Journal of Environmental Quality 30:648-655 (2001)
© 2001 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
TECHNICAL REPORT
WASTE MANAGEMENT
Nutrient Conversions by Photosynthetic Bacteria in a Concentrated Animal Feeding Operation Lagoon System
J.L. Sunda,
C.J. Evensona,
K.A. Strevetta,
R.W. Nairna,
D. Athaya and
E. Trawinskib
a School of Civil Engineering and Environmental Science, College of Engineering, Univ. of Oklahoma, 202 W. Boyd Rm. 334, Norman, OK 73019
b Dep. of Chemical Engineering, Rensselaer Polytechnic Institute, 110 8th St, Troy, NY 12180
Corresponding author (strevett{at}ou.edu)
Received for publication May 4, 2000.
 |
ABSTRACT
|
|---|
A diurnal examination was conducted to determine the effect of photosynthetic bacteria on nutrient conversions in a two-stage concentrated animal feeding operation (CAFO) lagoon system in west-central Oklahoma. Changes in nutrients, microbial populations, and physical parameters were examined at three depths (0, 1.5, and 3.0 m) every 3 h over a 36-h period. The south lagoon (SL) was anaerobic (dissolved oxygen [DO] = 0.09 ± 0.12 mg/L) while the north lagoon (NL) was facultative (DO ranged from 4.0–0.1 mg/L over 36-h period). Negative sulfide–sulfate (-0.85) and bacteriochlorophyll a (bchl a)–sulfate (-0.83) correlations, as well as positive bchl a–sulfide (0.87) and light intensity (I)–bchl a (0.89) correlations revealed that the SL was dominated by sulfur conversions driven by the photosynthetic purple sulfur bacteria (PSB). The correlation data was supported by diurnal trends for sulfate, sulfide, and bchl a. Both nitrogen and sulfur conversions played a role in the NL; however, nitrogen conversions appeared to dominate this system because of the activity of cyanobacteria. This was shown by positive chlorophyll a (chl a)–I (0.91) and chl a–nitrate (0.98) correlations and the negative correlation between ammonium and nitrite (-0.88). Correlation data was further supported by diurnal trends observed for chl a, DO, and ammonium. For both lagoons, the dominant photosynthetic microbial species determined which nutrient conversion processes were most important.
Abbreviations: bchl a, bacteriochlorophyll a • CAFO, concentrated animal feeding operation • chl a, chlorophyll a • DO, dissolved oxygen • I, light intensity • PSB, purple sulfur bacteria • SRB, sulfate-reducing bacteria
|
INTRODUCTION
|
|---|
A MAJOR CONCERN of CAFOs is disposing animal waste in a way that minimizes environmental impact. More than 75% of swine (Sus scrofa) production in North America uses anaerobic or liquid–slurry systems for waste holding and disposal (Harper and Sharpe, 1997). Typically, these systems are lined, earthen basins that treat raw wastewater and store stabilized solids and liquids until the waste can be land-applied. These systems can be operated either as anaerobic, facultative, or aerobic lagoons under quasi-steady state treatment conditions. Generally, temperature, precipitation, and organic loading rates affect the treatment efficiency of these lagoons, but they are adaptable to excessive inputs (mass loadings) and can operate to buffer biological processes against souring (Grady et al., 1999).
Anaerobic lagoon systems operate in the presence of little to no DO and are designed to be relatively deep (2 to 6 m) for process efficiency. These lagoons are used for both retention and biodegradation of animal wastes. Anaerobic conditions are easily maintained because the rate of biodegradation of organic matter is much greater than the oxygen transfer rate. This type of system requires limited land area, simple operation and maintenance, and low capital, operation and maintenance costs (Grady et al., 1999).
In facultative lagoon systems, organic matter is stabilized by both anaerobic and aerobic process. Anaerobic conditions are maintained in the deeper portions of the lagoon, where organic matter is degraded to methane and carbon dioxide. In the upper portion, oxygen is provided by algal growth and/or surface aeration to produce an aerobic environment (Grady et al., 1999). In order to maintain the aerobic upper layer, the lagoons require large land areas and shallow depths (1 to 2 m). Shallow construction allows for the maximum penetration of sunlight and a balance between animal waste loading and oxygen production. Diurnal variations are important in the functioning of facultative systems. During the day, the extent of the upper aerobic zone is increased due to increases in photosynthetic bacterial and algal activity. At night, a decrease in algal activity occurs, making it possible for the lagoon to become completely anaerobic.
