Off-flavor compounds from decaying cyanobacterial blooms of Lake Taihu

The effect of cyanobacterial bloom decay on water quality and the complete degradation of cyanobacterial blooms in a short period were examined by an enclosure experiment in Gonghu Bay of Lake Taihu,China.Water quality parameters as well as taste and odor compounds during the breakdown of cyanobacterial blooms were measured.Results showed that the decay of cyanobacterial blooms caused anoxic water conditions,decreased pH,and increased nutrient loading to the lake water.The highest concentrations of dimethyl sulfide (DMS),dimethyl trisulfide (DMTS),and β-cyclocitral were observed in the anoxic water,at 62331.8,12413.3,and 1374.9 ng/L,respectively.2-Methylisoborneol was dominant during the live growth phase of cyanobacterial blooms,whereas DMS and DMTS were dominant during the decomposition phase.Dissolved oxygen,pH,and chlorophyll a were negatively correlated with DMS,DMTS,and β-cyclocitral,whereas total phosphorus,total nitrogen,and ammonium (NH4+-N) were positively correlated with DMS,DMTS,β-cyclocitral,and β-ionone.The experimental results suggested that preventing the anaerobic decomposition of cyanobacterial blooms is an important strategy against the recurrence of a malodor crisis in Lake Taihu.     

Microcystis aeruginosa/Pseudomonas pseudoalcaligenes interaction effects on off-flavors in algae/bacteria co-culture system under different temperatures

We conducted an experiment to study the interaction effects of Microcystis aeruginosa and Pseudomonas pseudoalcaligenes on off-flavors in an algae/bacteria co-culture system at three temperatures (24, 28 and 32°C). Gas chromatography–mass spectrometry was applied to measure off-flavor compounds dimethyl sulfide (DMS), dimethyl trisulfide (DMTS), 2-methylisoborneol, geosmin (GEO) and β-cyclocitral. During the lag phase of co-cultured M. aeruginosa (first 15 days), P. pseudoalcaligenes significantly increased the production of DMS, DMTS and β-cyclocitral at all three temperatures. In the exponential phase of co-cultured M. aeruginosa (after 15 days), M. aeruginosa became the main factor on off-flavors in the co-culture system, and β-cyclocitral turned to the highest off-flavor compound. These results also indicated that DMS, DMTS and β-cyclocitral were the main off-flavor compounds in our M. aeruginosa/P. pseudoalcaligenes co-culture system. Univariate analysis was applied to investigate the effects of M. aeruginosa and P. pseudoalcaligenes on the production of off-flavors. The results demonstrated that both M. aeruginosa and P. pseudoalcaligenes could increase the production of DMS and DMTS, while β-cyclocitral was mainly determined by M. aeruginosa. Our results also provide some insights into understanding the relationship between cyanobacteria and heterotrophic bacteria.     

Simultaneous determination of ten taste and odor compounds in drinking water by solid-phase microextraction combined with gas chromatography-mass spectrometry

Taste and odor （T＆O） problems in drinking water frequently occur because of many compounds present in the water, of which trans-1,10-dimethyl-trans-9-decalol （geosrnin） and 2-methylisoborneol （MIB） are well-known. In this study, a fast and effective method was established for simultaneous determination of 10 T＆O compounds, including geosmin, MIB, 2,4,6-trichloroanisole （TCA）, 2-methylbenzofuran, 2-isopropyl-3-methoxypyrazine （IPMP）, 2-isobutyl-3-methoxypyrazine （IBMP）, cis-3-hexenyl acetate, trans,trans-2,4-heptadienal, trans, cis-2,6-nonadienal, and trans-2-decenal in water samples by headspace solid-phase microextraction （SPME） coupled with gas chromatography-mass spectrometry. An orthogonal array experimental design was used to optimize the effects of SPME fiber, extraction temperature, stirring rate, NaC1 content, extraction time, and desorption time. The limits of detection ranged from 0.1 to 73 ng/L were lower than or close to the odor threshold concentrations （OTCs）. All the 10 T＆O compounds were detected in the 14 water samples including surface water, treatment process water and tap water, taken from a waterworks in Lianyungang City, China. MIB and geosmin were detected in most samples at low concentration. Six T＆O compounds （IPMP, IBMP, trans,cis-2,6-nonadienal, 2-methylbenzofuran, trans-2-decenal, and TCA） were effectively decreased in water treatment process （sedimentation and filtration） that is different from cis-3-hexenyl acetate, MIB and geosmin. It is noted that the TCA concentrations at 15.9-122.3 ng/L and the trans,cis-2,6-nonadienal concentrations at 79.9-190.1 ng/L were over 10 times higher than their OTCs in tap water. The variation of the analytes in the all water samples, especially distribution system indicated that distribution system cannot be ignored as a T＆O compounds source.     

