Advertisement

Limnology

pp 1–9 | Cite as

Characterization of phosphorus in algae from a eutrophic lake by solution 31P nuclear magnetic resonance spectroscopy

  • Weiying Feng
  • Cuicui Li
  • Chen Zhang
  • Shasha Liu
  • Fanhao Song
  • Wenjing Guo
  • Zhongqi He
  • Tingting Li
  • Haiyan Chen
Open Access
Research paper

Abstract

The identification and quantification of phosphorus (P) compounds derived from algal biomass are crucial for a better understanding of algal P dynamics in lake ecosystems. Quantity and species of P in algae collected from Chao Lake (a typical ultra-eutrophic lake) in China were analyzed by chemical analysis and 31P NMR. Total P (TP) in algae biomass ranged from 2671 to 5385 mg kg−1 of dry matter. Proportion of organic P (Po) accounted for 78.3 ± 2.6% in algae biomass collected from the western part of Chao Lake, which was higher than that (64.7 ± 1.4%) in the eastern part of the lake. Eight P species including inorganic P species (orthophosphate and pyrophosphate) and Po species (five monoesters P and diesters P) were identified in NaOH–EDTA extracts of algal samples. Monoesters P accounted for 48.4% in extracted TP, which was the main component of Po. β-glycerophosphates were the largest component of monoesters P, which accounted for 22.6% in extracted TP. This study improved knowledge on the mechanism of the cycling of endogenous P in the aquatic system and would be helpful in developing a strategy for control of repeated algae blooms in eutrophic Chao Lake.

Keywords

31P NMR Algae Organic phosphorus Lake Eutrophication 

Introduction

Algae blooms are serious environmental problems around the world, especially in developing countries (Kagaloua et al. 2008; Pernet-Coundrier et al. 2012). Algae blooms occur in an aquatic environment if too much phosphorus (P) enters the system (Giles et al. 2015). For a eutrophic lake, release of P from dead algae is an important nutrient source that will support continuous algal blooms in lakes (Li et al. 2009; Feng et al. 2016a). Algae are not usually collected by humans because they are not valuable, so that the debris is allowed to decompose in situ. The decomposition of algal residues affects the bio-cycling and release of P, increasing the risk of resurgence of algal blooms (Feng et al. 2016b; Lehman et al. 2017). Decaying algal debris releases both inorganic P (Pi) and Po. The Po constituents need to be hydrolyzed to bioavailable Po by various enzymes (Feng et al. 2016b). Therefore, the forms and concentrations of P in algae shall be evaluated while algae debris is decomposing. However, until now, studies of the species, concentrations, and effects of Po in algae of eutrophic lakes have been limited because of the complexity and limitations of analytical methods (Turner et al. 2005; Bell et al. 2017).

Typical analytical approaches, such as enzymatic reactivity, high performance liquid chromatography (HPLC), and mass spectrometry are based on operational definitions so that they cannot discern P classes at a molecular level (Suzumura 2005; Baldwin 2013; Karl 2014). Phosphorus-31 nuclear magnetic resonance spectroscopy (31P NMR) is a non-destructive, non-invasive technique for identifying chemical forms in various environmental samples. Solid-state 31P NMR is focused on inorganic P compounds, solution 31P NMR is mainly used to determine organic P compounds (Turner et al. 2005; He et al. 2011; Abdi et al. 2014; Sørensen et al. 2014). Several P compounds have been detected by solution 31P NMR, including phosphonates, orthophosphate,monoesters P, diesters P, pyrophosphates and polyphosphates (He et al. 2007; Turner et al. 2012; Zhu et al. 2013). Generally, monoesters P represent a wide range of important Po compounds, such as inositol phosphate and sugar phosphates (He et al. 2007; Doolette et al. 2009; Jarosch et al. 2015). Therefore, it is an ideal technique for analyzing Po species in algae of eutrophic lakes, as it would not only provide important information pertaining to P biogeochemical cycling in lake ecosystems, but also yield abundant insight into identities of specific P compounds.

Chao Lake (31°25′28″–31°43′28″N, 117°16′54″–117°51′46″E) is one of the five largest freshwater lakes in China. It is situated on the flood plains between the Yangtze River and Huai River in the central Anhui Province of eastern China (Zan et al. 2010; Tang et al. 2015). Chao Lake is a typical shallow lake with a mean depth of 3 m and a surface area of 780 km2 and drainage area of 13,350 km2 (Wang et al. 2013). Due to the rapid increase in anthropogenic activities in the lake’s watershed over recent decades, the lake has suffered from serious pollution, eutrophication and algae blooms (Xu et al. 2005). As a matter of fact, since the mid 1980s, algae blooms have occurred each year in Chao Lake (Chen and Liu 2014). In order to assess the environmental risks of algae on the eutrophic lake, this study analyzed the P species in algae by solution 31P NMR, and based on the knowledge obtained, predicted the P bioavailability of the algal biomass in aquatic environments.

