Cyanobacteria threat

Among the microbial hazards, toxic cyanobacteria (also known as blue-green algae) are said to be “of public health importance”. Cyanobacteria are photosynthetic bacteria, which play a key role in the life cycle: they are primary-producers, some of them can fix the atmospheric nitrogen, others form symbiotic relationships with other organisms (e.g. plant, fungi), etc. However, their proliferations can also be harmful for aquatic ecosystems. Indeed, when the nutrient levels increase, the cyanobacterial populations present in the water can grow very quickly and accumulate on the water surface forming scums. This phenomenon, known as algal bloom, has important economic, ecological and health consequences. It impacts on the aquatic biodiversity by limiting the access to light to the other photosynthetic organisms, by modifying the food web [3] , or by decreasing the concentration of oxygen leading to hypoxia or anoxia and consequently to fish kills [4] . Because of the production of odorous and/or toxic compounds (cyanotoxins), cyanobacterial blooms also affect the use of water bodies, in particular for the production of drinking water and for recreational activities such as bathing [4] .

A lot of large lakes all over the world are frequently experiencing cyanobacterial Harmful Algal Blooms (CyanoHABs) as it is the case of Lake Victoria (Africa), Lake Erie (USA-Canada), Lake Taihu (China) and in a lesser extent Lake Zurich (Switzerland) or Lake Bourget (France). But not only large lakes are concerned with this problem: smaller water bodies such as reservoirs, rivers, or estuaries also suffer from CyanoHABs whose frequency is increasing over the time [5] . This can be explained by several factors, among which the global warming and the eutrophication of water bodies [6], [7] . To reduce the potential risks for human populations, some threshold and guidelines values have been proposed by WHO for the most frequent cyanotoxins (microcystins).

Context in France

In France, in 1998, the ministries of health and environment have funded a program called EFFLOCYA, to assess the toxic risk associated with freshwater cyanobacteria in France. The study has shown that CyanoHABs are present all over the French territory and can be affecting any water body [8] . Since this pioneer study, lot of papers and reports have been published showing that many French freshwater ecosystems are disturbed by cyanobacterial blooms. For example, a study on 36 water bodies (used for recreational activities or as drinking water supply sources) of the west of France (Bretagne) revealed that 82% of these water bodies were affected by CyanoHABs during the summer time [8] . This alarming situation is of particular concern when the surface water is used as source for the drinking water, as it is the case of 37% of the water distributed in France (and >80% in some regions as Bretagne) [9] .

Following the European directives (Council directives 2000/60/EC and 2006/7/EC), the French High Council for Public Health (CSHPF) has published some recommendations for the monitoring and management of cyanobacterial proliferation in bathing waters (Notice of CSHPF of 6 May 2003). Since then, several circulars of the French General Directorate of Health (DGS/SD7A 2003-270, 2004/364, 2005/304) have been issued. The circular DGS/SD7A 2003-270 defines four alert levels depending on the concentration of cyanobacteria (cell.ml^-1), the concentration of microcystin-LR (µg.l^-1) and the presence or absence of scum and foam. Concerning the drinking water, the official limit values of several microbiological and chemical parameters of the water are given in the decree of 11 January 2007, related to the articles R.1321-2 and R.1321-3 of the French Code of Public Health (CSP). The maximal concentration of total microcystin (including the microcystin-LR) authorized is 1 µg.l^-1, which is the limit value fixed by WHO for the only microcystin-LR. In Bretagne, in 2011, the cyanobacteria concentration has exceeded the limit of 10⁶ cell.ml^-1 (alert level 2) in 58% of the 36 monitored water bodies [10] ; the recreational activities have been prohibited (alert level 4) or restricted (alert level 2-3) in 47% of the water bodies (53% in 2008, 41% in 2009, 30.5% in 2010). Finally, over the 179 analysis performed, 7% of the measured microcystin concentrations were greater than 1 µg.l^-1. No estimation of the financial costs generated by cyanobacterial blooms has been established in France. However, the implementation of monitoring programs, the restriction of the use of water bodies for consumption or recreational activities during the holidays, which has a great impact on tourism, and the improvements of water treatment plants for the production of drinking water from water contaminated by cyanobacteria are known to be very costly.

