URL originale : https://books.openedition.org/irdeditions/35439
Bacterial community contribution to nitrogen fixation and nitrous oxides production in the Sontecomapan Lagoon
p. 87-104
Résumé
Nitrogen fixation and denitrification are processes poorly studied in Mexican coastal lagoons. In this study the N incorporation and loss rates of the bottom water and sediments were analyzed in six zones of Sontecomapan lagoon during “Nortes” and rainy seasons and their relation with the rivers outflows and the coastal marine waters entrance. The rate of N2 fixation was calculated through acetylene reduction and the denitrification through N2O production techniques. The N2 fixation was lower than the nitrogen loss as N2O production (denitrification). The greatest fixation rate was registered in the “Nortes” season; being favored by oxic conditions and high organic matter concentrations in the sediments. In the rainy season, the N2 fixation was lowered by 80 % compared to the “Nortes” season. Denitrification was favored by low salinities in November and was 23 % higher than in February, 2005. In the rainy season the nitrous oxide production was related to the high N-NO3- concentrations and decreased by 18 % when the salinity increased from 13 to 22 PSU.
Entrées d’index
Keywords : Coastal lagoon, denitrification rate, bottom water, N2 fixation rate, sediment
Texte intégral
Introduction
1The coastal waters are continuously enriched with anthropogenic inorganic nutrients, from polluting sources as wastewaters generated by peripheral human settlements or by farming activities. As they are shallow ecosystems it is assumed that the processes that occur it the water-sediment interface can control the biological processes that happen at the water column, thus influencing the system productivity (Capone, 1983; Day et al., 1989).
2Microbial metabolic processes play an essential role in the mineralization of the organic matter that is deposited into the sediments, thus enriching the interstitial water with soluble forms of nitrogen (NH4+, NO2-, NO3-), phosphorus (HPO42-), sulphur (SH-, SO42-, H2S) and iron (Fe2+, Fe3+); these produced ions are then transported towards supernatant waters by diffusion and by biological processes. The nitrogen (N) cycle is a key biogeochemical process in which transformations of multiple nitrogen compounds are mainly driven by bacterial activity. The cycle controls="true" the nitrogen nutrient availability for biological productivity in aquatic systems, as well as, atmospheric CO2 fixation and biogenic carbon dioxide export from the surface layer towards the atmosphere (Zehr & Ward, 2002).
3The N enrichment of the water column may be caused by rainfalls and supply due to the superficial and underground drainage as well as by biological fixation. The loss of N may be due to the discharges of lagoon waters towards the coastline under current effects and/or the reduction of nitrate to molecular nitrogen (N2), through denitrifying bacterial activity with the subsequent return of N to the atmosphere, and the permanent loss of organic and inorganic nitrogen compounds by deposition process (Wetzel, 1981; Andersen et al., 2004; Liu & Qiu, 2007). The microbial nitrogen fixation is the most important process that turns atmospheric nitrogen to fixed nitrogen, whereas bacterial denitrification is the most significant process of molecular nitrogen regeneration.
4The biological nitrogen fixation is confined to specialized groups of prokaryotes, which own the nitrogenase enzyme and can have heterotrophic or autotrophic metabolism. There is a wide variety of factors that can affect N2 fixation, no matter the type of ecosystem: oxygen, pH, temperature, light, salinity, inorganic nitrogen and organic substrates available, all of them can govern the nitrogenase activity in specific conditions (Viner, 1982; Hebst, 1998; Evans et al., 2000). Diverse methods have been used to quantify the N2 fixation rate, one of them is the stable isotopes technique (15N) however, the more widely used is acetylene reduction of (C2H2) to ethylene (C2H4) (Larkum et al., 1988; Herbert, 1999; Falcón et al., 2002, 2007). The C2H2 reduction rate, compared with the N2 incorporation rate to the cellular biomass, has a conversion factor of approximately 3 moles of C2H4 formed with respect to 1 mole of fixed N2 (Atlas & Bartha, 2002).