Materials and methods

Study sites and sample collection

Samples of algae were collected from six sites in Chao Lake in September 2015 (Fig. 1). These sampling sites were located in different eutrophic areas. Generally, Chao Lake is divided into two parts: the western part (samples C1 and C2) and the eastern part (samples C3, C4, C5 and C6) along the line of Zhongmiao–Mushan–Qitouzui, as shown in Fig. 1. The quality of water was worst in the western part of the lake and gradually became better from west to east (Zhu et al. 2006; Tang et al. 2015). The lake’s annual mean concentrations of total nitrogen (TN) and TP approached 2.85 and 0.26 mg l−1, respectively, and the annual mean chlorophyll-a reached up to 25.6 μg l−1 (Li et al. 2015). Algae were collected by use of a plankton collector (HB403-BWS). Samples were placed in sealed bags and put in ice boxes immediately. These algal samples were freeze-dried, ground, then passed through a 2-mm sieve before being stored at −20 °C (Feng et al. 2016a). The dominant species in Chao Lake was Microcystic aeruginosa with an appearance frequency of 90.9% (Yang et al. 2011).
Fig. 1

Major inlets and outlets of Chao Lake with algal sampling sites

Extraction of P and chemical analysis

Samples of algae were extracted by use of optimized NaOH–EDTA extracting agent (mixtures of 0.5 mol l−1NaOH and 25 mmol l−1EDTA) with a ratio of 150:1 (ml g−1), and the mixtures were shaken for 18 h at room temperature (Cade-Menun and Preston 1996; Feng et al. 2016b). The extracting solutions were centrifuged (8000 × g) for 30 min, and filtered through 0.45-μm glass-fiber filters (Whatman GF/C). Extractable total phosphorus (ETP) after digestion and free molybdate reactive phosphorus (MRP) were measured using the molybdenum blue method (He and Honeycutt 2005). Extractable organic phosphorus (EOP) was calculated by the difference between ETP and MRP. The remaining extracts were freeze-dried for solution 31P NRM spectroscopy analysis.

Percentages of carbon (C) and nitrogen (N) in algae were determined by use of an elemental analyzer (Elementarvario macro EL, Germany). Total phosphorus (TP) and inorganic phosphorus (Pi) were determined by the SMT method described by Ruban et al. (2001). Organic phosphorus (Po) in algae samples was calculated by the difference between TP and Pi. There were three replications for extraction of P and chemical analysis. Data were checked for deviations from normality and homogeneity of variance before performing statistical analyses.

31P NMR analysis

A 100-mg sample of freeze-dried algal extracts was ground, and then redissolved in 1 ml 1 mol l−1 NaOH + 0.1 mol l−1 EDTA and 0.2 ml D2O. After ultrasonication for 30 min and equilibration for 5 min, 2% (v/v) of bicarbonate buffered dithionite (0.11 mol l−1 NaHCO3 + 0.11 mol l−1 Na2S2O4) was added to the extract to reduce interference from paramagnetic ions, such as Fe and Mn (He et al. 2009; Giles and Cade-Menun 2014). The pH of the supernatant solution was adjusted using 10 mol l−1 NaOH to ensure a pH > 12. The supernatant solution was centrifuged (8000 × g) for 30 min and transferred to a 5-mm NMR tube. Solution 31P NMR spectra were acquired at 24 °C on a Bruker AVANCE 400 MHz spectrometer at a 31P frequency of 161.98 MHz, using a 90° pulse, a 5 s relaxation delay and a 0.21 s acquisition time, similar to the parameters used in Feng et al. (2016b). The scan time for each sample was more than 15 h. Peak areas were calculated by integration and completed using MestrelabMNova v.10.

Spiking experiments

The peak of specific monoesters P forms (i.e., glucose 6-phosphate, riboncleotides, α-glycerophosphate, β-glycerophosphate, myo-inositol hexaphosphate) needs to be confirmed with spiking experiments (Fig. 4). Methods for identifying specific P forms in NMR spectra of soil and other environmental samples are well-established and have been used for many years (Smernik and Dougherty 2007; He et al. 2011; McDowell and Hill 2015), combined with P compound libraries developed by Turner et al. (2003); Doolette et al. (2009) and Cade-Menun (2015). Standard samples of monoesters P were purchased from Sigma-Aldrich. Spiked samples were analyzed by 31P NMR as described above. Monoesters P compounds were identified by their chemical shifts, with the orthophosphate peak in all spectra standardized to 6.0 ppm. Spectral processing was done using MestReNove software version 9.0.1 (MestReNove Research SL).

Results and analysis

Nutrients (C, N and P) in debris of algae

Composition of C, N and their ratios in debris of algae are shown in Table 1. Percentages of C ranged from 31.5 to 50.3% with a mean value of 41.9% in the algae samples from Chao Lake. Content of N was 5.2–7.8% with a mean value of 6.4%. Both contents of C and N of algae was greater than those of aquatic macrophytes, which has been widely reported previously (Zhong et al. 2012; Qu et al. 2013, Feng et al. 2016a). The ratio of C:N was a good predictor of degradation in algae and aquatic macrophytes with a lower ratio of C:N for material more readily degradation (Reitzel et al. 2006). In this study, the ratios of C:N in algae from the western lake (7.1 ± 0.3) were higher than those of the eastern lake (6.4 ± 0.3), suggesting higher lability of the algal debris of the eastern lake. The ratio of C:N of aquatic macrophytes (average 12.9) (Feng et al. 2016a) was greater than that of algae in Chao Lake (average 6.7) (Table 1). Therefore, the algae decomposed more easily than aquatic macrophytes in the same lake. This was also consistent with the results of previous studies (Liu et al. 2016).
Table 1

