Microb Ecol (2003) 46:43–54 DOI: 10.1007/s00248-002-2041-9 2003 Springer-Verlag New York Inc.
Factors Controlling Extremely Productive Heterotrophic Bacterial Communities in Shallow Soda Pools A. Eiler,1 A.H. Farnleitner,2 T.C. Zechmeister,3 A. Herzig,4 C. Hurban,5 W. Wesner,5 R. Krachler,5 B. Velimirov,1 A.K.T. Kirschner1 1
Institute of Medical Biology, Vienna University, Waehringerstr. 10, A-1090 Vienna, Austria Institute of Chemical Engineering, Technical University, A-1060 Vienna, Austria 3 Institute of Bacteriology, Mycology, and Hygeine, University of Veterinary Medicine, A-1210 Vienna, Austria 4 Biological Research Institute Burgenland, A-7142 Illmitz, Austria 5 Institute of Inorganic Chemistry, Vienna University, A-1090 Vienna, Austria 2
Received: 20 June 2002; Accepted: 23 December 2002; Online publication: 13 May 2003
A
B S T R A C T
Dilute soda lakes are among the world’s most productive environments and are usually dominated by dense blooms of cyanobacteria. Up to now, there has been little information available on heterotrophic bacterial abundance, production, and their controlling factors in these ecosystems. In the present study the main environmental factors responsible for the control of the heterotrophic bacterial community in five shallow soda pools in Eastern Austria were investigated during an annual cycle. Extremely high cyanobacterial numbers and heterotrophic bacterial numbers up to 307 · 109 L)1 and 268 · 109 L)1 were found, respectively. Bacterial secondary production rates up to 738 lg C L)1 h)1 and specific growth rates up to 1.65 h)1 were recorded in summer and represent the highest reported values for natural aquatic ecosystems. The combination of dense phytoplankton blooms, high temperature, high turbidity, and nutrient concentration due to evaporation is supposed to enable the development of such extremely productive microbial populations. By principal component analysis containing the data set of all five investigated pools, two factors were extracted which explained 62.5% of the total variation of the systems. The first factor could be interpreted as a turbidity factor; the second was assigned to as concentration factor. From this it was deduced that bacterial and cyanobacterial abundance were mainly controlled by wind-induced sediment resuspension and turbidity stabilized by the high pH and salinity and less by evaporative concentration of salinity and dissolved organic carbon. Bacterial production was clustered with temperature in factor 3, showing that bacterial growth was mainly controlled by temperature. The concept of describing the turbid water columns of the shallow soda pools as ‘‘fluid sediment’’ is discussed.
Correspondence to: A.K.T. Kirschner; E-mail:
[email protected]
44
Introduction Dilute soda lakes represent the most alkaline naturally occurring aquatic ecosystems with pH values of up to 12 [13]. These ecosystems are characterized by the presence of large amounts of NaHCO3 and Na2CO3 and in many cases by low concentrations of Mg2+ and Ca2+ because of the insolubility of those cations as carbonate minerals under alkaline conditions. Conditions suitable for the formation of soda lakes are found in arid and semiarid climate zones [11, 40], where intense evaporative concentration rates exceed inflow rates such that salts accumulate [13]. Soda lakes are regarded as being among the worlds most productive environments, as the access to dissolved inorganic carbon in form of HCO3) and CO32) for primary producers is unlimited [6]. In most cases, alkaliphilic cyanobacteria are the dominating primary producers. Aerobic heterotrophic bacteria have been reported to reach extremely high numbers of 107 to 108 cells mL)1 [12, 16], and bacterial secondary production can be assumed to exceed values measured thus far for natural aquatic ecosystems. Seasonal variation in bacterioplankton biomass and production of alkaline aquatic ecosystems are poorly examined, as well as their controlling environmental factors. Plate count numbers of organotrophic bacteria were shown to remain more or less constant over the year in two deep African soda lakes, despite marked seasonal changes in salinity due to periods of heavy rain [14]. But to our knowledge, there is no information available on the seasonal changes of total bacterioplankton in shallow soda lakes. The soda pools investigated here are located in Eastern Austria, within the area of the national park Neusiedler See-Seewinkel (4745¢–49¢, 1647¢–53¢), above the largest mineral water deposit in Europe [24]. The mineral solutes ascending with the groundwater flux [24] formed these shallow soda pools (max. depth: 50 cm) with pH values ranging from 8.5 to 11. Na+ is the dominating cation, and HCO3), CO32), Cl), and SO42) represent the major anions. The salinity of the pools can vary strongly over the seasons, but also within years, ranging from 0.2% to >4.0% (w/v) before complete evaporation, as they are often exposed to periods of severe aridity, typical for the Pannonian climate in eastern Austria. Loss of salts can then occur by wind deflation. Chemophysical parameters such as salinity, alkalinity, and temperature may have a strong impact on the seasonal changes of bacterial activity in these pools. High solar radiation and regional winds re-