5In coastal environments, most of the recycled N is in the form of ammonium (NH4+). This NH4+ is formed by bacterial decomposition and deamination of organic matter, and it diffuses from the sediments towards the superficial layer of the water column where it can be assimilated by phytoplankton. In presence of oxygen, part of the regenerated NH4+ is oxidized to nitrate (NO3-), which can be used as terminal electron acceptor by the denitrifying bacteria (Pseudomonas, Thiobacillus, Thiosphaera) producing gaseous forms of N (N2O, N2) (Kemp et al., 1990).
6On the other hand, in the sediment, the vertical distribution and abundance of N species are governed by the redox state of the different substrates thus, in the sediment oxygenated superficial layer, environmental ammonification and nitrification processes will be more important than those of denitrification. In the sediments, temperature, NH4+ concentration, pH, dissolved CO2, salinity, macrofauna activity and macrophytes presence are also important for regulating N2 fixation, nitrification and denitrification processes.
7The denitrification is especially active in shallow waters that present anaerobic zones rich in organic matter (Thamdrup & Dalsgaard, 2002; Madigan et al., 2004). It is considered as one of the most important mechanisms in coastal waters biogeochemistry because it is energetically the most favorable form of anaerobic metabolism and also removes significant amounts of NO3- therefore, denitrification can influence primary productivity and seems to act as a “buffer” system, preventing the excessive NO3- increase in water bodies (Groffman, 1994). Generally, the zone of denitrification is typically located at few millimeters below the oxic superficial sediment layer, where there are limited oxygen concentrations (Ferrara & Bianchi 1990; Revsbech et al., 1980). Some of the current techniques for evaluating denitrification rates are based on the quantification of N2O formation in anaerobic incubations; this can be obtained by inhibiting the passage from N2O to N2 by non-competitive N2O-reductase enzyme inhibition using acetylene (C2H2) (Taylor, 1983; Seitzinger, 1988).
8The importance of N as a primary regulator for productivity has induced to the examination of the N-metabolism nature and importance in the coastal benthic communities and the establishment of these activities connection with the pelagic ecosystem (Herrera-Martinez et al., 2000).
9The denitrification rate is controlled by the nitrification one, which supplies NO3- as a substrate. Thus, the connection process between nitrification and denitrification represents a way to turn nitrogen outside of the recycling routes due to the loss of N in gaseous form towards the atmosphere. This connection is quantitatively important for N cycle in the coastal continental and estuarine sediments, where the N lost by denitrification could represent around half of the entries for continental contributions (Seitzinger, 1988).
10In addition to the nitrification process, there are two other main sources for NO3-: diffusion towards the sediments from the water column, and its transport through underground waters (Capone & Bautista, 1985; Seitzinger, 1988; Day et al., 1989).
11The study of the N biogeochemical cycle in coastal lagoons is fundamental to elucidate the role of these ecosystems within the global carbon cycle and the global climate change, since it has a relevant role in the water column productivity and eutrophication. In the same way, the biological N2 fixation helps to recover the N lost by denitrification in the coastal ecosystems and providing new nitrogen.
12Currently in Mexico, there are few scientific reports on N2 fixation and denitrification processes in aquatic ecosystems. Although both processes are major components for nitrogen cycling in coastal lagoons, only some of these studies consider nitrogen fixation and denitrification processes together (Valenzuela-Siu et al., 2007; Hakspiel-Segura, 2014).
13Because of the importance of N species within Mexican lagoon ecosystems, the aim of this investigation was to analyze the incorporation and loss processes of N species from the bottom water as well as from superficial sediments, in order to contribute to a better understanding of the nitrogen cycle functioning in Sontecomapan Lagoon.
Materials and Methods
Study Site and sampling
14Six sampling sites were selected according to the salt and fresh water interchanges from the coastline and the rivers flowing into the lagoon: Arroyo La Boya (near the pass of the lagoon to the sea). La Palma and Sábalo (both near the wouhs of small rivers). El Cocal and Punta Levisa (on the navigation canal) and Costa Norte in the interior of the lagoon and a zone of submerged vegetation (Ruppia maritima) (Figure 1). Samplings were performed at three dates (November, 2004, and February and June, 2005) corresponding to two seasons of the year: “Nortes” winds (November and February) and rains (June).
