The facilitating role of phycospheric heterotrophic bacteria in cyanobacterial phosphonate availability and Microcystis bloom maintenance.

BACKGROUND: Phosphonates are the main components in the global phosphorus redox cycle. Little is known about phosphonate metabolism in freshwater ecosystems, although rapid consumption of phosphonates has been observed frequently. Cyanobacteria are often the dominant primary producers in freshwaters; yet, only a few strains of cyanobacteria encode phosphonate-degrading (C-P lyase) gene clusters. The phycosphere is defined as the microenvironment in which extensive phytoplankton and heterotrophic bacteria interactions occur. It has been demonstrated that phytoplankton may recruit phycospheric bacteria based on their own needs. Therefore, the establishment of a phycospheric community rich in phosphonate-degrading-bacteria likely facilitates cyanobacterial proliferation, especially in waters with scarce phosphorus. We characterized the distribution of heterotrophic phosphonate-degrading bacteria in field Microcystis bloom samples and in laboratory cyanobacteria "phycospheres" by qPCR and metagenomic analyses. The role of phosphonate-degrading phycospheric bacteria in cyanobacterial proliferation was determined through coculturing of heterotrophic bacteria with an axenic Microcystis aeruginosa strain and by metatranscriptomic analysis using field Microcystis aggregate samples. RESULTS: Abundant bacteria that carry C-P lyase clusters were identified in plankton samples from freshwater Lakes Dianchi and Taihu during Microcystis bloom periods. Metagenomic analysis of 162 non-axenic laboratory strains of cyanobacteria (consortia cultures containing heterotrophic bacteria) showed that 20% (128/647) of high-quality bins from eighty of these consortia encode intact C-P lyase clusters, with an abundance ranging up to nearly 13%. Phycospheric bacterial phosphonate catabolism genes were expressed continually across bloom seasons, as demonstrated through metatranscriptomic analysis using sixteen field Microcystis aggregate samples. Coculturing experiments revealed that although Microcystis cultures did not catabolize methylphosphonate when axenic, they demonstrated sustained growth when cocultured with phosphonate-utilizing phycospheric bacteria in medium containing methylphosphonate as the sole source of phosphorus. CONCLUSIONS: The recruitment of heterotrophic phosphonate-degrading phycospheric bacteria by cyanobacteria is a hedge against phosphorus scarcity by facilitating phosphonate availability. Cyanobacterial consortia are likely primary contributors to aquatic phosphonate mineralization, thereby facilitating sustained cyanobacterial growth, and even bloom maintenance, in phosphate-deficient waters. Video Abstract.

The widespread capability of methylphosphonate utilization in filamentous cyanobacteria and its ecological significance.

Aquatic ecosystems comprise almost half of total global methane emissions. Recent evidence indicates that a few strains of cyanobacteria, the predominant primary producers in bodies of water, can produce methane under oxic conditions with methylphosphonate serving as substrate. In this work, we have screened the published 2 568 cyanobacterial genomes for genetic elements encoding phosphonate-metabolizing enzymes. We show that phosphonate degradation (phn) gene clusters are widely distributed in filamentous cyanobacteria, including several bloom-forming genera. Algal growth experiments revealed that methylphosphonate is an alternative phosphorous source for four of five tested strains carrying phn clusters, and can sustain cellular metabolic homeostasis of strains under phosphorus stress. Liberation of methane by cyanobacteria in the presence of methylphosphonate occurred mostly during the light period of a 12 h/12 h diurnal cycle and was suppressed in the presence of orthophosphate, features that are consistent with observations in natural aquatic systems under oxic conditions. The results presented here demonstrate a genetic basis for ubiquitous methane emission via cyanobacterial methylphosphonate mineralization, while contributing to the phosphorus redox cycle.

Species diversity and seasonal dynamics of filamentous cyanobacteria in urban reservoirs for drinking water supply in tropical China.

Filamentous cyanobacteria have been observed to become the dominant species in reservoirs, especially in small reservoirs for drinking water supply in southern China. The occurrences of filamentous cyanobacteria blooms in such reservoirs add additional costs for water plants by decreasing the filtration efficiency and the potential of toxin production. To serve the purpose of drinking water supply, the effective risk assessment requires the dynamic pattern of filamentous cyanobacteria. This study seasonally collected samples from 25 reservoirs in Dongguan, one of the most important 'world factories' in China in July, December and March, and investigated the temporal dynamics of phytoplankton, particularly cyanobacteria community. Our investigation showed that filamentous cyanobacteria, Planktothrix sp, Limnothrix sp. and Cylindrospermopsis raciborskii dominated in these reservoirs and climate-related water temperature was the primary factor for the seasonal shift of filamentous cyanobacteria. High abundance of filamentous cyanobacteria occurred in the high water level period with increasing temperature but less relevant with nutrient conditions. Our study observed the seasonal dynamics of filamentous cyanobacteria in tropical urban reservoirs and highlighted the association between temperature and filamentous cyanobacteria. our data and analysis provided an evidence that increased temperature could increase the likelihood of frequency and intensity of filamentous cyanobacteria blooms. In the scenario of global warming, more frequent monitoring of filamentous cyanobacteria and the potential to produce toxin should be considered for water quality and reservoir management.

Total phosphorus-precipitation and Chlorophyll a-phosphorus relationships of lakes and reservoirs mediated by soil iron at regional scale.