Aerobic systems operate in the presence of high DO concentrations, but at the same time inhibit algal production. Sufficient mixing or large land areas are required to maintain these conditions. Aerobic bacteria oxidize the soluble organic matter into new biomass. This type of aerobic digestion tends to be more complete than anaerobic digestion and, in most cases, maintains an odor-free environment and produces a high-quality effluent. A major drawback of this type of system is high operation and maintenance costs (Grady et al., 1999).
A less common treatment process in swine waste management involves the use of multiple-stage lagoon systems. This type of operation employs at least two lagoons or cells. The first cell receives the animal waste and relies on microorganisms for the degradation of organic matter. Through this process, solids are deposited and stored. The liquid effluent from this cell is transferred by gravity to the second cell. In the second cell, effluent is stored, and the top portion is used for irrigation of cropland (Hamilton, 1997).
The efficiency of all lagoon systems is directly related to concentrations and activity of nutrients and microorganisms present. Nutrient concentrations can vary depending on the type of livestock, temperature changes, I, rainfall, and mixing due to wind fluctuations. Swine manure typically consists of 6 kg/Mg total nitrogen, 3.5 kg/Mg ammonium nitrogen, 4.5 kg/Mg phosphorus, and 4.5 kg/Mg potassium (Zublena et al., 1993). Both daily and seasonal variations in temperature influence photosynthesis, microbial growth, and the biodegradation of organic carbon in the system (Kayambo et al., 2000). Diurnal or seasonal changes in I influence the activity of microorganisms, resulting in changes in oxygen production. The intensity and duration of light penetrating the water surface act as a forcing functions to influence the type of photosynthetic bacteria present. Typical forcing function parameters include temperature, I, pH, waste loads, and flow (Kayambo et al., 2000).
At the molecular level, it is believed that photosynthetic bacteria, in the presence of light, are the driving force behind photosynthesis and nutrient conversions (van Gemerden et al., 1985). As a driving force, photosynthetic organisms play a key role in both natural systems (i.e., wetlands and lakes) and engineered systems (i.e., waste lagoons and stabilization ponds). In natural systems, such as shallow, anaerobic lakes, anoxygenic photosynthetic bacteria are present and exhibit diurnal variations. Engineered systems are constructed to mimic natural ecosystems. Examples of engineered systems include waste stabilization ponds, wastewater lagoons, and constructed wetlands. These systems, like natural systems, utilize solar energy to transform and convert nutrients.
In waste lagoons, photosynthetic bacteria such as PSB and cyanobacteria act as the driving force for nutrient conversions. Purple sulfur bacteria are anoxygenic phototrophs and as a result will grow only under anaerobic or low oxygen tension environments in the presence of hydrogen sulfide (electron donor) and carbon dioxide (carbon source) (White, 2000). Under these conditions, photosynthetic bacterial growth is light-limited at deeper layers and sulfide-limited at the upper layers (Guerrero et al., 1985; van Gemerden et al., 1985). Purple sulfur bacteria are characterized by the photopigment bchl a and typically use a wavelength of 760 nm for growth (Pringault, 1999). A visual indication of their presence is seen in the pink to rose-red color of some lagoons. Cyanobacteria are oxygenic phototrophs found mostly in aerobic environments and are limited by I. These bacteria are the only photosynthetic prokaryotes that generate oxygen during photosynthesis (Perry and Staley, 1997). Cyanobacteria are characterized by the photopigment chl a and use a wavelength of 680 nm for growth (Pringault, 1999). Determining the activity of these photosynthetic bacteria and their influence on nutrient conversions will aid in understanding the performance of waste lagoons.
This paper reports the results of a diurnal study conducted to determine which nutrient conversions dominated each cell of a two-stage swine waste lagoon system. An examination of the role of photosynthetic bacteria as the driving force in nutrient conversions in both the anaerobic and facultative lagoon was completed.
|
MATERIALS AND METHODS
|
|---|
Site Description
The diurnal study was performed at a swine CAFO in west-central Oklahoma during July 1999. The CAFO has been in operation since 1986 and includes three swine barns with 150 sows per barn. The animal waste from all barns is collected and treated by a continuous-feed, two-stage, clay-lined lagoon system adjacent to the barns (Fig. 1)
. The SL receives influent directly from the barns and is 32 x 87 x 3 m (L x W x D) with a volume of 4408 m3. The wastewater from SL then flows into the NL. The NL is 29 x 83 x 3 m with a volume of 3743 m3, and effluent from it is periodically removed for land application. The system is designed to have a hydraulic retention time of 94 d; however, based on observed flow rates during this study, a much greater hydraulic retention time actually exists.