A. Eiler et al.
suspending a substantial portion of the sediment are considered additional important external factors. The aim of the study was to elucidate the special environmental features characterizing these environments and enabling the development of such abundant and productive bacterial populations in the five pools over a seasonal cycle. Therefore, a variety of ecological parameters were measured along with heterotrophic bacterial numbers and secondary production, and the main factors controlling the bacterial community in the pools were extracted by multivariate comparisons.
Materials and Methods Study Site and Sampling Samples were collected from five soda pools in biweekly intervals during summer and once every 6 weeks during the winter season from May 2000 to May 2001 (Fig. 1). According to the trophic classification system proposed by Forsberg and Ryding [9], the investigated soda pools are extremely hypertrophic ecosystems (Table 1). The Oberer Stinkersee (OS) is the pool with the highest total salt concentrations and a wind-independent permanent turbidity, whereas the Unterer Stinkersee (US) has a varying wind dependent turbidity and a varying concentration of humic substances leading to dark brown water color in periods of massive decay of plant material. The Illmitzer Zicksee (ZL) is characterized by a low turbidity caused by the fine sediment covered by an intense biofilm preventing resuspension of the sediment particles. The Lange Lacke (LL) and the Wo¨ rthenlacke (WL) exhibit a varying wind dependent turbidity. Despite their proximity they feature large differences in their chlorophyll a content and their amount of total suspended solids (Table 1).
Chemophysical Parameters Conductivity (WTW, LF 330), temperature, pH (Seibold Wien, GHM) and oxygen (Seibold Wien, SHO/2) were measured in situ three times along 20-m transects toward the center of the pools. Along the transects three 1-L water samples were collected and integrated for further analysis. Wind velocity was arbitrarily estimated according to the Beaufort wind scale (http://www.zetnet.co.uk/sigs/weather/Met_Codes/-beaufort.htm). For the determination of total suspended solids (TSS), a defined volume of sample water was filtered through premuffled glass-fiber filters (GF/C; Whatman; England) and dried to constant weight. To obtain the inorganic and organic fraction, the samples were further combusted in a muffle furnace. Total phosphorus was determined photometrically after dissolution of the unfiltered sample with potassium peroxydisulfate, using the molybdenium-blue method according to Strickland and Parsons [35]. After 1:10 dilution with distilled water, the ion concentra-
Bacterial Communities in Soda Pools
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Fig. 1. Location of the five investigated saltwater pools within the national park Neusiedler See—Seewinkel. Sampling sites are marked by arrows. Villages are black. tions in the samples were measured with ion chromatography. All columns and chemicals were supplied by Dionex (Sunnyvale, CA). For anions, AS-4A columns with AG-4A precolumns and for cations CS-12A columns with CG-12A precolumns were used. As displacing liquid for anions a sodium carbonate buffer (6 mM Na2CO3 + 12 mM NaHCO3) and for cations an 18 mM methanesulfonic acid solution was used. The ions were detected with a conductivity detector after removing the anions with the appropriate suppressors (AMMS-II) and for cations (CSRS-Ultra 4mm). Alkalinity (ALK; mmol L)1) was calculated by the following equation: þ
þ
2þ
2þ
ALK ¼ ½Na þ ½K þ 2½Mg þ 2½Ca ð½Cl þ 2 ¼ ½HCO 3 þ 2½CO3
The mean of the calculated pK values from each site (n = 10) was inserted in the following equations to calculate the carbonate and bicarbonate concentrations of the other sampling dates: pHþpK 1 ½CO2 Þ 3 ¼ ALK ð2 þ 10
ð3Þ
pKþpH 1 ½HCO Þ 3 ¼ ALK ð1 þ 2 10
ð4Þ
)1
Salinity (SAL; mg L ) was determined by the addition of the measured and calculated salt concentrations: SAL ¼½Naþ þ ½Kþ þ ½Mg2þ þ ½Ca2þ þ ½Cl þ ½SO2 4 2 þ ½HCO 3 þ ½CO3
ð5Þ
2½SO2 4 Þ ð1Þ
