Atmospheric CO2 Availability Induces Varying Responses in Net
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Aquatic Sciences (2021) 83:33 https://doi.org/10.1007/s00027-021-00788-6 Aquatic Sciences RESEARCH ARTICLE Atmospheric CO2 availability induces varying responses in net photosynthesis, toxin production and N2 fxation rates in heterocystous flamentous Cyanobacteria (Nostoc and Nodularia) Nicola Wannicke1 · Achim Herrmann2 · Michelle M. Gehringer2 Received: 21 April 2020 / Accepted: 3 February 2021 © The Author(s) 2021 Abstract Heterocystous Cyanobacteria of the genus Nodularia form major blooms in brackish waters, while terrestrial Nostoc species occur worldwide, often associated in biological soil crusts. Both genera, by virtue of their ability to fx N2 and conduct oxy- genic photosynthesis, contribute signifcantly to global primary productivity. Select Nostoc and Nodularia species produce the hepatotoxin nodularin and whether its production will change under climate change conditions needs to be assessed. In light of this, the efects of elevated atmospheric CO2 availability on growth, carbon and N2 fxation as well as nodularin production were investigated in toxin and non-toxin producing species of both genera. Results highlighted the following: • Biomass and volume specifc biological nitrogen fxa- • Elevated atmospheric CO 2 levels were correlated to a tion (BNF) rates were respectively almost six and 17 fold reduction in biomass specifc BNF rates in non-toxic higher in the aquatic Nodularia species compared to the Nodularia species. terrestrial Nostoc species tested, under elevated CO 2 con- • Nodularin producers exhibited stronger stimulation of ditions. net photosynthesis rates (NP) and growth (more positive • There was a direct correlation between elevated CO 2 and Cohen’s d) and less stimulation of dark respiration and decreased dry weight specifc cellular nodularin content BNF per volume compared to non-nodularin producers in a diazotrophically grown terrestrial Nostoc species, under elevated CO2 levels. and the aquatic Nodularia species, regardless of nitrogen availability. This study is the frst to provide information on NP and nodularin production under elevated atmospheric CO2 levels for Nodularia and Nostoc species under nitrogen replete and diazotrophic conditions. Keywords Climate change · Nitrogen fxation · Nodularia · Nodularin · Nostoc · Photosynthesis Abbreviations PON Particulate organic nitrogen BNF Biological nitrogen fxation NP Nett photosynthesis HC High CO2 (2000 ppm) NPP Net primary production LC Low CO2 (~ 440 ppm) CCM Carbon concentrating mechanism POC Particulate organic carbon * Introduction Michelle M. Gehringer [email protected]; [email protected] 1 Cyanobacteria, in their role as primary producers, form an Research Group Plasma-Agriculture, Leibniz Institute essential part of the global C and N cycles, both in terrestrial for Plasma Science and Technology, Felix‐Hausdorf‐Str. 2, 17489 Greifswald, Germany and aquatic environments (Visser et al. 2016; Elbert et al. 2012). The process of oxygenic photosynthesis, whereby 2 Department of Microbiology, Technical University of Kaiserslautern, Paul-Ehrlich Straße, 67653 Kaiserslautern, energy from the sun is used to reduce inorganic carbon Germany with the accompanying oxidation of water, is thought to Vol.:(0123456789)1 3 33 Page 2 of 17 N. Wannicke et al. have evolved during the Archean era when there was no dissolves in the oceans, reducing the pH by increasing the free oxygen in the Earth’s atmosphere (Lyons et al. 2014). partial pressure of CO2, accompanied by a smaller rela- − 2− The enzyme catalysing CO 2 fxation in Cyanobacteria and tive increase in HCO 3 and a decrease in CO 3 (Sabine modern-day C3 plants is ribulose-1,5-bisphosphate carbox- et al. 2004; Raven et al. 2017). Although the speciation of ylase/oxygenase (Rubisco), thought to be the most abun- dissolved inorganic carbon is directly linked to pH, how dant enzyme on Earth. Rubisco binds CO2 and generates 2 changes in their balance affects Cyanobacterial bloom molecules of 3-phosphoglycerate (3PGA) which is further occurrence and toxicity is unclear (Raven et al. 2020). processed in the Calvin-Benson-Bassham (CBB) cycle to The increase in growth rate observed for the marine, non- produce ribulose-1,5-biphosphate and glutamate. In order heterocystous, flamentous diazotrophic Cyanobacterium, to reduce undesirable oxygenase activity, Cyanobacteria Trichodesmium, grown at 900 ppm CO2 was ascribed to have evolved the carbon concentrating mechanism (CCM) down regulation of the CCM, thereby reducing the energy to increase the efective concentration of CO 2 around the demands on the cell (Kranz et al. 2011). Under Fe- limiting Rubisco active site by up to 1000-fold (Price 2011). CO2 dif- conditions, decreasing the