洞庭湖水体异味物质及其与藻类和水质的关系

以洞庭湖水体中异味物质为研究对象,开展异味物质调查,并结合藻类结构、水质及其营养状况等因素,深入分析洞庭湖异味物质的来源和变化情况. 结果表明,DMS(dimethylsulfide,甲硫醚)、DMTS(dimethyltrisulfide,二甲基三硫醚)、β-cyclocitral(β-环柠檬醛)、MIB(2-methylisoborneol,二甲基异冰片)和GSM(geosmin,土嗅素)在全湖广泛存在,其最高质量浓度分别达到500.80、28.80、21.84、14.50和22.40 ng/L. 结合与藻类生物量的相关分析发现,直链藻、冠盘藻等硅藻可能是洞庭湖中DMS、DMTS和β-cyclocitral的重要来源,湖区土壤、沉积物中的微生物和死亡分解的藻类是MIB和GSM主要来源. 洞庭湖水体绝大部分处于中营养水平,其中东洞庭湖TLI(综合营养状态指数,为48.3)最高,南洞庭湖(为47.3)其次,西洞庭湖(为42.7)最低. 异味物质含量和水质的相关分析发现,异味物质质量浓度与TLI、水温、pH、ρ(DO)、ρ(TN)和ρ(COD_Mn)显著相关,说明水质对异味物质含量有重要影响.      

Beyond hypoxia：Occurrence and characteristics of black blooms due to the decomposition of the submerged plant Potamogeton crispus in a shallow lake

Organic matter-induced black blooms(hypoxia and an offensive odor) are a serious ecosystem disasters that have occurred in some large eutrophic shallow lakes in China. In this study, we investigated two separate black blooms that were induced by Potamogeton crispus in Lake Taihu, China. The main physical and chemical characteristics, including color- and odor-related substances, of the black blooms were analyzed. The black blooms were characterized by low dissolved oxygen concentration(close to 0 mg/L), low oxidation-reduction potential, and relatively low pH of overlying water. Notably higher Fe2+and∑S2-were found in the black-bloom waters than in waters not affected by black blooms. The black color of the water may be attributable to the high concentration of these elements, as black FeS was considered to be the main substance causing the black color of blooms in freshwater lakes. Volatile organic sulfur compounds, including dimethyl sulfide, dimethyl disulfide, and dimethyl trisulfide, were very abundant in the black-bloom waters. The massive anoxic degradation of dead Potamogeton crispus plants released dimethyl sulfide, dimethyl disulfide, and dimethyl trisulfide, which were the main odor-causing compounds in the black blooms. The black blooms also induced an increase in ammonium nitrogen and soluble reactive phosphorus levels in the overlying waters. This extreme phenomenon not only heavily influenced the original lake ecosystem but also greatly changed the cycling of Fe, S, and nutrients in the water column.     

Effects of elevated CO2 on dynamics of microcystin-producing and non-microcystin-producing strains during Microcystis blooms

In an attempt to elucidate the effects of different CO₂ concentrations (270, 380, and 750 μL/L) on the competition of microcystin-producing (MC-producing) and non-MC-producing Microcystis strains during dense cyanobacteria blooms, an in situ simulation experimentwas conducted in the Meiliang Bay of Lake Taihu in the summer of 2012. The abundance of total Microcystis and MC-producing Microcystis genotypes was quantified based on the 16S rDNA and mcyD gene using real-time PCR. The results showed that atmospheric CO₂ elevation would significantly decrease the pH value and increase the dissolved inorganic carbon (DIC) concentration. Changes in CO₂ concentration did not show significant influence on the abundance of total Microcystis population. However, CO₂ concentrations may be an important factor in determining the subpopulation structure of Microcystis. The enhancement of CO₂ concentrations could largely increase the competitive ability of non-MC-producing over MC-producing Microcystis, resulting in a higher proportion of non-MC-producing subpopulation in treatments using high CO₂ concentrations. Concurrently, MC concentration in water declined when CO₂ concentrations were elevated. Therefore, we concluded that the increase of CO₂ concentrations might decrease potential health risks of MC for human and animals in the future.     