15The bottom water samples were obtained with a horizontal one-liter Van Dorn bottle. The oxygen concentration was determined by the Winkler technique (Aminot & Chaussepied, 1983). The salinity was measured with an ATAGOS MILL-E refractometer (± 1‰) and its pH with an Orion potentiometer. The water samples for the determination of nitrogen inorganic species (N-NH4+, N-NO2- and N-NO3-) were filtered through 45 mm diameter Whatman GF/F membranes and deep frozen immediately until their processing, following the colorimetric methods recommended by Aminot & Chaussepied (1983).
16The sediment samples were collected by diving, using 22 x 5cm inner diameter (i. d.) polycarbonate corers, avoiding disturbance of the sediment column. The pH and Eh were measured using ORION (2mm and 3mm i. d. respectively) needle-type mini-electrodes, in order to avoid disturbing the sediment during penetration they were inserted in a stepped way each 5 mm of depth. The interstitial water for measuring the nutrients was obtained from the first centimeter of sediment, using a polycarbonate capillary tube (10 cm length and 5 mm i.d.) sealed in its lower bound and pierced with a series of 1 mm i.d. holes throughout their last centimeter. The interstitial water from the first centimeter of depth was obtained by suction using a 50 mL syringe connected to the capillary tube by a latex hose. The water samples were filtered with a 25 mm diameter Whatman GF/F membrane and stored in 60 ml hermetic bottles previously gasified with N2 to prevent oxidation from the samples’ air, and then deep frozen to -18 °C until their processing.
17The remaining sediment from the cores was used for determining the percentage of organic matter (% OM) and sediment texture. Replicated cores were sliced into 1 cm thick layers and treated separately for % OM, using the potassium dichromate excess titration method, with a 0.5N solution of ferrous sulphate for organic matter oxidation (Gaudette et al., 1974) and the sediment texture by Bouyoucos’ hydrometer method (Holme & McIntyre, 1984).
Incubations for N2 fixation and denitrification rates
18The bottom water samples were obtained with a horizontal Van Dorn bottle and 300 mL from the sample were incubated in 500 mL hermetic glass jars. The first centimeter of the sediment was placed in another series of jars containing 300 mL of bottom water previously filtered through Whatman GF/F membranes. The incubations were performed in situ (two clear bottles and one dark) for four hours, one series by test. At the beginning of the incubations, 10 % of the air volume from each jar was extracted through a cork with turnover septum stoppers —folding rubber apron— (Fisher Scientific) placed in jar cover (Moran-Villa et al., 2009), and the same volume of acetylene was injected into the jar (C2H2). The jars stayed within a water bath to keep them at room temperature.
N2 fixation measurements
19After the four-hour incubation period, a sub-sample from the gaseous phase was taken and stored in a hermetically closed vial. The N2 fixation rate was estimated by acetylene reduction technique (ARA) (Capone, 1993; Morán-Villa et al., 2009). The ethylene analyses (C2H4) were performed with a Perkin Elmer Auto Analyzer gas chromatograph with a flame ionization detector (FID) equipped with a 15 x 0.55 mm i.d. and 1 mm thick RESTEK Corporation capillary column. The temperature of the oven, injector and detector was 165 °C and 230 °C respectively. As a gas carrier, a 1 mL min-1 He flow was used. A 100 µl aliquot from C2H2/C2H4 gas sample was injected. The gas chromatograph was calibrated with a standard 100 ppm C2H4, and the reduction rate of C2H2 was converted to N-fixed using the conventional molar conversion factor 3: 1 proposed by Postgate (1982) and Seitzinger & Garber (1987), and the Bunsen coefficient of solubility (Flett et al., 1976). The total fixation of N2 rate was calculated by adding the phototrophic fixation rate (in the light) to the heterotrophic one (in darkness).
N2O measurements
20The analysis of N2O present in the gaseous phase was made with a VARIAN chromatograph with a flame ionization electron capture detector 63Ni. As a gas carrier, a 30 mL min-1 He flow was used. The temperatures of the column and the detector were 50 °C and 300 °C respectively. A 1 ml aliquot was injected and the peak area was measured with a peak integrator. A standard of 100 ppm N2O (Alltech) and the Bunsen coefficient of solubility (Flett et al., 1976) were used.