On two occasions the carbonate and bicarbonate concentrations were measured with HCl titration to calculate the dissociation constant (pK) of the [CO32)] () [HCO3)] equilibrium (2): 1 pK ¼ logð½Hþ ½CO2 3 ½HCO3 Þ
ð2Þ
Dissolved Organic Carbon and Chlorophyll a For the determination of dissolved organic carbon (DOC), subsamples of the integrated water samples were filtered through precombusted Whatman GF/C filters. DOC was determined using
Table 1. Basic characterization of the five investigated soda pools
2
Area (km ) Total phosphorus (mg L)1) Chlorophyll a (lg L)1) Salinity (g L)1) pH Tot. susp. solids (mg L)1) Sediment a
OS
US
0.49 2.1 (0.9–4.3) 62 (4–133) 7.4 (4.2–31.3) 9.78 (9.4–10.05) 1254 (321–2480) Fine sand
0.19 1.1 (0.2–3.9) 88 (0–402) 4.4 (2.8–16.8) 9.47 (9.01–10.19) 769 (15–2980) Fine sand
ZL 0.6 8 5.4 9.76 81
0.7 (0.2–2.4) (0–48) (2.7–17.8) (9.36–10.89) (22–467) Clay
LL 1.1 197 3.8 9.46 344
2.24 (0.3–3.5) (21–430) (2.4–8.4) (9.10–9.85) (76–969) Silt
WL 1.0 52 5.4 9.23 290
0.29 (0.2–2.6) (0–135) (2.4–8.3) (8.88–9.82) (38–125) Silt
Values represent annual average and range (in parentheses) of 16 measurements. OS, Oberer Stinker; US, Unterer Stinker; ZL, Zicklacke; LL, Lange Lacke; WL, Wo¨ rthen Lacke
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A. Eiler et al.
a Shimadzu TOC 5000 carbon analyzer (Shimadzu Corporation, Tokyo, Japan). Chlorophyll a was extracted with 90% ethanol (1 h at 80C) and was measured spectrophotometrically (Hitachi U-2000) [30].
Bacterial and Cyanobacterial numbers For the determination of bacterial and cyanobacterial numbers, 15-mL samples were preserved with formalin (4% v/v final concentration) for direct epifluorescene microscopy. Each sample consisted of three 5-mL subsamples collected along the 20-m transects. Cells were stained with DAPI (0.01% v/v final concentration) and filtered through black polycarbonate membrane filters (Millipore, Ireland) of 0.2 lm pore size [29]. Bacterial (UV excitation: 340–380 nm, barrier filter: 430 nm) and cyanobacterial numbers (red light excitation: 515–560 nm, barrier filter: 580 nm) were counted with a Leitz Diaplan microscope. Bacterial cell volumes (V; lm3) of at least 100 cells were determined for representative samples by eyepiece micrometer to calculate the average cellular carbon content (C; fg C cell)1) after Norland [27]. Cyanobacteria in representative samples were taxonomically classified after Komarek and Anagnostidis [23].
Bacterial Secondary Production To measure bacterioplanktonic secondary production in the five saltwater pools the [3H]leucine incorporation method, initially developed by Kirchman et al. [18] and Simon and Azam [34], was used and the protocol of Kirschner and Velimirov [20] was followed. A wide range of leucine concentrations ranging from 30 to 240 nM was tested twice at each sampling site. The resulting incorporation velocities were iteratively fitted to the hyperbola function of the Michaelis–Menten enzyme kinetics by using nonlinear regression analysis (Delta Graph 4.0, Delta Point Inc., USA). The plots were used for the calculation of the theoretical maximal uptake velocity (Vmax) and of the half-saturation constant (Km). The mean of all calculated Km values (n = 10) was used to calculate Vmax for all other sampling dates from the [3H] leucine uptake velocity (V) at a substrate concentration (S) of 60 nM [3H]leucine according to Equation (6) [8]. Vmax ¼ V ðKm þ SÞ S1
ð6Þ
3
[ H]Leucine incorporation rates (leuinc) were converted to carbon production (BSP) according to Simon and Azam [34] by using the following equations: BPP ¼ leuinc 2 ð100=7:3Þ 131:2
ð7Þ
where BPP = bacterial protein production; 2 = isotope dilution as recommended by the authors; 100/7.3 = 100/mol% of leucine in protein; 131.2 = molecular weight of leucine. BSP ¼ BPP 0:86 1:18
ð8Þ
where 0.86 and 1.18 represent the factors requested for converting bacterial protein production into BSP, taking into account that 86% of the weight of the aminoacids is the carbon moiety and that 18% of the amino acids are not detected by [34].