Contents of C, N, and P in algae and their NaOH–EDTA extraction efficiency in Chao Lake

Samples

Coordinates

Original algae powders

NaOH–EDTA extract algae samples

C (%)

N (%)

C:N

TP(mg kg−1)

Po(mg kg−1)

Po/TP(%)

ETP(mg kg−1)

EOP(mg kg−1)

C1

31°38′3.52″E, 117°21′16.74″N

44.8 ± 2.5a

6.7 ± 0.5

6.7 ± 0.3

4173 ± 516

3372 ± 126

80.8 ± 1.6

1864 ± 126(44.7)b

785 ± 124(23.3)b

C2

31°34′3.50″E, 117°24′51.80″N

39.5 ± 0.6

5.3 ± 0.8

7.5 ± 0.2

4059 ± 125

3072 ± 432

75.7 ± 3.5

1757 ± 214(43.3)

464 ± 52(15.1)

C3

31°30′9.64″E, 117°28′56.52″N

38.3 ± 1.8

5.4 ± 0.2

7.1 ± 0.4

3787 ± 256

2536 ± 59

67.0 ± 2.5

1572 ± 56(41.5)

351 ± 98(13.8)

C4

31°27′56.84″E, 117°34′50.00″N

31.5 ± 3.5

5.2 ± 0.1

6.1 ± 0.1

2671 ± 198

1476 ± 123

55.3 ± 1.4

1292 ± 89(48.4)

567 ± 15(38.4)

C5

31°33′27.70″E, 117°36′46.18″N

50.3 ± 2.9

7.8 ± 0.8

6.5 ± 0.4

3543 ± 112

2107 ± 78

59.5 ± 0.9

2774 ± 21(78.3)

1141 ± 215(54.2)

C6

31°36′10.25″E, 117°47′38.55″N

46.9 ± 4.6

7.8 ± 0.7

6.0 ± 0.2

5385 ± 290

4136 ± 19

76.8 ± 0.8

2183 ± 51(40.5)

1066 ± 164(25.8)

ETP extractable total phosphorus, EOP extractable organic phosphorus

aMean ± standard deviation (n = 3)

bValues in brackets show the percentage of ETP, EOP in NaOH–EDTA extracts to TP and Po in the unextracted algae powders, respectively

Contents of TP in debris of algae ranged from 2671 to 5385 mg kg−1 dry mass (dm) with a mean value of 3936 mg kg−1. The greatest concentration of TP in debris of algae was observed in sample C6. This may be because of two major inflowing rivers (e.g., the Zhe gao river and Shuang qiao river) with heavy nutrition inputs (Tang et al. 2015). Contents of TP in the surface sediments from Chao Lake only ranged from 420 to 1090 mg kg−1 with a mean value of 687 mg kg−1 (Zhang and Xing 2013). Content of TP in debris of algae from Chao Lake was approximately 5 times higher than TP in surface sediments. Therefore, dead algae-derived P might be an important source of bioavailable P for repeated algal blooming in eutrophic lakes such as Chao Lake. Concentration of Po in these algal samples ranged from 2107 to 4136 mg kg−1with a mean value of 2783 mg kg−1. The greatest concentration of Po was also observed in the heavily polluted region (i.e., sample C6). The proportion of Po in algae of the western lake (78.3% ± 2.6%) was higher than that in the eastern lake (64.7% ± 1.4%). The mean ratio of Po/TP of the six algal samples was 69.2% in Chao Lake (Table 1). This value was greater than that of algae from Tai Lake (mean ratio of Po/TP 57.8%) (Feng et al. 2016b). The previous studies reported that Po could be converted to bioavailable P (e.g., HPO42−) for algae blooming through a series of redox-driven solubilization reactions and phosphatase-mediated hydrolytic processes (Wang and Pant 2010; Zhu et al. 2015). Thus, we believed that Po in debris of algae from Chao Lake possessed larger bioavailability potential than algae from Tai Lake per their difference in Po/TP ratios.

NaOH–EDTA extractable P from algae

In this study, contents of NaOH–EDTA extractable TP ranged from 1292 to 2774 mg kg−1, with an extraction efficiency of 40.5–78.3%, and contents of extractable Po from algae ranged from 351 to 1141 mg kg−1, with an extraction efficiency of 13.8–54.2% (Table 1). The recoveries of Po in debris of algae from Chao Lake were lower than those with pure algae such as Microcystis, Chlorella vulgaris, and Sprilinaplatensis (Feng et al. 2016a). However, the extraction efficiencies of Po of algae from Chao Lake were similar to those of particulate P from Tai Lake (23–56%) (Bai et al. 2017) and of sediments from Haihe River (30–73%) (Zhang et al. 2017). The extraction efficiency of TP from algae from Chao Lake was similar to that of soils and sediments (49–83%) (Xu et al. 2005; Tang et al. 2015). Multiple-step extractions (e.g., additional or sequential HCl extraction) (He et al. 2008; Cade-Menun 2015; Zhu et al. 2016; Liu et al. 2017) seem needed to increase the P recovery from these algal samples.