Seasonal dynamics of water bloom-forming Microcystis morphospecies and the associated extracellular microcystin concentrations in large, shallow, eutrophic Dianchi Lake

The increasing occurrence of Microcystis blooms is of great concern to public health and ecosystem due to the potential hepatotoxic microcystins （MCs） produced by these colonial cyanobacteria. In order to interpret the relationships between variations of Microcyst/s morphospedes and extracellular MC concentrations, the seasonal dynamics of phytoplankton community composition, MC concentrations, and environmental parameters were monitored monthly from August, 2009 to July, 2010. The results indicated that Microcystis dominated total phytoplankton abundance from May to December （96%--99% of total biovolume）, with toxic Microcystis viridis and non-toxic Microcystis wesenbergii dominating after July （constituting 65%- 95% of the Microcystis population）, followed by M. viridis as the sole dominant species from November to January （49%--93%）. Correlation analysis revealed that water temperature and nutrient were the most important variables accounting for the occurrence ofM. wesenbergii, while the dominance ofM. viridis was related with nitrite and nitrate. The relatively low content of MCs was explained by the association with a large proportion of M. viriclis and M. wesenbergii, small colony size of Microcystis populations, and low water temperature, pH and dissolved oxygen. The extracellular MC （mean of 0.5 ± 0.2 μg/L） of water samples analyzed by enzyme-linked immunosorbent assay （ELISA） demonstrated the low concentrations of MC in Dianchi Lake which implied the low potential risk for human health in the basin. The survey provides the first whole lake study of the occurrence and seasonal variability of Microcyst/s population and     

洪泽湖有毒和无毒微囊藻丰度及其与环境因子之间的相关分析

为了解洪泽湖有毒和无毒微囊藻丰度及其空间分布,于2014年8月对洪泽湖30个采样点水体的营养盐浓度和Calson富营养化指数(trophic state index,TSI)进行研究,同时采用实时荧光定量PCR技术测定了有毒和无毒微囊藻丰度.结果表明,洪泽湖水体的总氮和总磷浓度平均值分别为1.63 mg·L-1和0.11 mg·L-1,富营养化指数在58.1~73.6之间,洪泽湖水质呈富营养化状态;有毒微囊藻在洪泽湖广泛分布,其丰度在1.13×104~3.51×106copies·m L-1之间,总微囊藻丰度在1.06×105~1.10×107copies·m L-1之间,有毒微囊藻占总微囊藻的比例在8.5%~38.5%之间,平均值为23.6%,有毒微囊藻丰度及其比例均呈现出明显的空间差异性;相关分析结果显示,总微囊藻、有毒微囊藻和有毒微囊藻所占比例三者之间呈极显著正相关性(P0.01),总微囊藻和有毒微囊藻丰度与叶绿素a浓度和TSI有极显著正相关性(P0.01),与透明度有极显著负相关性(P0.01),有毒微囊藻所占比例与叶绿素a、总氮、总磷和TSI有极显著正相关性(P0.01),与TN/TP和透明度有极显著负相关(P0.01).因此,削减洪泽湖总氮、总磷浓度一方面可以降低水体富营养化水平,另一方面有利于抑制有毒微囊藻对无毒微囊藻的竞争优势.     

无锡市饮用水嗅味突发事件致嗅原因及潜在问题分析

针对2007年5月底6月初发生的无锡市饮用水嗅味事件,在嗅味层次分析法(FPA)的基础上,利用感官气相色谱法对污染水团、取水口以及管网水中的致嗅物质种类进行了鉴定,并利用GC-MS对主要致嗅物质进行了定量分析,同时,对微囊藻毒素含量以及生物遗传毒性进行了测定.结果表明,此次嗅味事件的主要致嗅物质为以二甲基三硫为主的硫醚类有机体腐败产物,6月4日采集的污染水团中二甲基三硫含量高达11399 ng·L-1.同时,含有一定量的2-甲基异莰醇(MIB)等藻类分泌物,但这些物质的嗅味被二甲基三硫等硫醚类化合物导致的腥臭味所掩盖,不是主要的致嗅物质.另外,6月4日及6月8日采集的取水口样品分析结果表明,原水中微囊藻毒素含量远低于新颁布的生活饮用水卫生标准,而且,利用umu测试得到的水中遗传毒性水平很低.     

