Responses of leaf-associated biofilms on the submerged macrophyte Vallisneria natans during harmful algal blooms☆
Graphical abstract
Introduction
Harmful algal blooms (HABs) are considered to be caused by eutrophication of waterbodies (Heisler et al., 2008). However, recent studies indicated that it was not guaranteed that eutrophic waterbodies would experience HABs (Scheffer, 1990). For example, two typical zones exist within Lake Taihu, the largest eutrophic lake in China, namely East Lake Taihu and Meiliang Bay. These zones have similar physical characteristics and exogenous pollution, as well as shared meteorological and climatological conditions; however, East Lake Taihu and Meiliang Bay could be categorized into alternative stable states: the grass-stable state (clear state) and the algae-stable state (turbid state) (Guan et al., 2018; Wu et al., 2010). Highly eutrophic water could also remain clear in cases where a dense and diverse submerged macrophyte community utilizes the available nutrients. Thus, the allelopathic effects of submerged macrophytes and phytoplankton is of great significance when determining the mechanisms governing these two stable states, and for controlling HABs.
Previous work has mainly focused on the allelopathic effects of submerged macrophytes on the phytoplankton community, as well as on how allelopathy could be utilized to remove algae from freshwater (Chang et al., 2012; Eigemann, 2013; Gross et al., 2007; Pan et al., 2011; Sun et al., 2014; Z. B. et al., 2009; Zhu et al., 2010). However, the effects of phytoplankton on submerged macrophytes and the growth status of these plants in eutrophic and algae-stable freshwater systems remain unclear.
The leaves of submerged macrophytes provided large attachment areas for bacteria, algae and other microorganisms, thereby allowing biofilm formation (Michael et al., 2008). Submerged macrophyte biofilms played an important role in allelopathy between the macrophytes and algae or other phytoplankton. Biofilm microorganisms could compete with their hosts (the submerged macrophytes) for nutrients in the water column (Jones et al., 2002). In addition, excessive biofilms on the macrophyte leaves could lead to physical barriers that reduced the efficiency for nutrient uptake, gas exchange and light utilization (Drake et al., 2003; Hill and Dimick, 2002). Moreover, the presence of epiphytic algae in the biofilms could lead to a high pH; a highly oxygenated microenvironment on the surface of the leaves; and direct induction of oxidative stress on submerged macrophytes (Song et al., 2015). Thus, changes of leaf-associated biofilms need to be further investigated as they related to eutrophic and algae-stable freshwater environments.
The present work examined the responses of leaf-associated biofilms on submerged macrophytes in freshwater systems by simulating clear and turbid eutrophic states. Microcystis aeruginosa (M. aeruginosa), one of the most harmful freshwater bloom-forming cyanobacteria (Black et al., 2011; Yamaguchi et al., 2015), was selected to simulate an algae-stable state (turbid) waterbody. Vallisneria natans (V. natans) was selected as the model macrophyte for the simulated eutrophic waterbody because its growth and survival potential in eutrophic freshwater is superior to other submerged macrophytes (Qiu et al., 2001; Yan et al., 1995). The objective of this study was to elucidate the responses of leaf-associated biofilms during an algal bloom by (1) determining the photosynthetic rates and extent of oxidative damage to V. natans leaves during HABs; and (2) assessing and comparing the bacterial communities of V. natans leaf-associated biofilms. The results will have important implications for better understanding the role of leaf-associated biofilms during shifts between the grass-stable state and the algae-stable state while providing useful information for controlling the formation of HABs in eutrophic freshwater systems.
Section snippets
M. aeruginosa and V. natans cultivation
M. aeruginosa (M.A., FACHB-912), isolated from algal blooms in Lake Taihu, was obtained from the Freshwater Algae Culture Collection at the Institute of Hydrobiology at the Chinese Academy of Sciences (FACHB, Wuhan City, China). Cultures were grown in 1000-mL Erlenmeyer flasks containing 250 mL of BG11 medium (Rippka et al., 1979). Conditions were controlled at 28 ± 2 °C and 70%–90% relative humidity under a 12:12 h light-dark cycle as facilitated by an 80 μmol quanta m−2 s−1 light, which was
Growth status of V. natans
In general, HABs negatively affected V. natans growth, especially in the SP group (p < 0.01, Fig. 2). Allelochemicals of M. aeruginosa had significant negative effects on V. natans fresh weight, which was reduced from an average of 1.9 g on day 0–1.4 g on day 12, and shoot length, which was reduced from an average of 17 cm on day 0–10.8 cm on day 12. However, the allelopathic effects on V. natans were not significant in the MT group. In the mixed system, the allelopathic effects of V. natans on
Conclusion
The response of V. natans leaf-associated biofilms during HABs was investigated. Results indicated that a mixed-culture of V. natans and M. aeruginosa promoted leaf biomass but decreased the bacterial abundance of biofilms on the surface of V. natans leaves. Algal blooms induced inhibition of photosynthesis, oxidative stress and the antioxidant system stress response in V. natan leaf-associated biofilms. The surface topography of V. natans leaves was also altered during the algal bloom. The
Acknowledgements
The study was supported by the National Science Foundation of China (51308127) and the Major Science and Technology Program for Water Pollution Control and Treatment (2012ZX07103-004).
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This paper has been recommended for acceptance by Dr. Sarah Harmon.