms with FV. The balance of photosynthesis and respiration was more important in affecting DO concentrations than decreased surface gas exchange. The denitrification fraction (N₂-N production: N retention) was higher in microcosms with FV (100 %) than those without (33 %) under increased (tripled) N loading. A 5 °C temperature increase resulted in significantly lower denitrification rates in the absence of FV and significantly lowered N₂O production with FV, but did not significantly change CH₄ production or N retention in either treatment. These results suggest that intentional introduction of FV in constructed wetlands could enhance N removal while leaving GHG production unchanged, an insight that should be further tested via in situ experiments.     

Leaf gas exchange characteristics and chlorophyll fluorescence of three wetland plants in response to long-term soil flooding

The effects of soil flooding on gas exchange and photosystem 2 (PS2) activity were analyzed in leaves of Phragmites australis, Carex cinerascens, and Hemarthria altissima. Pronounced decrease in net photosynthetic rate and stomatal conductance with flooding was found only in C. cinerascens. No significant changes in PS2 activity were observed in all three species which suggests that the photosynthetic apparatus was not damaged. Among the three species, H. altissima is better adapted to flooding than P. australis and C. cinerascens.     

Trade-offs in plant responses to herbivory influence trophic routes of production in a freshwater wetland

Responses of aquatic macrophytes to leaf herbivory may differ from those documented for terrestrial plants, in part, because the potential to maximize growth following herbivory may be limited by the stress of being rooted in flooded, anaerobic sediments. Herbivory on aquatic macrophytes may have ecosystem consequences by altering the allocation of nutrients and production of biomass within individual plants and changing the quality and quantity of aboveground biomass available to consumers or decomposers. To test the effects of leaf herbivory on plant growth and production, herbivory of a dominant macrophyte, Nymphaea odorata, by chrysomelid beetles and crambid moths was controlled during a 2-year field experiment. Plants exposed to herbivory maintained, or tended to increase, biomass and aboveground net primary production relative to controls, which resulted in 1.5 times more aboveground primary production entering the detrital pathway of the wetland. In a complementary greenhouse experiment, the effects of simulated leaf herbivory on total plant responses, including biomass and nutrient allocation, were investigated. Plants in the greenhouse responded to moderate herbivory by maintaining aboveground biomass relative to controls, but this response occurred at the expense of belowground growth. Results of these studies suggest that N. odorata may tolerate moderate levels of herbivory by reallocating biomass and resources aboveground, which in turn influences the quantity, quality and fate of organic matter available to herbivores and decomposers.