medium pH reduced N 2 fxation fuses freely into the cell and is converted to bicarbonate in an rates in Trichodesmium, with the reduced N2 fxation rates NADPH-dependent reaction. Most Cyanobacteria sequenced corresponding to reduced nitrogenase efciency at lower to date carry the high fux, low afnity CO2 converting pH (Kranz et al. 2011). Exposing cultures of the freshwater − enzyme, NDH-I4, as well as the low fux, high afnity NDH- diazotroph, Nostoc muscorum, to raised HCO 3 concentra- I3 variant. Uptake of bicarbonate from the surrounding liquid tions under diazotrophic conditions resulted in enhanced requires an investment in energy and the synthesis of spe- growth, O2 and pigment production and nitrogenase activi- cifc transporters. Two sodium –dependent symporters, BicA ties (Bhargava et al. 2013). The brackish diazotroph, Nodu- (high fux, low afnity) and SbtA (low fux, high afnity) laria spumigena sp. KAC12, when grown at elevated CO2 bicarbonate transporters occur occasionally together with of 960 ppm, demonstrated increased photochemical yield the BCT1 high afnity low fux transporter, found in almost after 5 days exposure (Karlberg and Wulf 2013), suggest- all Cyanobacteria investigated to date on the cell membrane ing higher potential net primary productivity rates. Nodu- (Burnap et al. 2015; Visser et al. 2016). The presence of laria spumigena CCY9414, grown under elevated CO2 BicA provides aquatic Cyanobacterial species a growth conditions (548 ppm), exhibited increased C fxation rates − advantage under elevated levels of HCO3 availability (San- compared to control cultures, with increased carbon to nitro- drini et al. 2014). Oxygenic photosynthetic organisms that gen (POC:PON) and nitrogen to phosphate ratios recorded rely on the construction of a carbon concentrating mecha- (Wannicke et al. 2012). Only a slight increase was observed nism (CCM) are thought to be sensitive to changes in pCO2 in the C:N ratios in three Cyanobacterial cultures grown (e.g. Raven et al. 1991; Rost et al. 2003; Price 2011; Shi at elevated CO 2 (~ 900 ppm) in continuous culture in bub- et al. 2012; Raven et al. 2017). The plasticity of the CCM to ble reactors, namely Cyanothece sp. ATCC51142, Nodu- elevated levels of atmospheric CO2 was found to be high in laria spumigena IOW-2000/1 and Calothrix rhizosoleniae Cyanobacteria when compared to the more recently evolved sp. SC01 (Eichner et al. 2014). This study emphasised the haplophytes and diatoms (Van de Waal et al. 2019). This need to generate more data on the efects of elevated CO2 phenotypic plasticity in carbon fxation was demonstrated on levels on Cyanobacterial BNF, and highlighted the diver- Microcystis grown under conditions of elevated CO2 (Ji et al. sity in observed responses of marine Cyanobacterial species 2020). The maximum CO 2 uptake rate of Microcystis grown to elevated atmospheric CO 2. Wannicke et al. (2018b), in at 1000 ppm CO 2 was increased 1.5–1.8 times compared to their metadata study, found indications that ocean acidif- the low CO 2 control cultures, suggesting that elevated CO 2 cation would beneft BNF in the future ocean. They also conditions may stimulate Cyanobacterial bloom growth (Ji drew attention to the fact that these studies were mostly con- et al. 2020). Furthermore, by reducing the levels of dissolved ducted on only two species, the flamentous Trichodesmium CO2 and increasing the pH in dense blooms, Cyanobacterial and unicellular Crocosphaera. Very few studies were pub- species succession is thought to be driven towards strains lished on flamentous heterocystous Nodularia, Calothrix with a more efcient carbon concentrating mechanisms and Anabaena (alias: Dichlospermum) species (reviewed by (Lines and Beardall 2018). Wannicke et al. 2018b). A more recent study suggested that Globally, an increase in phytoplankton blooms, includ- growth of the diazotrophic Dolichospermum circinale might ing Cyanobacterial harmful algal blooms, has been recorded beneft from increased CO 2 levels of 1700 ppm (Symes and since the 1980’s (Ho et al. 2019). While the reasons for the van Ogtrop 2019). observed increase is unclear, temperature, elevated atmos- Studies investigating the efect of climate change on fla- pheric CO2 levels and eutrophication especially of the mentous diazotrophic Cyanobacteria in terrestrial habitats freshwater lakes are potential drivers of this phenomenon. are rare too. Terrestrial surfaces are often inhabited by cryp- Approximately a third of all anthropogenic CO2 released togrammic covers, including Cyanobacteria that contribute 1 3 Atmospheric CO2 availability induces varying responses in net photosynthesis, toxin… Page 3 of 17 33 a signifcant amount to global net primary productivity Microcystis aeruginosa (Downing et al. 2005), particularly (Elbert et al. 2012). Specifcally, it is