Phosphorus is a critical element determining trophic status and Chlorophyll a (Chl a) level in natural lakes and reservoirs, and total phosphorus (TP) concentrations can be predicted from data on phosphorus loading, hydraulic flushing rate and sedimentation. Due to their interactions with phosphorus, iron (hydr) oxides in suspended particles, originally derived from watershed soil, can strongly influence the phosphorus sedimentation and phosphorus bioavailability in water columns. Thus, the TP-precipitation relationship and the response of Chl a to TP are likely associated with watersheds soil iron. To test this assumption, we built hierarchical linear models for summer observation of natural lakes and reservoirs across a large geographic gradient. The intercepts and slopes of TP-precipitation relationships are higher in natural lakes than those in reservoirs, and these model coefficients exhibit latitudinal variations that are explained by the natural soil iron gradient. Soil iron, operating at a regional level, significantly mediates the effect of precipitation on TP concentration in both natural lakes and reservoirs, and drives the latitudinal variation in the Chl a-TP relationships for reservoirs. Our results imply that the increase in extreme precipitation events anticipated under future climate conditions may substantially mitigate eutrophication in tropical and subtropical reservoirs, but may worsen conditions in temperate lakes.

[Distribution and Factors Affecting Cylindrospermopsis raciborskii in Guangdong Reservoirs].

Cylindrospermopsis raciborskii originating from tropical and subtropical regions is potentially toxic and attracts much attention due to its extension to the global temperate zone in recent years. Based on historical data of 20 reservoirs with different trophic levels (dry season, wet season, and transitional season of 2010), this study focuses on the analysis of the occurrence and distribution of C. raciborskii in the Guangdong Province. Based on the results, C. raciborskii was found in 19 of the 20 reservoirs and its biomass ranges from 0.0001-39.740 mg·L-1 and accounts for 0.02%-97.07% of the total phytoplankton biomass. Both a notable spatial and seasonal distribution of C. raciborskii were observed. Its occurrence is higher in the western coastal area (77.78%) than in the Zhujiang Delta (66.67%) and northern coastal area (33.33%) and is relatively lower in the dry season (40%) compared with the rainy season (70%) and transition season (85%). The trophic level has a significant effect on the presence of C. raciborskii, which is notably higher in eutrophic reservoirs (81.48%) than in mesotrophic reservoirs (66.67%) and oligotrophic reservoirs (33.33%). The redundancy analysis shows that C. raciborskii biomass is positively correlated with total nitrogen (TN) and the trophic state index (TSI) and negatively correlated with dissolved inorganic nitrogen (DIN), soluble reactive phosphorus (SRP), and the secchi depth (SD). Thus, C. raciborskii in Guangdong reservoirs may be promoted by environmental factors such as high nitrogen contents, low phosphorus concentration, and transparency.

[Distribution and pollution characteristics of nutrients and heavy metals in sediments of Hedi Reservoir].

Core sediments were collected from the riverine, transition and lacustrine zones of Hedi Reservoir in southern China to investigate the spatial distributions of nutrients and heavy metals and assess the potential ecological risk of heavy metals. The total nitrogen (TN) contents of the sediments at three sampling sites are between 2.314-2.427 mg x g(-1), while total phosphorus (TP) contents range from 0.591 mg x g(-1) to 0.760 mg x g(-1), TN contents of the surface sediments increase from the riverine zone to the lacustrine zone, but the TP content in the transition zone is higher than that in the other two sites (riverine zone and lacustrine zone). The mean contents of heavy metals are: 31.094, 46.85, 75.615, 385.739, 0.624 and 0.171 mg x kg(-1) respectively, except Cr, the contents of heavy metals in sediment of lacustrine zone are higher than the sediment of transition zone. In all core sediments, the contents of nutrients and heavy metals decrease from the surface to the bottom of core sediments. Inorganic phosphorus (IP) is the dominant fraction of phosphorus in the sediment and the NaOH-P is the main forms of inorganic phosphorus. The potential ecological risk assessed by using of the highest environmental background values before industrialization as the reference indicates that each single heavy metal only causes slightly pollution, but two heavy metals (Cd and Hg) cause heavy pollution based on the soil environmental background values of Guangdong province. In spite of the slight difference between two kinds of risk assessment, all demonstrated that Cd and Hg resulted in more serious pollution than the other metals and these two metals contributed most to the RI values.

Effects of local climate and hydrological conditions on the thermal regime of a reservoir at Tropic of Cancer, in southern China.

Thermal regime is strongly associated with hydrodynamics in water, and it plays an important role in the dynamics of water quality and ecosystem succession of stratified reservoirs. Changes in both climate and hydrological conditions can modify thermal regimes. Liuxihe Reservoir (23°45'50″N; 113°46'52″E) is a large, stratified and deep reservoir in Guangdong Province, located at the Tropic of Cancer of southern China. The reservoir is a warm monomictic water body with a long period of summer stratification and a short period of mixing in winter. The vertical distribution of suspended particulate material and nutrients are influenced strongly by the thermal structure and the associated flow fields. The hypolimnion becomes anoxic in the stratified period, increasing the release of nutrients from the bottom sediments. Fifty-one years of climate and reservoir operational observations are used here to show the marked changes in local climate and reservoir operational schemes. The data show increasing air temperature and more violent oscillations in inflow volumes in the last decade, while the inter-annual water level fluctuations tend to be more moderate. To quantify the effects of changes in climate and hydrological conditions on thermal structure, we used a numerical simulation model to create scenarios incorporating different air temperatures, inflow volumes, and water levels. The simulations indicate that water column stability, the duration of the mixing period, and surface and outflow temperatures are influenced by both natural factors and by anthropogenic factors such as climate change and reservoir operation schemes. Under continuous warming and more stable storage in recent years, the simulations indicate greater water column stability and increased duration of stratification, while irregular large discharge events may reduce stability and lead to early mixing in autumn. Our results strongly suggest that more attention should be focused on water quality in years of extreme climate variation and hydrological conditions, and selective withdrawal of deep water may provide an efficient means to reduce internal loading in warm years.