A flow cytometer based protocol for quantitative analysis of bloom-forming cyanobacteria (Microcystis) in lake sediments

A quantitative protocol for the rapid analysis of Microcystis cells and colonies in lake sediment was developed using a modified flow cytometer, the CytoSense. For cell enumeration, diluted sediment samples containing Microcystis were processed with sonication to disintegrate colonies into single cells. An optimized procedure suggested that 5 mg dw (dry weight)/mL dilution combined with 200 W × 2 min sonication yielded the highest counting efficiency. Under the optimized determination conditions, the quantification limit of this protocol was 3.3×10⁴ cells/g dw. For colony analysis, Microcystis were isolated from the sediment by filtration. Colony lengths measured by flow cytometry were similar to those measured by microscopy for the size range of one single cell to almost 400 μupm in length. Moreover, the relationship between colony size and cell number was determined for three Microcystis species, including Microcystis flos-aquae, M. aeruginosa and M. wessenbergii. Regression formulas were used to calculate the cell numbers in different-sized colonies. The developed protocol was applied to field sediment samples from Lake Taihu. The results indicated the potential and applicability of flow cytometry as a tool for the rapid analysis of benthic Microcystis. This study provided a new capability for the high frequency monitoring of benthic overwintering and population dynamics of this bloom-forming cyanobacterium.     

Upper Yellow River air concentrations of organochlorine pesticides estimated from tree bark, and their relationship with socioeconomic indices

Organochlorine pesticide(OCP) concentrations in tree bark from the upper Yellow River region were determined. Total OCP concentrations ranged from 2.7 to 82 ng/g dw, with a mean of 20 ng/g dw. Concentrations of total(Σ) DDTs(0.49–37 ng/g dw), HCHs(0.55–4.5 ng/g dw), and HCB(0.1–1.0 ng/g dw) were much higher than the other OCPs and accounted for 89% of the ΣOCP concentrations. p,p′-DDT was the dominant member of the DDT pesticide group and-HCH was the dominant HCH isomer. The p,p′-DDT/p,p′-DDE and-HCH/-HCH ratios suggested that there were recent DDT and-HCH releases. OCP concentrations in the air were estimated from the tree bark, and the estimated median ΣDDTs, ΣHCHs, and HCB concentrations in the air were 0.09, 0.14, and 0.024 pg/m3, respectively. The relationship between total OCP concentrations and socioeconomic and natural environment indices were assessed using multiple linear regression analysis, and a regression equation including all these factors was obtained. Population density and tertiary industry were the two dominant factors that appeared to affect OCP concentrations in the upper Yellow River region.     

Evolution of chemical composition of fogwater in winter in Chengdu, China

Two sampling sites representing the urban and suburban area of Chengdu, China were sampled and analyzed for selected chemicals to characterize the evolution of the chemical composition of fogwater. A trend of total organic carbon (TOC) > total nitrogen (TN) > total inorganic carbon (TIC) was observed for both sites. Variation of inorganic ions indicated that inorganic pollutants were not accumulated in the fog. Concentrations of n-alkanes (C11-C37) at the urban site ranged from 7.58 to 27.75 ng/mL while at the suburban site concentrations were 2.57-21.55 ng/mL. The highest concentration of n-alkanes was observed in the mature period of fog (393.12 ng/mL) which was more than ten times that in the fog formation period (27.83 ng/mL) and the fog dissipation period (14.87 ng/mL). Concentrations of Σ15PAHs were in the range of 7.27-38.52 ng/mL at the urban site and 2.59-22.69 ng/mL at the suburban site. Contents of PAHs in the mature period of fog (27.15 ng/mL) > fog dissipation period (11.59 ng/mL) > fog formation period (6.42 ng/mL). Concentrations of dicarboxylic acids (C5-C9) ranged from 10.92 to 40.78 ng/mL, with glutaric acid (C5) as the dominant dicarboxylic acid. These data provide strong indications of the accumulation of certain organic chemicals of environmental concern in fog and fog water, and provide additional insights about processes in urban and suburban air acting on organic chemicals with similar physical chemical properties.     