Solution 31P NMR spectra of NaOH–EDTA extracts of algae

Eight main P species including inorganic P species (orthophosphate and pyrophosphate) and Po species (five monoesters P and diesters P) were identified in the NaOH–EDTA extracts of the six algal samples by solution 31P NMR (Fig. 2; Table 2). The peak of orthophosphate was at 6.00 ppm in the 31P NMR spectra, monoesters P was at 3.33–5.49 ppm, diesters P was at −0.69 to −0.31 ppm, and pyrophosphate was at −4.21 to −4.12 ppm (Fig. 2). The sum of orthophosphate and monoesters P in ETP accounted for more than 93% of ETP (Table 1; Fig. 3b). With the peak of orthophosphate as the largest signal in these 31P NMR spectra. The content of orthophosphate was between 615.1 and 1331.7 mg kg−1, and accounted for 41.5–54.0% of ETP (Table 1; Fig. 3). Polyphosphates were not detected in any algae of Chao Lake.
Fig. 2

Solution 31P NMR spectra of NaOH–EDTA extracts of algae in Chao Lake

Table 2

Concentrations of P compounds in NaOH–EDTA extracts of the algae determined by solution 31P NMR

Algae

Pi (mg kg−1)

Po (mg kg−1)

Orthophosphate

Pyrophosphate

Monoesters P

Diesters P

Total Po

Glucose 6-phosphate

Ribonucleotides

α-glycerophosphate

β-glycerophosphate

Other monoesters P

Total monoesters P

C1

818.2(43.9)a

n.d

32.7(1.8)

204.6(11.0)

60.6(3.2)

526.9(28.3)

220.9(11.9)

1045.7(56.1)

n.d

1045.7(56.1)

C2

938.1(53.4)

115.4(6.6)

42.2(2.4)

144.5(8.2)

63.8(3.6)

322.7(18.4)

130.4(7.4)

703.5(40.0)

n.d

703.5(40.0)

C3

849.1(54.0)

15.8(1.0)

n.d

137.6(8.7)

49.2(3.1)

325.2(20.5)

201.5(12.7)

714.1(45.0)

n.d

714.1(45.0)

C4

615.1(47.6)

65.8(5.1)

15.4(1.2)

131.2(8.8)

44.9(3.5)

297.7(23.0)

131.0(10.1)

604.4(46.6)

9.2(0.7)

611.4(47.3)

C5

1331.7(48.0)

87.9(3.2)

49.3(1.8)

487.4(17.6)

103.9(3.7)

636.6(22.9)

67.9(2.4)

1346.1(48.5)

9.3(0.3)

1354.4(48.8)

C6

905.6(41.5)

32.6(1.5)

92.4(4.2)

203.8(9.3)

70.6(3.2)

487.2(22.3)

329.6(15.1)

1184.0(54.2)

61.6(2.8)

1245.2(57.0)

Pi inorganic P, Po organic P, Total Po the sum of monoesters P and diesters P, n.d not detected

aValues in parentheses are percentages of individual P compounds in NaOH–EDTA extracts TP

Fig. 3

Content and percentage of major P types (a, b) and monoesters P compound forms (c, d) in algae collected from six sites (C1–C6) of Chao Lake

Monoesters P comprised the largest Po fraction with NaOH–EDTA extracts, and accounted for 48.4% (average) in ETP (Table 2; Fig. 3b). Through the spiking experiments (Fig. 4), the peak at 4.88 ± 0.02 ppm was assigned to α-glycerophosphates and the peak at 4.50 ± 0.02 ppm was assigned to β-glycerophosphates, based on Turner and Richardson (2004) and Doolette et al. (2009); the percentages of α- and β-glycerophosphates in ETP were 3.4% (65.5 mg kg−1) and 22.6% (432.7 mg kg−1), respectively. β-glycerophosphates were the largest component of monoesters P. The peak at 4.32 ± 0.01 ppm was assigned to ribonucleotides (He et al. 2011) and the percentage of ribonucleotides in ETP was 10.6% (218.2 mg kg−1). The peak at 5.12 ± 0.01 ppm was assigned to glucose 6-phosphate (Cade-Menun 2015), the percentage of which in ETP was 1.9% (38.7 mg kg−1). In addition, a few of the peaks in the monoesters P region were unidentified, because chemical shifts were strongly influenced by subtle differences among samples for viscosity, pH, salts and paramagnetic ions (Young et al. 2013; Abdi et al. 2014; He et al. 2011; Giles et al. 2015). Unidentified monoesters P are defined as ‘other monoesters P’ in this study. These other monoesters P accounted for 9.9% of ETP in algae of Chao Lake (Table 2).
Fig. 4

Solution 31P NMR spectra of monoesters P standard compounds (a–e) and C1 algal sample in Chao Lake (f)

Pyrophosphate was detected in most samples except the sample C1, which is consistent with a number of other studies (Bedrock et al. 1995; Mahieu et al. 2000; He et al. 2011). In other literature, polyphosphates and pyrophosphate were detected in some samples, but not necessarily (Busato et al. 2005; Feng et al. 2016b).