Diurnal changes in nutrients, microbial populations, and in situ parameters (i.e., DO, conductivity, temperature, pH, and salinity) were examined in both lagoons at three depths (0.5, 1.5, and 3.0 m) over a period of 36 h. Grab samples were obtained at the center of each lagoon at 3-h increments for both field and lab analyses. Field analyses were conducted immediately. Samples for laboratory analyses were preserved as necessary and stored on ice until laboratory analysis.
Field Methods
Physical measurements were taken in situ and included DO, conductivity, temperature, and salinity. Samples for pH were brought to the surface and measured on shore. Grab samples were analyzed using Hach methods for various water quality parameters including sulfate (8051), sulfide (8131), sulfite (8216), nitrate (8171), nitrite (8507), ammonium (8155), phosphate (TRP) (8048), and alkalinity (8203) (Hach Company, 1997). Light intensity was also measured in the field every 3 h using a SPER Scientific Broad Range Lux/FC meter (Technika, Phoenix, AZ).
Laboratory Methods
Photosynthetic pigment, dissolved organic carbon (DOC), and nitrate, phosphate, and sulfate analyses were performed in the laboratory. Samples for photosynthetic pigment analyses were collected in amber bottles and protected from light exposure. The DOC samples were acidified in the field with 0.1 M H2SO4 (pH < 2). All samples were stored on ice at 4°C until they were returned to the laboratory.
Photosynthetic pigments chl a and bchl a were analyzed using Standard Method 10200 (American Public Health Association, 1992). Samples were concentrated by centrifugation, and the pigments were extracted with 30 mL of a 7:2 (v/v) acetone to methanol solution. The samples were then centrifuged again and the supernatant was analyzed on a Beckman DU65 Scanning Spectrophotometer (Beckman Coulter, Fullerton, CA) at a wavelength range of 350 to 900 nm. Samples were reread after acidification with 0.1 M HCl. Bacteriochlorophyll a was calculated using an extinction coefficient of 76 mM-1 x cm-1 (Evans et al., 1990; Porra et al., 1989).
Dissolved organic carbon samples were diluted and filtered using a 0.45-µm filter. They were analyzed using a total organic carbon analyzer (Model 524; O.I. Corporation, College Station, TX) with an injection volume of 20 µL at all depths every 3 h using Standard Method 5310 (American Public Health Association, 1992).
Nitrate, phosphate, and sulfate concentrations were confirmed in the laboratory using a Dionex (Sunnyvale, CA) ion chromatograph. Sample preparation and analysis followed USEPA Method 300 (USEPA, 1984). The Dionex ion chromatograph was equipped with an IonPac AS9-SC column (Dionex, Sunnyvale, CA) and anion suppressor using 1.7 mM NaHCO3–1.8 mM Na2CO3 eluent (Alltech Associates, Deerfield, IL) at a flow rate of 1.0 mL/min.
|
RESULTS AND DISCUSSION
|
|---|
In this study, the lagoon systems are viewed as engineered systems that tend toward quasi-steady state. Each lagoon has its own unique properties and forcing functions that govern its treatment efficiency.
South Lagoon
The SL is anaerobic throughout the water column, as indicated by DO values that did not vary with time or depth (mean = 0.09 ± 0.12 mg/L), and is dominated by sulfur conversions at all depths. In addition, in situ measurements such as temperature, pH, salinity, and conductivity did not vary with depth or time (Table 1). Sulfur conversions were shown to be dominant by strong correlations (>0.80) for sulfate, sulfide, bchl a, and I (Table 2). Because of the turbid nature of this lagoon, light does not penetrate past approximately 10 cm from the surface, thus limiting the activity of photosynthetic bacteria to the top layer of water in this lagoon. However, because anoxygenic photosynthetic PSB act as the driving force in this lagoon with I as the forcing function, the effects of these bacteria reach far below their zone of activity.