The specific growth rate (l; [h)1]) and the doubling time (g; [h]) were determined by the following equations (9, 10): l ¼ ½lnðBN0 þ BNbsp Þ lnðBN0 Þ 2
ð9Þ
where BN0 = bacterial numbers at time 0, corresponding to the bacterial numbers determined for this sampling point via the epifluorescence technique, and BNbsp-bacterial secondary production expressed in cells L)1 measured within the 0.5 h incubation interval. The doubling times were then calculated after: g ¼ lnð2Þ l1
ð10Þ
Microautoradiography Because of the high concentration of cyanobacteria, microautoradiography was used to determine whether cyanobacteria were capable of leucine uptake under conditions similar to the determination of BSP (180 nM 3H-leucine, 30 min, in situ temperature). On two occasions during summer, 1-mL samples from each sampling site were incubated with 30 lL [3H]leucine and stopped with 60 lL TCA (5% v/v final concentration). After staining with DAPI (0.01% v/v final concentration) the samples were diluted 10·–50· to obtain optimal cell densities for microscopic examination. The protocol by Fuhrman and Azam [10] was followed, which allows simultaneous visualization of developed silver grains and DAPI-stained bacteria, avoiding interference of the silver grains with viewing the bacteria. Bacteria and cyanobacteria were viewed by epifluorescence microscopy, and clusters of silver grains (‡5 grains) were viewed by phase contrast microscopy.
Statistical Analysis Data were analyzed according to Zar [39]. A nonparametric Tukey test was applied for two independent samples and a Kruskal– Wallis test for more than two independent samples to compare the five saltwater pools. Principal component analysis (PCA, varimax rotated with Kaiser normalization) was performed to evaluate the parameters responsible for the seasonal fluctuations of the investigated environmental factors in the saltwater pools. For multiple linear stepwise regression analyses and PCA analyses, data not meeting the requirements of homoscedaticity and normal distribution (Shapiro–Wilks test) were log10-transformed after adding 1 to the variable. Further nonparametric Spearman rank correlations were performed for the data of each pool. For calculation of annual averages, monthly means were used. All statistical analyses were performed using the software SPSS 10.0 for Windows.
Results Physical and Chemical Parameters The water temperature during the investigation period varied from 1.2C to 34.4C, following the typical pattern
Bacterial Communities in Soda Pools
47
the carbonate and bicarbonate anions comprised up to 60% of total salinity (data not shown) and was responsible for the observed high pH values up to 10.89 in the pools. The high alkalinity (Fig. 2B) was in turn responsible for the relatively low calcium and magnesium concentrations with mean values of 47 mg L)1 and 148 mg L)1, respectively. The peak of conductivity and alkalinity in spring 2000 at US was observed when the part of the US which was used as sampling site for the first four sampling dates desiccated and thereafter an adjacent sampling site was chosen.
DOC and Chlorophyll a DOC values and conductivity were highly significantly correlated (rs = 0.80, p < 0.001). The highest DOC value coincided with the highest conductivity value in ZL before complete evaporation (Fig. 2C). Chlorophyll a values ranged from 0 to 430 ng L)1 with the lowest concentration in the ZL (annual average: 8.2 lg L)1) and the highest concentration in LL (annual average: 197 lg L)1; Table 1).
Cyanobacterial and Bacterial Numbers
Fig. 2. Annual cycle (8 May 2000 to 28 May 2001) of conductivity (A), alkalinity (B), and DOC (C) in the five investigated soda pools: Oberer Stinkersee (OS), Unterer Stinkersee (US), Illmitzer Zicklacke (ZL), Lange Lacke (LL), and Wo¨ rthen Lacke (WL). Conductivity values represent the mean of three measurements; standard errors are smaller than the symbols used. Missing September values for ZL are due to complete evaporation of the pool.