21where:
22C.S. = Coefficient of N2O standard
23Vgas = Volume of the gas phase in the incubation bottle
24VH20 = Volume of incubated water (or sediment, as the case might be)
250.1 = Bunsen coefficient for nitrous oxide at the appropriate salinity and temperature
26Δt = Incubation time
27The volume of the gas phase injected into the gas chromatograph was 100 µl
Statistical analysis
28In order to determine the physical and chemical factors that influence the N2 fixation (FixN) and denitrification (N2O) rates during the “Nortes” and the rainy seasons, a Canonic Correspondence Analysis (CCA) using Multi-Variate Statistical Package (MVSP) 3.22 ® program was performed on the loge standardized data, using the centered data options and the Kaiser rule for the axes extraction (Kovach, 1999).
Results
Physical and chemical parameters
Bottom water
29Table 1 shows the mean values of oxygen, temperature, pH and salinity at the bottom water of the six stations. The bottom water was found in suboxic conditions but with acceptable values for most of the pelagic organisms. Oxygen varied between 2.6 and 10.1 mg/l-1 in the zones with greater boat traffic. The pH was around neutrality all year long (7.23 ± 0.55). Temperatures varied between 20 and 30 °C. Salinity varied from 0.2 to 37 PSU (mean value = 19.6 ± 11.4 PSU), with the lowest values measured in November (from 0.2 to 28 PSU). The Eh values were highly variable but generally positive (Table 1).
30N-NH4+ concentration had mean values of 3.98 ± 3.21 µmol l-1, with the lowest values registered at La Boya and Costa Norte (0.01 and 0.39 µmol l-1 respectively) and the highest at Punta Levisa and La Palma (10.6 and 7.9 µmol l-1 respectively) during “Nortes” season (February). In general, the ammonium concentration was 6 times higher in February that in November (6. 08 ± 3.3 and 1.04 ± 0.65 µmol l-1 respectively). During the three surveys, the N-NO2- concentrations fluctuated between 0.15 and 9.0 µmol l-1 (La Boya and El Cocal, respectively); the low concentrations of this nutrient in the bottom water could be due to an intense ammonium oxidation to nitrate. The high concentration of N-NO2- found in El Cocal was due to the effect of the sediment re-suspension provoked by the constant boat transit in the navigation canal, and it is in this same sampling area where the smallest N-NO3- concentration was obtained (0.8 µmol l-1) in February. In June (rain season), high concentrations of N-NO3- in all the sampling areas (81±35.5 µmol l-1) were generally registered.
Sediments
31The sediments were of the silty-sandy type, moderately rich in organic matter (1.73 ± 1.5 %), with the highest values in the sampling sites near the two river mouths (Table 2). The Eh varied from -240.9 to 291 mV.
32The highest concentrations of ammonium were recorded during the “Nortes” period (November 2004, February 2005) at Punta Levisa (26.5 µmol l-1 N-NH4+), La Palma (22.6 µmol l-1 N-NH4+) and La Boya (25.2 µmol l-1 N-NH4+). Generally, ammonium concentrations in the sediment were higher than at the bottom water (Tables 1 and 2). Nevertheless, the diffusive flow of the sediment towards the water column sometimes allows leads to higher concentration in the bottom water than in the sediment (Tables 1 and 2).
33The highest concentrations of N-NO2- were registered in November at La Palma (22.6 µmol l-1), Punta Levisa (16.5 µmol l-1) and Costa Norte (13.9 µmol l-1) and were related to negative Eh, pH between 7.1 and 8.7 and high percentages of organic carbon (3.6, 2.1 and 1.2 % org C respectively). The highest concentrations of N-NO3- in sediment were registered in June 2005, at Costa Norte and Punta Levisa (121 and 129 µmol l-1 respectively). No significant difference in the concentrations of N-NO3- between the bottom water and the interstitial water of the sediments were found.