At the surface, microscopic examination of surface water and a major absorption peak at 760 nm indicated the presence of PSB. The major function of these PSB is to capture light energy through photophosphorylation and to use this energy to oxidize the sulfur compounds, as described by the following equation (Perry and Staley, 1997):
 | [1] |
The oxidation of sulfide (H2S) to sulfate (SO2-4) as driven by the activity of PSB was shown by positive correlations between bchl a and sulfite (0.83), bchl a and sulfide (0.87), I and sulfide (0.86), and I and bchl a (0.89), as well as by negative correlations between bchl a and sulfate (-0.83) and sulfide and sulfate (-0.85) (Table 2). During daylight hours, the bchl a pigments in PSB reached a maximum of approximately 400 mg/L and corresponded with the sulfide minimum of 1.4 mg/L (Fig. 2a) . At night, sulfide concentrations increased due to the inactivity of the PSB, as indicated by the decrease in bchl a. Sulfate concentrations did not vary throughout the day (Fig. 2a).
At 1.5 m, light penetration was limited, but PSB activity was still occurring and acting as the driving force for nutrient conversions. Purple sulfur bacteria were oxidizing sulfide to sulfate as indicated by positive correlations between bchl a and sulfite (0.90) and bchl a and sulfide (0.88). Sulfate-reducing bacteria (SRB) were also active at this depth with sulfate reduction represented by negative correlations between sulfide and sulfate (-0.86) and sulfide and sulfite (-0.83). Sulfate-reducing bacteria are responsible for the conversion of sulfate (SO2-4) and/or sulfur compounds to sulfide (S2-) (Pescod, 1996):
 | [2] |
The influence of PSB on this process was observed by the diurnal trends for sulfide and sulfate (Fig. 2b). During daylight hours, PSB were active and oxidizing sulfur compounds to produce sulfate. Sulfate was then used by the SRB present at this depth as a terminal electron acceptor to form sulfide. At night, PSB activity decreased and sulfide concentrations increased (Fig. 2b). This increase in sulfide caused a thermodynamic backpressure that made it less favorable for bacteria to carry out sulfate reduction. As a result, sulfate concentrations also began to increase at night due to decreased SRB activity. This was shown by a maximum sulfide concentration of 2.5 mg/L at 0600 hours followed closely by a maximum sulfate concentration of approximatley 1000 mg/L at 0900 hours.
As depth increased to 3.0 m, light no longer penetrated, and PSB were not present but still influenced nutrient conversions. Sulfate reduction was the dominant nutrient conversion process at this depth. This was indicated by an inverse diurnal trend between sulfate and sulfide and by strong negative correlations between sulfide and sulfate (-0.86) and sulfide and sulfite (-0.92) (Table 2 and Fig. 2c). The effect of PSB at this depth was seen in the accumulation of sulfide at night, which resulted in a maximum concentration of 4.3 mg/L at 0900 hours. Because PSB were not removing sulfide from the system through oxidation at night and SRB were still actively reducing sulfate, an accumulation of sulfide was possible.
Purple sulfur bacteria were the driving force for all nutrient conversions throughout this system while light acted as the forcing function. The diurnal trend and correlation data showed a strong connection between the proliferation of the photosynthetic bacteria and sulfur conversions throughout the vertical water column profile. Neither nitrogen nor carbon conversions showed any diurnal trends or correlations with the activity of the anoxygenic photosynthetic bacteria.
North Lagoon
The NL can be described as a facultative system due to its aerobic characteristics at the surface and anaerobic conditions in the deeper layers, as determined by in situ DO analysis. Dissolved oxygen concentrations showed variations with both depth and time. At the surface, DO ranged from approximately 4 to 0.1 mg/L with maximum concentrations measured in the late afternoon (1500–2100 hours) and minimum concentrations measured in the early morning hours (0000–0300 hours) (Table 1). These fluctuations indicate the presence of an active population of photosynthetic organisms, identified as cyanobacteria by pigment analysis. Cyanobacteria were determined to be the dominant photosynthetic bacteria in this system.
Algae were not observed visually, indicated by a lack of algal mats, or microscopically. Subsequent analysis with the Hill reaction for chloroplasts supported this finding. The rate of oxygen production is a function of the activity of the cyanobacteria, light, and temperature. Other in situ parameters measured (pH, salinity, and conductivity) did not vary with depth or time, while temperature showed a variation with depth only (Table 1). Limiting nutrients, such as phosphorus and nitrogen, are often the factors that limit the activity of algae and cyanobacteria in freshwater ecosystems and, as such, affect the rate of oxygen production. However, these nutrients are not limiting in these engineered systems. At 1.5 and 3.0 m, DO was <0.5 mg/L, indicating anaerobic conditions (Table 1). These conditions allowed for the presence of denitrifying bacteria and SRB.