observed in lakes located in the temperate climate zone. The conductivity in the five habitats increased with the summer evaporation to maximal values of 32 mS cm)1 (ZL) and decreased with the autumn and winter rainfalls and the subsequent groundwater raising (Fig. 2A). The conductivity was highly correlated with salinity (rs = 0.89, p < 0.001) and alkalinity (rs = 0.63, p < 0.001) and was a good indicator for the evaporative concentration. Salinity varied from 2.4 g L)1 to 31.3 g L)1 (Table 1) and was dominated by chloride, sulfate, carbonate, and bicarbonate anions and sodium cations. The proportion of
Cyanobacterial numbers ranged from 0 to 307 · 109 cells L)1 with highest values observed at OS and LL in early August 2000 and early May 2001, respectively. US exhibited two peaks with values of more than 170 · 109 cells L)1 in July and September (Fig. 3A). ZL and WL featured the lowest median cyanobacterial numbers (Table 2). During the winter months cyanobacterial numbers were low (1 and their explained variance
Fig. 4. Example of a microautoradiogram of autofluorescent picocyanobacteria from OS after the addition of 180 nM 3Hleucine (1200· magnification). The overwhelming majority of picocyanobacterial cells are not labeled. Arrows indicate sporadic autofluorescent cells with 3H-leucine label incorporation. The other silver grains in the leucine autoradiogram were associated with bacteria (at UV excitation 340–380 nm, barrier filter 430 nm).
Cyanobacterial numbers Bacterial secondary production Bacterial numbers Dissolved organic carbon Chlorophyll a Temperature Inorganic suspended solids Organic suspended solids Total phosphorus Alkalinity pH Conductivity Salinity Wind Explained variance (%) a
PC 1
PC 2
PC 3
PC 4
0.87 — 0.83 — 0.84 — 0.84 0.90 0.72 — — — — — 45.2
— — — 0.82 — — — — — — — 0.77 0.74 )0.75 17.3
— 0.82 — — — 0.90 — — — — — — — — 10.0
— — — — — — — — — 0.73 0.77 — — — 7.6
Variables not of importance for the explanation of five systems were omitted
50
Fig. 5. Two-dimensional plot of the principal component analysis (PCA) (rotation: varimax with Kaiser normalization) performed for the whole data set of all investigated soda pools. cond, conductivity; doc, dissolved organic carbon; sal, salinity; alk, alkalinity; bsp, bacterial secondary production; ptot, total phosphorus; sso, organic suspended solids; ssi, inorganic suspended solids; bn, bacterial numbers; cyb, cyanobacterial numbers; temp, temperature; chla, chlorophyll a.
iance was found at LL, whereas PC 1 (33% explained variance) is interpreted as a combination of suspended solids and phytoplankton. The turbidity and the concentration factor were of inverted importance in WL. PC 1, explaining 52% of the observed variance, additionally included BSP, chlorophyll a, and total phosphorus.
Discussion Soda Pools as Sites of Extreme Bacterial Abundance and Growth The soda pools of the national park Neusiedler See—Seewinkel appear to be sites of extremely high microbial activity and biomass. In past studies on hypertrophic aquatic environments highest bacterial numbers up to 356 · 109 L)1 were reported by Kilham [16] for African alkaline lakes. Grant et al. [12] reported that aerobic heterotrophic bacteria can reach numbers of 100 · 109 L)1 in dilute soda lakes, and Zinabu and Taylor [42] found maximal bacterial numbers of 117 · 109 L)1 in a variety of different Ethiopian soda lakes. These values are thus of the same magnitude as our measurements (Table