Discussion

Identification of inositol hexaphosphate (IHP) in algae of Chao Lake

The inositol hexaphosphate (IHP) stereoisomers (scyllo-, myo-, chiro-, neo-IHP) were important monoesters P components in many environmental samples (Turner et al. 2012; Cade-Menun 2015). Each of these compounds contains six phosphates, and the conformation of those phosphate groups causes them to have multiple peaks in a single spectrum, in an arrangement specific to each compound. The only exception is scyllo-IHP, which has one peak for the six phosphates; the peak at 3.55 ± 0.02 ppm was assigned to scyllo-IHP, based on Turner and Richardson (2004) and Doolette et al. (2009). None of the spectra shown in Fig. 2 have a peak at 3.55 ppm, so the scyllo-IHP was not present in algae of Chao Lake. Myo-IHP has four peaks in a 1:2:2:1 arrangement (with respect to peak areas), with peaks at 5.79 ± 0.01, 4.88 ± 0.01, 4.55 ± 0.01 and 4.42 ± 0.01 ppm (in Fig. 4e). Three of these peaks were not present in algae samples in Chao Lake (Fig. 2), so myo-IHP was not present in algae of Chao Lake. The fact that myo-IHP had not been observed in algae in a previous study is consistent with the observation of this study (Feng et al. 2016a). For chiro-IHP [in either the 4 equatorial/2 axial (4e/2a) conformation or the 2e/4a conformation], three peaks must be clearly visible, in a 2:2:2 arrangement, and the diagnostic peaks for each are at 6.2–6.5 ppm (Cade-Menun 2015); however, none of the spectra shown in Fig. 2 have any peaks between 6.0 and 7.0 ppm, so these compounds were not present in algae of Chao Lake. In addition, neo-IHP requires two peaks to be present, in a 4:2 arrangement, so that the peak at 6.4 ± 0.01 ppm is twice as large as the one at 4.3 ± 0.01 ppm. Given that there were no peaks between 6.0 and 7.0 ppm, it can be assumed that neo-IHP was not present in algae of Chao Lake.

Degradation behaviors of diesters P in algae of Chao Lake

Apart from monoesters P, other important Po compounds, diesters P, were detected in some algae samples. The concentration of diesters P was generally low (mean 0.63% of ETP), compared to other Po fractions, and only detected in samples C4, C5 and C6 (9.2–61.6 mg kg−1).

It is well established that some diesters P such as phospholipids and RNA can degrade to monoesters P [e.g., α-,β-glycerophosphates (phospholipids) and various monophosphates (e.g., nucleotides) when analyzed at the high pH required for good peak separation in 31P NMR spectra](Turner et al. 2003; Doolette et al. 2009; He et al. 2011; Schneider et al. 2016). The degree of degradation will vary depending on the length of NMR experiment and other factors (Cade-Menun and Liu 2014; Cade-Menun 2015; Feng et al. 2018). It was essential that these degradation peaks were identified and quantified, in order to determine the correct concentrations of monoesters P and diesters P (Young et al. 2013; Vincent et al. 2013). Therefore, the corrected total monoesters P and corrected total diesters P were those corrected by moving the percentages of α- and β-glycerophosphates and nucleotides from monoesters P to diesters P. When uncorrected, the total monoesters P were significantly higher than the total diesters P, but the reverse was true for the corrected values.

Eutrophication and algal blooming versus biogeochemical cycling of algae-derived P in Chao Lake

Based on the results in this study, we were able to think further about the biogeochemical cycling of P driven by algal blooming in Chao Lake. The TP of algae-derived biomass loading was 10.94 × 103 kg in Chao Lake (Li et al. 2015). With the Po content in algae determined in this study (Table 1), we estimated the Po biomass of algae to be approximately 7.57 × 103 kg in Chao Lake. In previous research (Feng et al. 2016b) with Tai Lake samples, we estimated that approximately 32.7–41.3% of extractable Po from algae has the potential for phosphatase hydrolysis to soluble orthophosphate which can be released into the water body. Thus, in the case of Chao Lake, this bioavailable P would be 2475–3126 kg in algae and would be released into the water and promote repeated algal blooms in Chao Lake if not appropriately removed naturally or artificially. This conclusion indicated that decomposition of algal debris would be a key factor in regeneration of bioavailable P for life in eutrophic lakes, even when external P is excluded. It is therefore necessary to remove algae debris from eutrophic lakes to control the release of P from internal P cycling and the phenomenon of eutrophication of lakes.

Conclusion

This research used solution 31P NMR to provide insights into the P species and distribution of P in algae of the heavily polluted Chao Lake. Data derived from this study showed that the eutrophic lake algae have accumulated remarkable amounts of Pi and Po. The proportion of Po in algae ranged from 55.3 to 80.8% with a mean of 69.2% in Chao Lake.

Eight compounds P were detected in the NaOH–EDTA extracts of algal samples by 31P NMR. The sum of orthophosphate and monoesters P in ETP was greater than 93% of algal P. Our observations implied that the release of P induced by the decomposition of algae debris could be a potential source of bioavailable P in aquatic systems of Chao Lake even without any more external P input. Thus, recycling of the potential bioavailable P in algae might be the mechanism of repeated algae blooming in eutrophic Chao Lake. Remediation of the lake requires a strategy to remove the algal biomass P effectively.

Notes

Acknowledgements

This research was jointly supported by the National Natural Science Foundation of China (41703115, 41521003, 41630645, 41807372) and Postdoctoral Science Foundation of China (2017M610967).