Nitrogen fixation
34In all the sampling stations, nitrogenase activity was detected. In the bottom water, the highest N2 fixation rates (309.98± 160.35 µmol C2H4 m2 h-1) were observed in November ( “Nortes” season). A drastic decrease (81 %) was observed in rainy season (58.72 ± 19.5 µmol C2H4 m2 h-1), when the highest salinity was noted at the bottom water (19.6 ± 12.8 PSU). In the sediments the fixation rate of N2 was 10 times lower (31.62 ± 28.4) than in the bottom water (Fig. 3), and the lowest values were recorded in February and June, 2005 in Punta Levisa (4.17 and 5.98 µmol C2H4 m2 h-1 respectively).
Denitrification rate
35Generally, it was observed, as well as for the N2 fixation, that the highest N2O production occurred in November (764 ± 114,3 µmol N2O m2 h-1), this being the reason why this process was favored by the low salinities (19,6 ± 11,06 PSU) and the highest oxygen concentrations registered (6.6±1.53 mg L-1) at this season. The lowest rates were observed in February (593.9 ± 107.4 µmol N2O m2 h-1), being 23 % lower than those from November. During the rainy season, the denitrification rate varied between 465.5 and 1094 µmol N2O h-1 m2. At this season the highest values were obtained at La Boya (Fig. 4).
CCA analysis
36The CCA analysis showed that in November the high N2 fixation rate recorded at the bottom water had an inverse relationship with the slightly electronegative Eh (r=-0.663), and a positive relationship with N-NO2- (r=0.92). Within the same period, the high N2 fixation rate in the sediments was also correlated to slightly electronegative Eh (r= - 0.680), but also to high sand concentrations (r= -0.667), low ammonium concentrations (r= 0.696) low nitrates (r= -0.782) and high O2 concentrations in bottom water (Fig. 5).
37In February, the low N2 fixation rate in bottom water was correlated positively with electropositive values of Eh (r=0.795), high O2 (r=0.636), and negatively with high N-NH4+ concentrations (r= -0.696), low N-NO2- (r= -0.659) and low OM percentage (r= - 0.77) in the sediment. Within the same period, the low N2 fixation rates in the sediment were positively linked to the greatest percentage of silt (r=-0.788), and negatively to the lowest percentage of sands (r= -0.958), slightly basic pHs (r= -0.955) and low N-NO3- concentrations (r= -0.602) in the interstitial water. In November, the high N2 fixation rate in the sediments (higher than in February) was correlated to slightly electronegative Eh (r=- 0.680), high sand concentrations (r=-0.667), low ammonium concentrations (r=0.696), low nitrates (r=-0.782) and high O2 concentrations in the bottom water (Fig. 5).
38As for the N2 fixation, the denitrification rate in the “Nortes” season, was correlated to slightly electronegative Eh values (r=-0.680), low N-NO3- concentrations in the interstitial water (r=0.782) and low salinities (r=0.98). The rainy season (June) was related to high N-NO3- concentrations in the interstitial water (Fig. 5 and 6).
Discussion
39Although it is considered that the N2 fixation is a O2-sensitive process, the highest rates were recorded during the “Nortes” season (November, 2004 and February, 2005), when the oxygen concentrations in the bottom water (7 ± 1.5 mg L-1) were the highest. This can be partly due to the development of diazotrophic microorganisms of conformational protection mechanisms against nitrogenase inactivation by high O2 concentrations, as reported by Soto-Urzúa & Baca (2001). A second reason should be linked to wind re-suspension of sediment particles driven by Nortes winds at this season. Indeed, re-suspended particles may constitute a microhabitat (within a few microns deep into the particle’s interior) with aerobic and anaerobic spaces favoring the bacterial processes of N2 fixation and denitrification (Ferrara-Guerrero et al., 2007). In the sediments the deposit of labile organic matter is also related to these hydrodynamic processes and bio-perturbation from benthic organisms, which will induce environmental changes in each sampling station (Brune et al., 2000).
40The oxygen sediment concentrations in the two seasons studied were high enough to allow recent organic matter mineralization and to provide enough ammonium to the sediment, which would explain the lower rates of N2 fixation compared to bottom water.