Context in China

In China, the government has established a classification for the quality of surface waters (Environmental Quality Standards for Surface Water; GB 3838-2002). There are five grades of pollution ranging from level I to V. Water areas of grade higher than grade IV (included) can be used neither for drinking water supply, nor for recreational activities with direct contact with the water. The Ministry of Environmental Protection (MEP) of China has evaluated (2011 State Of Environment report - SOE) that among the 26 major lakes and reservoirs under national monitoring program 11 lakes (42.3%) have a water quality of grade I to III, 13 (50.0%) a water quality of grade IV to V and 2 (7.7%) are over the limits of grade V. Finally, 53% of the lakes are eutrophic, the others being mesotrophic. The World Bank has estimated the cost of water scarcity related to pollution at 147 billion RMB [11] ,p93].

In the middle and lower reaches of the Yangtze River, which contain more than 60% of the total freshwater lakes in China, the situation is worse. Among the 50 lakes of this area studied in [12] , 37 (74%) have a water quality of grade higher than grade IV (included), and 21 (42%) are even above the limits of grade V. The water quality of Lake Taihu, the third largest freshwater lake of China, was averagely grade IV in the middle of the 1990s, with one third of the Lake at grade V [13] . The eutrophication of the lake has promoted cyanobacterial blooms, mainly composed of Microcystis spp. [14], [15] . The microcystin concentration of untreated water samples taken from Taihu has been measured during the summer 2010 [16] . Among the 34 samples, 15 (respectively 4) exceeded the guideline value for drinking water of 1 µg.l^-1 (respectively for recreational water of 20 µg.l^-1) recommended by WHO [2], [17] . It has also been shown that microcystins are still present in tap water after treatment [18] .

In May 2007, the proliferation of cyanobacteria in Lake Taihu resulted in a serious crisis of drinking water supply in Wuxi City, which has forced several millions of residents to drink bottled water during nearly a week. Sample analysis showed that the TN, TP, COD_Mn and Chlorophyll a concentrations were up to 10 times higher than usual [19] . The 2007 direct and indirect economic losses due to cyanobacterial blooms in Lake Taihu has been estimated at 2.88 and 5.2 billion RMB respectively [20] . Since the crisis of 2007, the control of cyanobacterial blooms in Lake Taihu has become a priority for local government.

Environmental context

The world population growth has led to the intensification of the industrialization, urbanization, and land exploitation, resulting in the production of huge amounts of pollutants. These pollutants are discharged into ecosystems like rivers and lakes often without treatment, leading to the nutrient over-enrichment of freshwaters. As an attempt to restore the water quality, some control strategies have been applied, most of which are based on the reduction of external nutrient loading (reduction of P only, or of P and N) which directly impacts the N/P ratio of the lakes. The evolution of this ratio depends on the countries. In France and Europe, the P concentrations tend to decrease in freshwater ecosystems when at the same time, N concentrations slightly increase or remain stable. In China, the opposite trend is observed concerning the evolution of N and P concentrations. In parallel, the atmospheric CO₂ level has increased from its preindustrial level of 280ppm to the current level (January 2016) of 402.59 ppm (database of NOAA Earth System Research Laboratory), which changes the carbonate equilibrium in water bodies [21] . Over the last century, the stoichiometric ratio C/N/P of freshwater bodies has therefore changed significantly [22] , and will certainly continue to change, considering the forecasts of population growth and climate. These changes may have significant impact on cyanobacteria population [23], [24] . For example, in Lake Bourget, a French deep perialpine lake, in spite of the nutrient load reduction applied during the 1970s and the early 1980s, the cyanobacterium Planktothrix rubescens has proliferated and has dominated the phytoplankton community from 1995 [25] . Despite their importance, the changes of C/N/P ratio have been poorly documented, which increases the uncertainty about the future evolution of lake ecosystems. For example, nobody knows if the currently applied control strategies will be still well-adapted to the future environmental conditions. Therefore, studying the impact of such environmental changes on the water ecosystem becomes a big challenge for lake management.