References

  1. Abdi D, Cade-Menun BJ, Ziadi N, Parent LE (2014) Long-term impact of tillage practices and P fertilization on soil P forms as determined by 31P-NMR spectroscopy. J Environ Qual 43:1432–1441CrossRefGoogle Scholar
  2. Bai X, Sun J, Zhou Y, Gu L, Zhao H, Wang J (2017) Variations of different dissolved and particulate phosphorus classes during an algae bloom in a eutrophic lake by 31P NMR spectroscopy. Chemosphere 169:577–585CrossRefGoogle Scholar
  3. Baldwin DS (2013) Organic phosphorus in the aquatic environment. Environ Chem 10:439–454CrossRefGoogle Scholar
  4. Bedrock CN, Cheshire MV, Chudek JA, Fraser AR, Goodman BA, Shand CA (1995) Effect of pH on precipitation of humic acid from peat and mineral soils on the distribution of phosphorus forms in humic and fulvic acid fractions. Commun Soil Sci Plant Anal 26:1411–1425CrossRefGoogle Scholar
  5. Bell DW, Pellechia P, Chambers LR, Longo AF, McCabe KM, Ingall ED, Benitez-Nelson CR (2017) Isolation and molecular characterization of dissolved organic phosphorus using electrodialysis-reverse osmosis and solution 31P-NMR. Limnol Oceanogr-Methods.  https://doi.org/10.1002/lom3.10171 CrossRefGoogle Scholar
  6. Busato JG, Canellas LP, Rumjanek VM, Velloso ACX (2005) Phosphorus in an inceptisol under long-term sugarcane: II. Humic acid analysis by NMR P-31. Rev Bras Cienc Solo 29:945–953CrossRefGoogle Scholar
  7. Cade-Menun BJ (2015) Improved peak identification in 31P-NMR spectra of environmental samples with a standardized method and peak library. Geoderma 257:102–114CrossRefGoogle Scholar
  8. Cade-Menun BJ, Liu CW (2014) Solution phosphorus-31 nuclear magnetic resonance spectroscopy of soils from 2005 to 2013: a review of sample preparation and experimental parameters. Soil Sci Soc Am J 78:19–37CrossRefGoogle Scholar
  9. Cade-Menun BJ, Preston CM (1996) A comparison of soil extraction procedures for 31P NMR spectroscopy. Soil Sci 161:770–785CrossRefGoogle Scholar
  10. Chen Y, Liu Q (2014) On the horizontal distribution of algal-bloom in Chaohu Lake and its formation process. Acta Mech Sinca 30:656–666CrossRefGoogle Scholar
  11. Doolette A, Smernik R, Dougherty W (2009) Spiking improved solution phosphorus-31 nuclear magnetic resonance identification of soil phosphorus compounds. Soil Sci Soc Am J 73:919–927CrossRefGoogle Scholar
  12. Feng W, Zhu Y, Wu F, Meng W, Giesy JP, He Z, Song L, Fan M (2016a) Characterization of phosphorus forms in lake macrophytes and algae by solution 31P nuclear magnetic resonance spectroscopy. Environ Sci Pollut Res 23:7288–7297CrossRefGoogle Scholar
  13. Feng W, Zhu Y, Wu F, He Z, Zhang C, Giesy JP (2016b) Forms and lability of phosphorus in algae and aquatic macrophytes characterized by solution 31P NMR coupled with enzymatic hydrolysis. Sci Rep 6:37164CrossRefGoogle Scholar
  14. Feng W, Wu F, He Z, Song F, Zhu Y, Giesy JP, Wang Y, Qin N, Zhang C, Chen H, Sun F (2018) Simulated bioavailability of phosphorus from aquatic macrophytes and phytoplankton by aqueous suspension and incubation with alkaline phosphatase. Sci Total Environ 616:1431–1439CrossRefGoogle Scholar
  15. Giles CD, Cade-Menun BJ (2014) Applied manure and nutrient chemistry for sustainable agriculture and environment. In: Zhang H (ed) Phytate in animal manure and soils: abundance, cycling and bioavailability. Springer, The Netherland, pp 163–190Google Scholar
  16. Giles CD, Lee LG, Cade-Menun BJ, Hill JE, Isles PD, Schroth AW, Druschel GK (2015) Characterization of organic phosphorus form and bioavailability in lake sediments using P nuclear magnetic resonance and enzymatic hydrolysis. J Environ Qual 44:1–13CrossRefGoogle Scholar
  17. He Z, Honeycutt CW (2005) A modified molybdate blue method for orthophosphate determination suitable for investigating enzymatic hydrolysis of organic phosphates. Commun Soil Sci Plant Anal 36:1373–1383CrossRefGoogle Scholar
  18. He Z, Cade-Menun BJ, Toor GS, Sim JT (2007) Comparison of phosphorus forms in wet and dried animal manures by solution phosphorus-31 nuclear magnetic resonance spectroscopy and enzymatic hydrolysis. J Environ Qual 36:1086–1095CrossRefGoogle Scholar
  19. He Z, Honeycutt CW, Cade-Menun BJ, Senwo ZN, Tazisong IA (2008) Phosphorus in poultry litter and soil: enzymatic and nuclear magnetic resonance characterization. Soil Sci Soc Am J 72:1425–1433CrossRefGoogle Scholar
  20. He Z, Honeycutt CW, Griffin TS, Cade-Menun BJ, Pellechia PJ, Dou Z (2009) Phosphorus forms in conventional and organic dairy manure identified by solution and solid state P-31 NMR spectroscopy. J Environ Qual 38:1909–1918CrossRefGoogle Scholar