Nitrogen Conversions
Nitrogen conversions were determined to be the dominant processes in this system and were driven by the activity of the oxygenic photosynthetic cyanobacteria. At the surface, nitrogen-fixing cyanobacteria were present, while at 3.0 m denitrifiers were active. At 1.5 m, these two populations both play an active role in nitrogen conversions.
Microscopic examination of surface water and a major absorption peak at 680 nm support the hypothesis that cyanobacteria were the dominant microbial species at the surface. The presence of cyanobacteria is further indicated by the positive correlation between chl a and I (0.91) and the diurnal trend of chl a and DO where chl a reached a maximum concentration of approximatley 400 mg/L at 2100 hours (Table 3 and Fig. 3a)
. The rate of oxygen production follows the growth pattern of the cyanobacteria and results in greater concentrations during daylight hours (Kayambo et al., 2000). The oxygen produced by cyanobacteria is available to carry out nitrification, as can be seen in the positive correlations between chl a and nitrate (0.98) and the negative correlations between ammonium and nitrite (-0.88) (Table 3). Nitrification is the aerobic oxidation of ammonium (NH+4) to nitrite (NO-2) and nitrate (NO2-3) mediated by nitrifying bacteria and is shown in the following equation (Perry and Staley, 1997):
 | [3] |
Correlations show that as cyanobacteria activity (i.e., oxygen production) increases there is also an increase in nitrate concentrations due to increased nitrification.
At 1.5 m, the presence of denitrifying bacteria and cyanobacteria was indicated by positive correlations between chl a and I (0.86) and chl a and nitrate (0.99) and by a negative correlation between ammonium and nitrite (-0.84) (Table 3). The chl a and I correlation demonstrated a relationship between photosynthetic activity by cyanobacteria and I. Chlorophyll a concentrations were lower than that seen at the surface, but were still active in oxygenic photosynthesis, as seen by the strong correlation between chl a and nitrate and the diurnal trend of chl a (Table 3 and Fig. 3b). When decreased DO levels favored anaerobic conditions, denitrification occurred. Denitrification is the anaerobic conversion of nitrate (NO2-3) to nitrogen gas (N2) (Perry and Staley, 1997):
 | [4] |
This nitrogen gas can then be used by the cyanobacteria at the surface for nitrogen fixation during daylight hours. In this mixed population of denitrifying bacteria and cyanobacteria, denitrifiers are reducing nitrate and cyanobacteria are producing oxygen.
With increasing depth, the lagoon becomes anaerobic and at 3.0 m photosynthesis is limited and anaerobic conversion processes, such as denitrification, dominate. The presence of the denitrifiers was indicated by the positive correlation between nitrate and chl a (0.99) and the negative correlation between ammonium and nitrite (-0.97) (Table 3). The strong positive correlation between chl a and nitrate indicates that a decrease in chl a corresponded with a decrease in nitrate.
Sulfur Conversions
Even though nitrogen conversions are the dominant processes in this lagoon, sulfur conversions are an important component of the system. At the surface, the production of oxygen by cyanobacteria fuels the oxidation of sulfide to sulfate (Eq. [1]), similar to the activity of the PSB in the SL. At 1.5 and 3.0 m, negative correlations between sulfate and sulfide (-0.80 and -0.84, respectively) support the activity of SRB in sulfate reduction (Eq. [2] and Table 3). The presence of SRB can be attributed to the carryover of the waste stream from the SL, where SRB are a major factor. At 3.0 m, sulfate exhibits a diurnal trend and a maximum concentration is reached at 0600 hours, corresponding to a subdued chl a diurnal trend (Fig. 3c). The accumulation of sulfide in the upper layers resulted in a maximum sulfate concentration at 3.0 m in the early morning. This accumulation occurred when the cyanobacteria were not actively producing oxygen for sulfide oxidation, thus preventing any further sulfate reduction through a thermodynamic back-pressure similar to that seen at 1.5 m in the SL.
