Experiment design and bacterial abundance control extracellular H2O2 concentrations during four series of mesocosm experiments
Open Access
- 16 March 2020
- journal article
- research article
- Published by Copernicus GmbH in Biogeosciences (online)
- Vol. 17 (5), 1309-1326
- https://doi.org/10.5194/bg-17-1309-2020
Abstract
The extracellular concentration of H2O2 in surface aquatic environments is controlled by a balance between photochemical production and the microbial synthesis of catalase and peroxidase enzymes to remove H2O2 from solution. In any kind of incubation experiment, the formation rates and equilibrium concentrations of reactive oxygen species (ROSs) such as H2O2 may be sensitive to both the experiment design, particularly to the regulation of incident light, and the abundance of different microbial groups, as both cellular H2O2 production and catalase-peroxidase enzyme production rates differ between species. Whilst there are extensive measurements of photochemical H2O2 formation rates and the distribution of H2O2 in the marine environment, it is poorly constrained how different microbial groups affect extracellular H2O2 concentrations, how comparable extracellular H2O2 concentrations within large-scale incubation experiments are to those observed in the surface-mixed layer, and to what extent a mismatch with environmentally relevant concentrations of ROS in incubations could influence biological processes differently to what would be observed in nature. Here we show that both experiment design and bacterial abundance consistently exert control on extracellular H2O2 concentrations across a range of incubation experiments in diverse marine environments. During four large-scale (> 1000 L) mesocosm experiments (in Gran Canaria, the Mediterranean, Patagonia and Svalbard) most experimental factors appeared to exert only minor, or no, direct effect on H2O2 concentrations. For example, in three of four experiments where pH was manipulated to 0.4-0.5 below ambient pH, no significant change was evident in extracellular H2O2 concentrations relative to controls. An influence was sometimes inferred from zooplankton density, but not consistently between different incubation experiments, and no change in H2O2 was evident in controlled experiments using different densities of the copepod Calanus finmarchicus grazing on the diatom Skeletonema costatum (< 1% change in [H2O2] comparing copepod densities from 1 to 10 L-1). Instead, the changes in H2O2 concentration contrasting high- and low-zooplankton incubations appeared to arise from the resulting changes in bacterial activity. The correlation between bacterial abundance and extracellular H2O2 was stronger in some incubations than others (R-2 range 0.09 to 0.55), yet high bacterial densities were consistently associated with low H2O2. Nonetheless, the main control on H2O2 concentrations during incubation experiments relative to those in ambient, unenclosed waters was the regulation of incident light. In an open (lidless) mesocosm experiment in Gran Canaria, H2O2 was persistently elevated (2-6-fold) above ambient concentrations; whereas using closed high-density polyethylene mesocosms in Crete, Svalbard and Patagonia H2O2 within incubations was always reduced (median 10 %-90 %) relative to ambient waters.Funding Information
- Horizon 2020 Framework Programme (603773)
This publication has 49 references indexed in Scilit:
- Haemolytic activity and reactive oxygen species production of four harmful algal bloom speciesEuropean Journal of Phycology, 2017
- Major Effect of Hydrogen Peroxide on Bacterioplankton Metabolism in the Northeast AtlanticPLOS ONE, 2013
- The influence of solar ultraviolet radiation on the photochemical production of H2O2 in the equatorial Atlantic OceanJournal of Sea Research, 2004
- Recovery of Hydrogen Peroxide-Sensitive Culturable Cells of Vibrio vulnificus Gives the Appearance of Resuscitation from a Viable but Nonculturable StateJournal of Bacteriology, 2000
- Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communitiesScientia Marina, 2000
- Catalase activity in macro- and microorganisms as an indicator of biotic stress in coastal waters of the eastern Mediterranean SeaHelgoland Marine Research, 1999
- Photochemically produced carboxylic acids as substrates for freshwater bacterioplankton>Limnology and Oceanography, 1998
- Factors Affecting the Distribution of H2O2 in Surface WatersPublished by American Chemical Society (ACS) ,1994
- Spectrophotometric seawater pH measurements: total hydrogen ion concentration scale calibration of m-cresol purple and at-sea resultsDeep Sea Research Part I: Oceanographic Research Papers, 1993
- Photochemical formation of hydrogen peroxide in natural waters exposed to sunlightEnvironmental Science & Technology, 1988