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Rapid adaptation of harmful cyanobacteria to rising CO2.

ABSTRACT: Rising atmospheric CO2 concentrations are likely to affect many ecosystems worldwide. However, to what extent elevated CO2 will induce evolutionary changes in photosynthetic organisms is still a major open question. Here, we show rapid microevolutionary adaptation of a harmful cyanobacterium to changes in inorganic carbon (Ci) availability. We studied the cyanobacterium Microcystis, a notorious genus that can develop toxic cyanobacterial blooms in many eutrophic lakes and reservoirs worldwide. Microcystis displays genetic variation in the Ci uptake systems BicA and SbtA, where BicA has a low affinity for bicarbonate but high flux rate, and SbtA has a high affinity but low flux rate. Our laboratory competition experiments show that bicA + sbtA genotypes were favored by natural selection at low CO2 levels, but were partially replaced by the bicA genotype at elevated CO2 Similarly, in a eutrophic lake, bicA + sbtA strains were dominant when Ci concentrations were depleted during a dense cyanobacterial bloom, but were replaced by strains with only the high-flux bicA gene when Ci concentrations increased later in the season. Hence, our results provide both laboratory and field evidence that increasing carbon concentrations induce rapid adaptive changes in the genotype composition of harmful cyanobacterial blooms.

SUBMITTER: Sandrini G

PROVIDER: S-EPMC4995953 | biostudies-literature | 2016 Aug

REPOSITORIES: biostudies-literature

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Rapid adaptation of harmful cyanobacteria to rising CO2.

Sandrini Giovanni G Ji Xing X Verspagen Jolanda M H JM Tann Robert P RP Slot Pieter C PC Luimstra Veerle M VM Schuurmans J Merijn JM Matthijs Hans C P HC Huisman Jef J

Proceedings of the National Academy of Sciences of the United States of America 20160801 33

Rising atmospheric CO2 concentrations are likely to affect many ecosystems worldwide. However, to what extent elevated CO2 will induce evolutionary changes in photosynthetic organisms is still a major open question. Here, we show rapid microevolutionary adaptation of a harmful cyanobacterium to changes in inorganic carbon (Ci) availability. We studied the cyanobacterium Microcystis, a notorious genus that can develop toxic cyanobacterial blooms in many eutrophic lakes and reservoirs worldwide. M ...[more]

PMID: 27482094

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Project description:Lake restoration practices based on reducing fish predation and promoting the dominance of large-bodied Daphnia grazers (i.e., biomanipulation) have been the focus of much debate due to inconsistent success in suppressing harmful cyanobacterial blooms. While most studies have explored effects of large-bodied Daphnia on cyanobacterial growth at the community level and/or on few dominant species, predictions of such restoration practices demand further understanding on taxa-specific responses in diverse cyanobacterial communities. In order to address these questions, we conducted three grazing experiments during summer in a eutrophic lake where the natural phytoplankton community was exposed to an increasing gradient in biomass of the large-bodied Daphnia magna. This allowed evaluating taxa-specific responses of cyanobacteria to Daphnia grazing throughout the growing season in a desired biomanipulation scenario with limited fish predation. Total cyanobacterial and phytoplankton biomasses responded negatively to Daphnia grazing both in early and late summer, regardless of different cyanobacterial densities. Large-bodied Daphnia were capable of suppressing the abundance of Aphanizomenon, Dolichospermum, Microcystis and Planktothrix bloom-forming cyanobacteria. However, the growth of the filamentous Dolichospermum crassum was positively affected by grazing during a period when this cyanobacterium dominated the community. The eutrophic lake was subjected to biomanipulation since 2005 and nineteen years of lake monitoring data (1996-2014) revealed that reducing fish predation increased the mean abundance (50%) and body-size (20%) of Daphnia, as well as suppressed the total amount of nutrients and the growth of the dominant cyanobacterial taxa, Microcystis and Planktothrix. Altogether our results suggest that lake restoration practices solely based on grazer control by large-bodied Daphnia can be effective, but may not be sufficient to control the overgrowth of all cyanobacterial diversity. Although controlling harmful cyanobacterial blooms should preferably include other measures, such as nutrient reductions, our experimental assessment of taxa-specific cyanobacterial responses to large-bodied Daphnia and long-term monitoring data highlights the potential of such biomanipulations to enhance the ecological and societal value of eutrophic water bodies.

Project description:Harmful algal blooms threaten the water quality of many eutrophic and hypertrophic lakes and cause severe ecological and economic damage worldwide. Dense blooms often deplete the dissolved CO2 concentration and raise pH. Yet, quantitative prediction of the feedbacks between phytoplankton growth, CO2 drawdown and the inorganic carbon chemistry of aquatic ecosystems has received surprisingly little attention. Here, we develop a mathematical model to predict dynamic changes in dissolved inorganic carbon (DIC), pH and alkalinity during phytoplankton bloom development. We tested the model in chemostat experiments with the freshwater cyanobacterium Microcystis aeruginosa at different CO2 levels. The experiments showed that dense blooms sequestered large amounts of atmospheric CO2, not only by their own biomass production but also by inducing a high pH and alkalinity that enhanced the capacity for DIC storage in the system. We used the model to explore how phytoplankton blooms of eutrophic waters will respond to rising CO2 levels. The model predicts that (1) dense phytoplankton blooms in low- and moderately alkaline waters can deplete the dissolved CO2 concentration to limiting levels and raise the pH over a relatively wide range of atmospheric CO2 conditions, (2) rising atmospheric CO2 levels will enhance phytoplankton blooms in low- and moderately alkaline waters with high nutrient loads, and (3) above some threshold, rising atmospheric CO2 will alleviate phytoplankton blooms from carbon limitation, resulting in less intense CO2 depletion and a lesser increase in pH. Sensitivity analysis indicated that the model predictions were qualitatively robust. Quantitatively, the predictions were sensitive to variation in lake depth, DIC input and CO2 gas transfer across the air-water interface, but relatively robust to variation in the carbon uptake mechanisms of phytoplankton. In total, these findings warn that rising CO2 levels may result in a marked intensification of phytoplankton blooms in eutrophic and hypertrophic waters.

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Rapid adaptation of harmful cyanobacteria to rising CO2.

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Rapid adaptation of harmful cyanobacteria to rising CO2.

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