In this facultative lagoon, the cyanobacteria were the driving force in both the nitrogen and sulfur conversions with I acting as the forcing function. Strong correlation data between chl a and the nitrogen and sulfur species and the diurnal trends support the influence of the oxygenic photosynthetic cyanobacteria.
|
CONCLUSION
|
|---|
Both of the lagoons studied were engineered systems that tended toward quasi-steady state. The south lagoon was an anaerobic system whereas the north lagoon was a facultative system. In both of these lagoons, light was the forcing function for nutrient conversions while photosynthetic bacteria were the driving forces. The dominant photosynthetic microbial species determined which nutrient conversion processes were most important in these lagoons. Because PSB were the major photosynthetic microbial species in the south lagoon, sulfur conversion processes dominated this lagoon. Nitrogen conversion processes were the major contributors to nutrient conversions in the north lagoon, as dictated by the dominance of cyanobacteria.
|
ACKNOWLEDGMENTS
|
|---|
The authors wish to thank the Alig brothers (Alig Brothers Farm, Okarche, OK) for many valuable discussions and the use of their lagoon system for this study. This work was supported in part by the State of Oklahoma Conservation Commission (Oklahoma City, OK) and the United States Environmental Protection Agency (Dallas, TX) through Grant no. 1995 319 (H) TASK 68 and the National Science Foundation through Grant no. EEC-9619886; both were awarded to the University of Oklahoma. This work has not been subjected to any of the above Agencies' peer and administrative review process and therefore may not necessarily reflect the views of these Agencies, and no official endorsement should be inferred.
|
REFERENCES
|
|---|
- American Public Health Association. 1992. Standard methods for the examination of water and wastewater. 18th ed. APHA, American Water Works Association, and Water Environment Federation, Washington, DC.
- Evans, W.R., D.E. Fleischman, H.E. Calvert, P.V. Pyati, G.M. Alter, and N.S. Subba Rao. 1990. Bacteriochlorophyll and photosynthetic reaction centers in Rhizobium strain BTAi 1. Appl. Environ. Microbiol. 56:3445–3449.[Abstract/Free Full Text]
- Grady, L.C.P., Jr., G.T. Daigger, and H.C. Lim. 1999. Biological wastewater treatment. 2nd ed. Marcel Dekker, New York.
- Guerrero, E.M., C. Pedros-Alio, I. Esteve, J. Mas, H. van Gemerden, P.A.G. Hofman, and J.F. Bakker. 1985. Phototrophic sulfur bacteria in two Spanish lakes: Vertical distribution and limiting factors. Limnol. Oceanogr. 30:919–931.
- Hach Company. 1997. Water analysis handbook. Hach Company, Loveland, CO.
- Hamilton, D.W. 1997. Lagoons for livestock waste treatment. F-1736. Oklahoma Coop. Ext. Service, Stillwater.
- Harper, L.A., and R.R. Sharpe. 1997. Lagoon nutrient cycling and atmospheric nitrogen losses. USDA-ARS, Watkinsville, GA.
- Kayambo, S., T.S.A. Mbwette, A.W. Mayo, J.H.Y. Katima, and S.E. Jorgensen. 2000. Modelling diurnal variation of dissolved oxygen in waste stabilization ponds. Ecol. Modell. 127:21–31.
- Perry, J.J., and J.T. Staley. 1997. Microbiology: Dynamics and diversity. Saunders College Publ., New York.
- Pescod, M.B. 1996. The role and limitations of anaerobic pond systems. Water Sci. Technol. 33:11–21.
- Porra, R.J., W.A. Thompson, and P.E. Kriedemann. 1989. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: Verification of the concentration of chlorophyll standards by atomic adsorption spectroscopy. Biochem. Biophys. Acta 975: 384–394.
- Pringault, O., R. de Wit, and M. Kuhl. 1999. A microsensor study of the interaction between purple sulfur and green sulfur bacteria in experimental benthic gradients. Microbial Ecol. 37:173–184.[ISI][Medline]
- USEPA. 1984. The determination of inorganic anions in water by ion chromatography. EPA/600/4-84-017. USEPA, Washington, DC.
- Van Gemerden, H., E. Montesinos, J. Mas, and R. Guerrero. 1985. Diel cycle of metabolism of phototrophic purple sulfur bacteria in Lake Ciso (Spain). Limnol. Oceanogr. 30:932–943.
- White, D. 2000. Physiology and biochemistry of prokaryotes. Oxford Univ. Press, New York.
- Zublena, J.P., J.C. Barker, J.W. Parker, and C.M. Stanislaw. 1993. Soil facts: Swine manure as a fertilizer source. North Carolina Coop. Ext. Serv., Statesville.
TOP
ABSTRACT
INTRODUCTION
), sulfate (
), and bacteriochlorophyll a (
) as a function of time at (a) 0 m, (b) 1.5 m, and (c) 3.0 m for the south lagoon. Actual sulfate concentrations are divided by 10 to fit on graph
) as a function of time at (a) 0 m, (b) 1.5 m, and (c) 3.0 m for the north lagoon