Irresistible bouquet of death—how are burying beetles (Coleoptera: Silphidae: Nicrophorus) attracted by carcasses

Chemical composition of volatiles emitted from fresh mouse carcasses (laboratory mice, Mus musculus) was studied using solid sample injection technique (solid-phase micro-extraction), two-dimensional gas chromatography with time of flight mass spectrometric detection and gas chromatography with electroantennographic detection. Electroantennography (EAG) and laboratory olfactometric behavioural observations were used to study the antennal sensitivity to identified infochemicals and their attractiveness for burying beetles Nicrophorus vespillo and Nicrophorus vespilloides (Silphidae: Nicrophorinae). Chemical analysis showed that immediately after death, emitted volatiles did not differ from those emitted by a living organism. However, in the course of time, sulphur-containing chemicals, specifically methanethiol, methyl thiolacetate, dimethyl sulphide, dimethyl disulphide and dimethyl trisulphide appear. EAG measurements revealed antennal sensitivity to these compounds. Behavioural tests in laboratory olfactometer showed that dimethyl sulphide, dimethyl disulphide and dimethyl trisulphide are highly attractive to both studied species. The data suggest that sulphur-containing chemicals are involved in mediating the fresh carcass attractiveness for N. vespillo and N. vespilloides.     

Identification of odorous compounds in reclaimed water using FPA combined with sensory GC-MS

Odorous compounds in the influent of a reclaimed water treatment plant (RWTP), consisting of coagulation, sedimentation, continuous micro-filtration (CMF), and chlorination in succession, in a north China city, were identified by combining flavor profile analysis (FPA) with sensory gas chromatograph-mass spectrometry (GC-MS). The sewery/swampy/septic odor with an odor intensity of 6.4 was found to be the major odor group in the RWTP influent, and the existence of well-known odorant including dimethyl disulfide, dimethyl trisulfide, indole and skatole were confirmed using GC-MS. The result of a spiking test showed that the intensity (3.6) of the sewery/swampy/septic odor caused by these four chemicals contributed to over 50% of the odor intensity of the influent. The FPA intensity for sewery/swampy/septic odor in the RWTP effluent was 3.8, showing that the treatment process was not efficient for the removal of odorants, particularly indole and skatole.     

Quantification of microcystin-producing and non-microcystin producing Microcystis populations during the 2009 and 2010 blooms in Lake Taihu using quantitative real-time PCR

Lake Taihu, a large, shallow hypertrophic freshwater lake in eastern China, has experienced lake-wide toxic cyanobacterial blooms annually during summer season in the past decades. Spatial changes in the abundance of hepatotoxin microcystin-producing and non-microcystin producing Microcystis populations were investigated in the lake in August of 2009 and 2010. To monitor the densities of the total Microcystis population and the potential microcystin-producing subpopulation, we used a quantitative real-time PCR assay targeting the phycocyanin intergenic spacer (PC-IGS) and the microcystin synthetase gene (mcyD), respectively. On the basis of quantification by real-time PCR analysis, the abundance of potential toxic Microcystis genotypes and the ratio of the mcyD subpopulation to the total Microcystis varied significantly, from 4.08× 10⁴ to 5.22× 10⁷ copies/mL, from 5.7% to 65.8%, respectively. Correlation analysis showed a strong positive relationship between chlorophyll-a, toxic Microcystis and total Microcystis; the abundance of toxic Microcystis correlated positively with total phosphorus and ortho-phosphate concentrations, but negatively with TN:TP ratio and nitrate concentrations. Meanwhile the proportion of potential toxic genotypes within Microcystis population showed positive correlation with total phosphorus and ortho-phosphate concentrations. Our data suggest that increased phosphorus loading may be a significant factor promoting the occurrence of toxic Microcystis bloom in Lake Taihu.     

Pollution level and distribution of PCDD/PCDF congeners between vapor phase and particulate phase in winter air of Dalian,China

In December 2009, ambient air was sampled with active high-volume air samplers at two sites: on the roof of the No. l building of Dalian Jiaotong University and on the roof of the building of Dalian Meteorological Observatory. The concentrations and the congeners between vapor phase and particulate phase of polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs) in the air were measured. Sample analysis results showed that the concentrations of PCDD/Fs in particulate phase was higher than that in gaseous phase. The ratio of PCDD to PCDF in gaseous phase and particulate phase was lower than 0.4 in all samples. The total I-TEQ value in gaseous phase and particulate phase was 5.5 and 453.8 fg/m³ at Dalian Jiaotong University, 16.6 and 462.1 fg/m³ at Dalian Meteorological Observatory, respectively. The I-TEQ value of Dalian atmosphere was 5.5-462.1 fg/m³ which was lower than international standard, the atmospheric quality in Dalian is better.     