A. Eiler et al.
5). Ecosystems similar to the Austrian soda pools exist in Eastern Europe, Russia, and East Africa, but to the best of our knowledge no information is available on heterotrophic bacterial production and growth rates. The highest BSP rates found in the literature, up to 129 lg C L)1 h)1, were reported by Boon [5] for the Australian billabongs—values which were far exceeded by our measurements. White et al. [42] reported maximal l values of 0.36 h)1 for freshwater ecosystems and 1.28 h)1 for saltwater habitats, which also included data from an artificial aquaculture pond. In Table 5 ecosystems are listed which exhibit similarities to the Austrian soda pools in salinity, trophy, depth, turbidity, and/or alkalinity. With the exception of Big Soda Lake, all of the mentioned environments are shallow and highly productive. The study of Big Soda Lake was chosen because it provides the only data on bacterial production in aquatic alkaline environments. The presented environments in Table 5 exhibit significantly lower bacterial production and growth rates than in this study, except for the Indus River Delta: Bano et al. [3] reported an unprecedented bacterial growth rate of 1.0 h)1 for a natural assemblage, coinciding with a dense cyanobacterial bloom. For the East African soda lakes it is conceivable that growth rates of magnitude similar to those observed for the Austrian soda pools may be encountered, but no data are available. We suppose that the combination of shallowness, the existence of growing algal blooms, and high temperature is probably the driving factor enabling growth rates of l ‡ 1. The extremely high specific growth rates of up to 1.65 h)1, corresponding to doubling times of 25 min, suggest that bacterioplankton in the pools has the potential to grow at close to maximal rates. It was shown for laboratory cultures of Escherichia coli and other Enterobacteriaceae that the minimal time necessary for cell division under optimal nutrient and temperature conditions is in the range of 15–20 min [22]. We are aware that uptake rates of radiotracers do not directly measure growth. However, we believe that this approach provides a good estimate of bacterial growth rates, when conversion factors are chosen carefully and methodological limitations are taken into account. A recommended isotopic dilution of 2 [34] was applied for converting radioactive leucine uptake into carbon production. It is generally assumed that even at substrate concentrations leading to saturation of the incorporated label, intracellular isotope dilution does still occur. However, it is conceivable that in these extremely hypertrophic ecosystems bacteria do not synthesize leu-
Bacterial Communities in Soda Pools
51
Table 4. Principal component analysis of the five investigated soda pools showing the principal components (PC) with an eigenvalue >1 and their explained variance PC 1 OS Variables Expl. variance US Variables Expl. variance ZL Variables Expl. variance LL Variables Expl. variance WL Variables Expl. variance
PC 2
PC 3
(%)
cyb, bn, ssi, sso, ptot 34.9
doc, cond, sal, -wind 21.8
chla, temp 12.3
(%)
cyb, ssi, sso, ptot 58.6
bn, doc, cond, sal, -wind 15.0
bsp, temp, pH 9.8
(%)
cyb, bn, bsp, ssi, sso, doc, cond, sal 55.0
ptot, alk 17.8
chla, temp, pH, -wind 12.3
(%)
chla, ssi, sso, cond 32.6
cyb, bsp, bn, doc 19.8
temp, ptot, pH 13.8
(%)
bsp, doc, chla, ptot, cond, sal, -wind 52.2
cyb, bn, ssi, sso 14.1
temp, pH 11.1
PC 4 bsp, ptot 11.3
alk, sal 10.2
a
Variables of importance for the explanation (r > 0.65) of each system are shown. Abbreviations: cond, conductivity; doc, dissolved organic carbon; sal, salinity; alk, alkalinity; bsp, bacterial carbon production; ptot, total phosphorus; sso, organic suspended solids; ssi, inorganic suspended solids; bn, bacterial numbers; cyb, cyanobacterial numbers; temp, temperature; chla, chlorophyll a
cine in their cells when external sources are available at high concentrations. Therefore, when no isotopic dilution may be taken into account, the maximal l would then amount to 1.0 h)1 (LL) and 0.65 h)1 (ZL), respectively, corresponding to g = 42 min and g = 64 min. This is still only approximately two to four times slower than the minimal doubling time of Escherichia coli. Other sources of error are the conversion factors used in the calculations for converting cell volumes into carbon content and leucine incorporation into carbon production, i.e., mol% of leucine in protein and the cellular protein carbon moiety.
However, when bacterial abundance is determined by the direct-count method, the calculated growth rates are most probably underestimated because of the presence of nonactive cells [17]. As indicated by our microautoradiography results, the percentage of active bacteria in the pools varied from 40% to 90%, which would increase the calculated growth rates by a factor up to 2.5, corresponding to l > 1.65 h)1. Microautoradiograms, on the other hand, indicated clearly that cyanobacteria could be ruled out as contributing significantly to the leucine uptake, which would have led to an overestimation of
Table 5. Bacterial specific growth rates, abundance, chlorophyll a, dissolved organic carbon, pH, and salinity in selected estuarine areas, river deltas, and soda lakes
Ecosystem Indus River delta [3] Urdaibai estuary [32]
Description
Mangrove ecosystem Shallow, hypertrophic, turbid Humboldt Lake [33] Shallow, hypertrophic Australian billabongs [5] Shallow, hypertrophic, turbid Big soda lake [43] Meromictic lake Ethiopian soda lakes [44] Meso-, hypertrophic East African rift valley Meso-, hypertrophic [12, 13, 18a] Austrian soda pools Shallow, hypertrophic, (present study) turbid a
Salinity (g L)1)
pH
DOC chl a (mg C L)1) (lg L)1)
Bact. numbers (109 L)1)
BSP (lg C L)1 h)1
Growth rate (h)1)
32–38 1–35
n.d. n.d.
n.d.
