
Light-dominated selection shaping filamentous cyanobacterial assemblages drives odor problem in a drinking water reservoir
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Filamentous cyanobacteria have substantial niche overlap, and the causal mechanism behind their succession remains unclear. This has practical significance since several filamentous genera
are the main producers of the musty odorant 2-methylisoborneol (MIB), which lead to odor problems in drinking water. This study investigates the relationships between two filamentous
cyanobacteria, the MIB-producing genus Planktothrix and the non-MIB-producing genus Pseudanabaena, in a drinking water reservoir. We firstly identified their niche characteristics based on a
monitoring dataset, combined this information with culture experiments and developed a niche-based model to clarify these processes. The results reveal that the optimal light requirements
of Pseudanabaena (1.56 mol m−2 d−1) are lower than those of Planktothrix (3.67 mol m−2 d−1); their light niche differentiation led to a fundamental replacement of Planktothrix (2013) by
Pseudanabaena (2015) along with MIB decreases in this reservoir during 2013 and 2015. This study suggests that light is a major driving force responsible for the succession between
filamentous cyanobacteria, and that subtle niche differentiation may play an important role in shaping the filamentous cyanobacterial assemblages that drives the MIB odor problems in
drinking water reservoirs.
Odor problems in source water caused by 2-methylisoborneol (MIB), a secondary metabolite of filamentous cyanobacteria in many reservoirs and lakes1, have been a common issue in the Northern
Hemisphere, and have now been moving southward2,3,4,5,6,7. The major MIB producers include Oscillatoria8,9,10, Planktothrix11, Phormidium10, Pseudanabaena12, Lyngbya13 and
Planktothricoides14. It should be noted that MIB yield varies among different strains11,15,16,17, and some strains of the known MIB-producing species are in some cases not even able to
produce MIB8,13,18. Nonetheless, MIB occurrences and concentrations are mainly determined by the presence and abundance of MIB-producing filamentous cyanobacteria in the aquatic environment.
Nutrients, water temperature and light are essential factors governing the growth and competition of phytoplankton. Recent studies have emphasized the importance of underwater light
condition on their seasonal successions in both field investigations19,20 and numeric models21,22,23. The cellular projected area (CPA, the two-dimensional area measurement by projecting
cell shape on to a plane, as defined in22) has been proposed as a key indicator of cellular light harvesting potential, and the specific CPA (CPA/V, normalized CPA by cell volume) could be
used to indicate the optimum light requirements for various species with different cell shapes22,24. For example, the bloom-forming cyanobacteria Microcystis with a low specific CPA requires
high light intensity and hence is usually observed in surface water, particularly in the summer period, while filamentous cyanobacteria having a higher specific CPA tend to live in
subsurface layers, where light intensity is usually low, but nutrient availability is high25. The low-irradiance-tolerating characteristics of filamentous cyanobacteria have been verified by
laboratory culture experiments26 and field investigation27. The light niche differentiation between filamentous cyanobacteria and other phytoplankton enables us to model their succession
based on ecological niche modeling25,28,29,30. However, little is known about the competition between different filamentous cyanobacterial genera, since they are likely to have substantial
niche overlap. Therefore, it is desirable to know whether the changes in composition of filamentous cyanobacterial assemblages are deterministic (governed by niche differentiation) or
stochastic (dominated by neutral theory).
QCS Reservoir is a newly constructed estuary reservoir used as the major drinking water resource for Shanghai, China. It directly imports highly turbid water from the Yangtze River, leading
to underwater light conditions that favors filamentous cyanobacteria rather than Microcystis7, and therefore has suffered from MIB odor problems since it was put into use in 2011. The
filamentous cyanobacterium Planktothrix was the main MIB producer according to our previous study7. From 2011 to 2015, MIB concentrations showed a decreasing pattern along with the decrease
of Planktothrix cell densities and the increase of another filamentous cyanobacterium, Pseudanabaena. We therefore hypothesize that their competition and succession might have great impact
on MIB occurrence in this reservoir. The aim of this study is to identify the driving forces responsible for the filamentous cyanobacterial assemblages, so that it can provide scientific
basis to solve the practical MIB problem in drinking water reservoirs. Accordingly, we identified their niche characteristics based on a monitoring dataset together with culture experiments,
and developed a niche-based model to clarify these ecological processes.
MIB concentration of the river water (inlet) was rather low during the investigation (Supplementary Fig. 1). Significant seasonal variation of MIB was observed in QCS Reservoir (Fig. 1b);
higher MIB concentrations (mean: 49.2 ng L−1, range: 0.5–97.8 ng L−1) were mainly observed during the period June to September (mean: 7.5 ng L−1, range: 0.5–12.3 ng L−1). The long-term
development of MIB in June to September between 2011 and 2015 exhibited a significant decrease (Fig. 1c). The mean concentrations in the first year were 101.0 ng L−1 (range: 0.5–257.0 ng
L−1), equivalent to 6 times its human olfactory threshold (15 ng L−1,11), and thus aroused great attention. However, in the following 2 years the mean MIB concentrations decreased to 34.2 ng
L−1 (range: 0.5–107.0 ng L−1) and 29.4 ng L−1 (range: 0.5–66.4 ng L−1), respectively. In 2014 and 2015, the concentrations further decreased to 6.2 ng L−1 (range: 0.5–15.6 ng L−1).
a Sampling sites in QCS Reservoir. b Seasonal dynamics of MIB concentration from 2011 to 2015. c Annual dynamics of MIB concentration in July to September from 2011 to 2015.
Four main filamentous cyanobacteria were recorded during the investigation in QCS Reservoir (Supplementary Fig. 2); Planktothrix (30.2%) and Pseudanabaena (30.5%) exhibited higher occurrence
frequencies than Phormidium (14.9%) and Lyngbya (2.5%). Lyngbya was only observed for eight samples, so it was not possible to identify the seasonality. Planktothrix (n = 175),
Pseudanabaena (n = 168) and Phormidium (n = 88) were mainly observed during May to October (Supplementary Fig. 3). Planktothrix was identified as the MIB producer in QCS Reservoir according
to our previous study7. Microcystis dominated during August and September, which could affect the growth of filamentous cyanobacteria (Supplementary Fig. 3). Therefore, Pseudanabaena was
considered as the most important competitor to Planktothrix based on their seasonal distribution patterns (Supplementary Fig. 3) and their habitats.
20.5% of the variances of Planktothrix cell density could be explained by seasonal and long-term trend terms using the GAM model (Eq. (4), Supplementary Table 7, Supplementary Fig. 5). The
model suggested that the variance of Planktothrix was dominated by strong seasonality (p