  21. He Z, Olk DC, Cade-Menun BJ (2011) Forms and lability of phosphorus in humic acid fractions of Hord silt loam soil. Soil Sci Soc Am J 75:1712–1722CrossRefGoogle Scholar
  22. Jarosch KA, Doolette AL, Smernik RJ, Tamburini F, Frossard E, Bünemann EK (2015) Characterisation of soil organic phosphorus in NaOH–EDTA extracts: a comparison of 31P NMR spectroscopy and enzyme addition assays. Soil Biol Biochem 91:298–309CrossRefGoogle Scholar
  23. Kagaloua I, Papastergiadoub E, Leonardasa I (2008) Long-term changes in the eutrophication process in a shallow Mediterranean lake ecosystem of W Greece: response after the reduction of external load. J Environ Manag 87:497–506CrossRefGoogle Scholar
  24. Karl DM (2014) Microbially mediated transformations of phosphorus in the sea: new views of an old cycle. Ann Rev Mar Sci 6:279–337CrossRefGoogle Scholar
  25. Lehman PW, Kurobe T, Lesmeister S, Baxa D, Tung A, Teh SJ (2017) Impacts of the 2014 severe drought on the Microcystis bloom in San Francisco estuary. Harmful Algae 63:94–108CrossRefGoogle Scholar
  26. Li M, Wu Y, Yu Z, Sheng G, Yu H (2009) Enhanced nitrogen and phosphorus removal from eutrophic lake water by Ipomoea aquatica with low-energy ion implantation. Water Res 43:1247–1256CrossRefGoogle Scholar
  27. Li J, Cui K, Lu W, Cheng Y, Jiang Y (2015) Community dynamics of spring-summer plankton in Lake Chaohu. Acta Hydrobiol Sinica 39:185–194 (in Chinese) Google Scholar
  28. Liu S, Zhu Y, Meng W, He Z, Feng W, Zhang C, Giesy JP (2016) Characteristics and degradation of carbon and phosphorus from aquatic macrophytes in lakes: insights from solid-state 13C NMR and solution 31P NMR spectroscopy. Sci Total Environ 543:746–756CrossRefGoogle Scholar
  29. Liu S, Zhu Y, Wu F, Meng W, Wang H, He Z, Guo W, Song F, Giesy JP (2017) Using solid 13C NMR coupled with solution 31P NMR spectroscopy to investigate molecular species and lability of organic carbon and phosphorus from aquatic plants in Tai Lake. China Environ Sci Pollut Res 24:1880–1889CrossRefGoogle Scholar
  30. Mahieu N, Olk DC, Randall EW (2000) Analysis of phosphorus in two humic acid fractions of intensively cropped lowland rice soils by 31P NMR. Eur J Soil Sci 51:391–402CrossRefGoogle Scholar
  31. McDowell RW, Hill SJ (2015) Speciation and distribution of organic phosphorus in river sediments: a national survey. J Soil Sediment 15:2369–2379CrossRefGoogle Scholar
  32. Pernet- Coundrier B, Qi WX, Liu HJ, Nüller B, Berg M (2012) Sources and pathway of nutrients in the semi-arid region of Beijing–Tianjin. China Environ Sci Technol 46:5294–5301CrossRefGoogle Scholar
  33. Qu X, Xie L, Lin Y, Bai Y, Zhu Y, Xie F, Geisy JP, Wu F (2013) Quantitative and qualitative characteristics of dissolved organic matter from eight dominant aquatic macrophytes in Lake Dianchi. China Environ Sci Pollut Res 20:7413–7423CrossRefGoogle Scholar
  34. Reitzel K, Ahlgren J, Gogoll A (2006) Effects of aluminum treatment on phosphorus, carbon, and nitrogen distribution in lake sediment: a 31P NMR study. Water Res 40:647–654CrossRefGoogle Scholar
  35. Ruban V, López-Sánchez JF, Pardo P (2001) Harmonized protocol and certified reference material for the determination of extractable contents of phosphorus in freshwater sediments—a synthesis of recent works. Fresen J Anal Chem 370:224–228CrossRefGoogle Scholar
  36. Schneider K, Resl P, Spribille T (2016) Escape from the cryptic species trap: lichen evolution on both sides of a cyanobacterial acquisition event. Mol Ecol 25:3453–3468CrossRefGoogle Scholar
  37. Smernik RJ, Dougherty WJ (2007) Identification of phytate in phosphorus-31 nuclear magnetic resonance spectra: the need for spiking. Soil Sci Soc Am J 71:1045–1050CrossRefGoogle Scholar
  38. Sørensen DR, Nielsen UG, Skou EM (2014) Solid state 31P MAS NMR spectroscopy and conductivity measurements on NbOPO4 and H3PO4 composite materials. J Solid State Chem 219:80–86CrossRefGoogle Scholar
  39. Suzumura M (2005) Phospholipids in marine environments: a review. Talanta 66:422–434CrossRefGoogle Scholar
  40. Tang J, Shi T, Wu X, Cao H, Li X, Hua R, Tang F, Yue Y (2015) The occurrence and distribution of antibiotics in Lake Chaohu, China: seasonal variation, potential source and risk assessment. Chemosphere 122:154–161CrossRefGoogle Scholar
