Interspecific protection against oxidative stress: green algae protect harmful cyanobacteria against hydrogen peroxide

Abstract

Summary Oceanographic studies have shown that heterotrophic bacteria can protect marine cyanobacteria against oxidative stress caused by hydrogen peroxide (H2O2). Could a similar interspecific protection play a role in freshwater ecosystems? In a series of laboratory experiments and two lake treatments, we demonstrate that freshwater cyanobacteria are sensitive to H2O2 but can be protected by less‐sensitive species such as green algae. Our laboratory results show that green algae degrade H2O2 much faster than cyanobacteria. Consequently, the cyanobacterium Microcystis was able to survive at higher H2O2 concentrations in mixtures with the green alga Chlorella than in monoculture. Interestingly, even the lysate of destructed Chlorella was capable to protect Microcystis, indicating a two‐component H2O2 degradation system in which Chlorella provided antioxidant enzymes and Microcystis the reductants. The level of interspecific protection provided to Microcystis depended on the density of Chlorella. These findings have implications for the mitigation of toxic cyanobacterial blooms, which threaten the water quality of many eutrophic lakes and reservoirs worldwide. In several lakes, H2O2 has been successfully applied to suppress cyanobacterial blooms. Our results demonstrate that high densities of green algae can interfere with these lake treatments, as they may rapidly degrade the added H2O2 and thereby protect the bloom‐forming cyanobacteria.

Cyanobacterial Harmful Algal Blooms in Aquatic Ecosystems: A Comprehensive Outlook on Current and Emerging Mitigation and Control Approaches

“…Oxidative stress is becoming a major approach to mitigate toxic blooms. In general, cyanobacteria are far more sensitive to oxidative stress, such as H 2 O 2 applications, than many eukaryotic phytoplankton [ 65 , 70 , 71 , 72 , 73 , 74 , 75 , 76 , 77 ], most likely because they display a lower ability to decompose H 2 O 2 than eukaryotic algae [ 78 , 79 ]. The evolutionary reasons for this observation are not clear but may be related to the fact that, in cyanobacteria, light-dependent O 2 uptake in the photosynthetic electron transport route is mediated via flavodiiron (known as FLV proteins) that release water [ 80 ].…”

“…Experiments where various H 2 O 2 concentrations were applied to assess the effective concentration showed the differential sensitivity of various toxic cyanobacteria to H 2 O 2 . Planktothrix showed the highest sensitivity, Microcystis was moderately sensitive, and Cylindrospermopsis was the most resistant [ 75 , 78 , 89 ]. Another set of experiments showed the following order of sensitivities: Pseudanabaena limnetica > Raphidiopsis curvata > Cylindrospermopsis raciborskii [ 77 ].…”

“…Another set of experiments showed the following order of sensitivities: Pseudanabaena limnetica > Raphidiopsis curvata > Cylindrospermopsis raciborskii [ 77 ]. Noticeably, the sensitivity to H 2 O 2 is strongly affected by biotic and abiotic conditions such as nutrient status [ 76 ], prior exposure to ROS [ 90 ], and the presence of other organisms that may possess a significant H 2 O 2 detoxification capability [ 78 ]. The cell density and phase of growth are also important biotic factors that affect sensitivity to H 2 O 2 applications [ 90 ].…”

Resilience of Microbial Communities after Hydrogen Peroxide Treatment of a Eutrophic Lake to Suppress Harmful Cyanobacterial Blooms

“…Addition of hydrogen peroxide (H 2 O 2 ) to lakes is a promising method for rapid mitigation of cyanobacterial blooms because cyanobacteria are more sensitive to low concentrations of H 2 O 2 than most eukaryotic organisms [ 19 , 20 , 21 , 22 , 23 , 24 , 25 , 26 ]. Furthermore, H 2 O 2 is a naturally occurring compound that degrades into water and oxygen, and hence, unlike other algicides, the added H 2 O 2 disappears within a few days [ 27 ].…”

“…In cyanobacteria, the transfer of excess electrons generated by photosynthesis is mediated by flavodiiron proteins which produce water without the formation of O 2 − or H 2 O 2 [ 30 , 31 ]. Accordingly, cyanobacteria produce less H 2 O 2 during photosynthesis, and hence they tend to be much less protected against H 2 O 2 than eukaryotic phytoplankton [ 25 , 27 ].…”