Hydrophobic organic chemicals in urban fog

The concentrations and aqueous/particle distributions of three classes of hydrophobic organic chemicals, n-alkanes, polycyclic aromatic hydrocarbons (PAHs), and polychlorinated biphenyls (PCBs) were measured during the autumn of 1986's fog events in the urban area of Zürich, Switzerland. Concentrations of the chemicals in fog were in the range of 10–110 ng ml⁻¹ for n-alkanes (C₁₉–C₃₅), 6–60 ng ml⁻¹ for PAHs (21 compounds) and 7–22 ng ml⁻¹ for PCBs (31 congeners). In many samples, the concentration of individual n-alkanes and PAHs exceeded their water solubility, probably due to their association with dissolved and/or colloidal organic matter. All of the PAHs, except for phenanthrene, were measured as part of the particulate phase. Both the n-alkanes and PCBs showed a trend of increasing particle association with increasing hydrophobicity, but the trends were distinctly different. The presence of PCBs, PAHs, and n-alkanes at these concentrations suggest that fog is an excellent scavenger of hydrophobic organic chemicals. For a forested area near Zürich, Switzerland, it was estimated that the deposition of n-alkanes and PAHs by fog may be about equal to deposition via rain, but that fog may be 100 times more important than rain for the deposition of PCBs.     

Nutrients regeneration pathway, release potential, transformation pattern and algal utilization strategies jointly drove cyanobacterial growth and their succession

In order to better understand the contribution of nutrients regeneration pathway, release potential and transformation pattern to cyanobacterial growth and succession, 7 sampling sites in Lake Chaohu with different bloom degree were studied every two months from February to November 2018. The carbon, nitrogen (N) and phosphorus (P) forms or fractions in surface, interstitial water and sediments as well as extracellular enzymatic activities, P sorption, specific microbial abundance and community composition in sediments were analyzed. P regeneration pathway was dominated by iron-bound P desorption and phosphorus-solubilizing bacteria solubilization in severe-bloom and slight-bloom area respectively, which both resulted in high soluble reactive phosphorus (SRP) accumulation in interstitial water. However, in severe-bloom area, higher P release potential caused the strong P release and algal growth, compared to slight-bloom area. In spring, P limitation and N selective assimilation of Dolichospermum facilitated nitrate accumulation in surface water, which provided enough N source for the initiation of Microcystis bloom. In summer, the accumulated organic N in Dolichospermum cells during its bloom was re-mineralized as ammonium to replenish N source for the sustainable development of Microcystis bloom. Furthermore, SRP continuous release led to the replacement of Dolichospermum by Microcystis with the advantage of P quick utilization, transport and storage. Taken together, the succession from Dolichospermum to Microcystis was due to both the different forms of N and P in water column mediated by different regeneration and transformation pathways as well as release potential, and algal N and P utilization strategies.     

营养盐恢复对氮磷饥饿铜绿微囊藻生长的影响

在自然水体中微囊藻经常经历营养盐的限制和再补充,营养盐浓度的波动影响着微囊藻的生长和暴发.本文利用14C标记和荧光定量PCR研究了营养盐恢复对氮磷饥饿的铜绿微囊藻细胞生理和光合作用相关基因表达的影响.结果表明经过氮磷饥饿的铜绿微囊藻在补充营养盐后,都能快速生长,氮饥饿的藻细胞生长更快,但其经过快速增长期后很快开始衰亡.补充营养盐后,经过磷饥饿的藻细胞固碳能力和光合作用相关基因表达很快恢复至未经饥饿藻细胞的水平,而经过氮饥饿的藻细胞其固碳能力和相关基因虽然有很大提升,却难以恢复至未经饥饿的藻细胞的水平.这可能也是氮饥饿的藻细胞在饥饿解除后虽然能暂时地快速生长,但很快又进入衰亡的原因之一.