  41. Turner BL, Richardson AE (2004) Identification of -inositol phosphates in soil by solution phosphorus-31 nuclear magnetic resonance spectroscopy. Soil Sci Soc Am J 68:802–808CrossRefGoogle Scholar
  42. Turner BL, Mahieu N, Condron LM (2003) Phosphorus-31 nuclear magnetic resonance spectral assignments of phosphorus compounds in soil NaOH–EDTA extracts. Soil Sci Soc Am J 67:497–510CrossRefGoogle Scholar
  43. Turner BL, Cade-Menun BJ, Condron LM, Newman S (2005) Extraction of soil organic phosphorus. Talanta 66:294–306CrossRefGoogle Scholar
  44. Turner BL, Cheesman AW, Godage HY, Riley AM, Potter BVL (2012) Determination of neo- and d-chiro-inositol hexakisphosphate in soils by solution 31P NMR spectroscopy. Environ Sci Technol 46:4994–5002CrossRefGoogle Scholar
  45. Vincent AG, Vestergren J, Gröbner G, Persson P, Schleucher J, Biesler R (2013) Soil organic phosphorus transformations in a boreal forest chronosequence. Plant Soil 367:149–162CrossRefGoogle Scholar
  46. Wang J, Pant HK (2010) Enzymatic hydrolysis of organic phosphorus in river bed sediments. Eco Eng 36:963–968CrossRefGoogle Scholar
  47. Wang X, Xi B, Huo S, Deng L, Pan H, Xia X, Zhang J, Ren Y, Liu H (2013) Polybrominateddiphenyl ethers occurrence in major inflowing rivers of Lake Chahu (China): characteristics, potential sources and inputs to lake. Chemosphere 93:1624–1631CrossRefGoogle Scholar
  48. Xu M, Cao H, Xie P, Deng D, Feng W, Xu J (2005) The temporal and spatial distribution, composition and abundance of protozoa in Chaohu Lake, China: relationship with eutrophication. Europ J Protistol 41:183–192CrossRefGoogle Scholar
  49. Yang L, Han X, Sun P, Yan W, Li Y (2011) Canonical correspondence analysis of algae community and its environmental factors in Lake Chaohu. China J Agro-Environ Sci 30:952–958Google Scholar
  50. Young EO, Ross DS, Cade-Menun BJ, Liu CW (2013) Phosphorus speciation in riparian soils: a phosphorus-31 nuclear magnetic resonance spectroscopy and enzyme hydrolysis study. Soil Sci Soc Am J 77:1636–1647CrossRefGoogle Scholar
  51. Zan F, Huo S, Xi B, Li Q, Liao H, Zhang J (2010) Phosphorus distribution in the sediments of a shallow eutrophic lake. Lake Chaohu, China. Environ Earth Sci 62:1643–1653CrossRefGoogle Scholar
  52. Zhang WQ, Xing BS (2013) Detection of phosphorus species in the sediments of Chaohu Lake by 31P nuclear magnetic resonance spectroscopy (31P-NMR). Acta Sci Circum 33:1967–1973 (in Chinese) Google Scholar
  53. Zhang WQ, Zhu XL, Jin X, Meng X, Tang WZ, Shan BQ (2017) Evidence for organic phosphorus activation and transformation at the sediment-water interface during plant debris decomposition. Sci Total Environ 583:458–465CrossRefGoogle Scholar
  54. Zhong W, Zhang Z, Luo Y (2012) Biogas productivity by co-digesting Taihu blue algae with corn straw as an external carbon source. Bioresource Technol 114:281–286CrossRefGoogle Scholar
  55. Zhu G, Qin B, Zhang L, Luo L (2006) Geochemical forms of phosphorus in sediments of three large, shallow lakes of China. Pedosphere 16:726–734CrossRefGoogle Scholar
  56. Zhu Y, Wu F, He Z, Guo J, Qu X, Xie F, Giesy JP, Liao H, Guo F (2013) Characterization of organic phosphorus in lake sediments by sequential fractionation and enzymatic hydrolysis. Environ Sci Technol 47:7679–7687CrossRefGoogle Scholar
  57. Zhu Y, Wu F, He Z (2015) Bioavailability and preservation of organic phosphorus in freshwater sediments and its role in lake eutrophication. In: He Z, Wu F (eds) Labile organic matter—chemical compositions, function, and significance in soil and the environment. SSSA, Madison, pp 275–294Google Scholar
  58. Zhu Y, Wu F, Feng W, Liu S, Giesy JP (2016) Interaction of alkaline phosphatase with minerals and sediments: activities, kinetics and hydrolysis of organic phosphorus. Colloids surf A: Physicochem Eng Aspects 495:46–53CrossRefGoogle Scholar

Copyright information

© The Author(s) 2018

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  • Weiying Feng
    • 1
  • Cuicui Li
    • 1
    • 2
    • 3
  • Chen Zhang
    • 1
  • Shasha Liu
    • 1
  • Fanhao Song
    • 1
  • Wenjing Guo
    • 1
  • Zhongqi He
    • 4
  • Tingting Li
    • 1
  • Haiyan Chen
    • 1
  1. 1.State Key Laboratory of Environmental Criteria and Risk AssessmentChinese Research Academy of Environmental SciencesBeijingChina
  2. 2.Guangzhou Institute of GeochemistryChinese Academy of SciencesGuangzhouChina
  3. 3.University of Chinese Academy of SciencesBeijingChina
  4. 4.USDA-ARSSouthern Regional Research CenterNew OrleansUSA

Personalised recommendations