41The fact that the highest ammonium concentrations of the bottom water were registered in February, 2005 is due to strong winds and tidal effects that provoked sediment re-suspension thus allowing NH4+ diffusion towards the bottom water, as has been already demonstrated for this type of environment by Kemp et al. (1990). In such shallow ecosystems, the interchange of dissolved substances through the water-sediment interface is a process that affects the chemical composition of the water column since it regenerates the ammonium and nitrate required for the primary biomass production in the superficial layers (Maksymowska-Brossard & Piekarek-Jankowska, 2001). Generally, the relatively low concentrations of N-NH4+ in bottom water favored N2 fixation in both seasons.
42The high salinities registered at the bottom water in June inhibited the N2 fixation, so it was about 80 % lower than in November and February, this coincide with Herbst (1998), Serraj & Drevon (1998) who reported that salinity is a N2 fixation inhibitor (Figs. 2 and 5). Generally, planktonic nitrogen fixation is greater in freshwater than in marine ecosystems (Nielsen et al., 2003) however, it appears to be no difference in nitrogen fixation rate in the sediments in relation to different salinities from bottom water (Figs. 3 and 5).
43The denitrification rates measured in our study match with those reported for eutrophic estuarine ecosystems impacted by waste water inputs (Seitzinger, 1988). The relationship between the high denitrification rates and the high N-NO2- concentrations in reduced sediments was not too clear, as high denitrification rates were also recorded in reduced sediments with low N-NO2- concentration during the rainy season. According to Codispoti et al. (2001) nitrites tend to accumulate in the water column only when the oxygen concentrations are <2.5 µM, however, this trend is hardly observed in the sediments due to the interment activity of the benthic meiofauna provoking the formation of patches in the superficial sediments (Hendricks, 1993; Sheibley et al., 2003) and thus the formation of slightly oxidized microhabitats with low N-NO2- concentrations. This was observed in the “Nortes” season at El Cocal station where high denitrification rates, low NO2- concentrations and slightly oxidized sediments were observed.
44The denitrification rate was also affected by salinity and sediment organic matter in agreement with Richardson et al. (2004) and Rysgaard et al. (1999) who reported, in estuarine ecosystems, 50 % decrease of denitrification with an increase of salinity from 0 to 10 PSU. In our study we found a 18 % decrease of denitrification rate when the salinity changed from 13 to 32 PSU.
45The high N2O concentrations produced during the denitrification depend mainly on electronegative Eh values, nitrate concentration and sediments texture. Nevertheless, the denitrification process was extremely variable temporarily and spatially, because when the N-NO3- concentration increases, it is not fully used for denitrification process since a proportion can be reduced to NH4+ (Ullah & Zinati, 2006).
46On the other hand, given that the mineralization of the organic matter that has been recently deposited in the superficial sediments produces the greatest quantity of N-NH4+ and N-NO3- used for the denitrification; it can be expected that the sites with highest deposition of labile OM present a high N2O production.
Conclusions
47The exchange of ammonium and nitrate ions between the water-sediment interface and the bottom water is a key factor for nitrogen regeneration that strongly varies between the different seasons of the year ( “Nortes” and rains).
48The results suggest that increased salinity, from 24 to 29 PSU, may limit nitrogen fixation in bottom water.
49The greatest loss of nitrogen as N2O through denitrification happened in the reduced sediments with greatest silt percentage and high NO3- concentrations, located at the deepest zones of the navigation canal.
50The strong variations of N2 fixation and denitrification rates registered in the “Nortes” and rainy seasons can be linked to the runoff of terrestrial nitrogen within the lagoon, originating from the bordering zones that have been deforested for farming purposes.
51For future investigations on the global N cycle it will be necessary to extend the measurements of N2 fixation, denitrification and nitrification rates as well as their connection with the regeneration and loss of N, to other Mexican coastal lagoons that are still poorly studied.
Acknowledgements
52This study was supported by the 2002-39634-F/A-1CONACYT project and the Mobility ECOS-ANUIES-CONACYT Program (189448). The authors thank Dr. Flor María Cuervo and Dr. Felipe Martinez from the Universidad Autónoma Metropolitana, Unidad Iztapalapa for their support in the determination of nitrous oxides.
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Ecology of the Sontecomapan Lagoon, Veracruz
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