Cyanobacterial surface blooms formed by Aphanizomenon sp. and Nodularia spumigena in the Baltic Sea: Small-scale fluxes, pH, and oxygen microenvironments

Summer blooms of filamentous cyanobacteria, mainly Aphanizomenon sp. and Nodularia spumigena, are characteristic for the Baltic Sea, where they accumulate at the sea surface in calm weather. The chemical microenvironment, and thus the actual growth conditions within these cyanobacterial surface blooms of the Baltic Sea, are largely unknown. Using microsensors, it is shown that photosynthesis is substantial within these millimeter-thin cyanobacterial layers accumulating at the air–water interface. Net oxygen fluxes at the air–sea interface were on average 2.7-fold higher than those at the aggregate–water interface beneath the layers. Net photosynthesis at light saturation was 1.7–2.4 mmol O2 m22 h21. Dark respiration varied between 0.21 6 0.12 mmol O2 m22 h21 and 0.50 6 0.30 mmol O2 m22 h21. There is a tight coupling of O2-producing and O2consuming processes within aggregates of these large, heterocystous, nitrogen-fixing cyanobacteria and their associated heterotrophic microbial community. It is suggested that the close association of autotrophic and heterotrophic organisms and processes creates a pH microenvironment that is favorable for iron uptake for the cyanobacteria, which in turn may release surplus nitrogen to the heterotrophic community. The pH varied between 7.4 and 9.0 between darkness and saturating light intensities. Decaying aggregates were anoxic up to 12 h. The volumetric oxygen consumption rate in an anoxic aggregate was 1.2 mmol O2 cm23 h21. During the initial 12 h of decay, aggregate sinking velocity increased 10-fold, concurrent with a decrease in volumetric oxygen consumption to 0.67 mmol O2 cm23 h21. The Baltic Sea is characterized by summer blooms of two large, heterocystous, N2-fixing cyanobacteria species, N. spumigena and Aphanizomenon sp., of which the former species is toxic (Bianchi et al. 2000). It has been proposed that gas vesicles within filaments make these cyanobacteria positively buoyant to reach high light intensities at the sea surface, where they cover the energy needed for N2 fixation through photosynthesis (Walsby et al. 1997). In calm weather, a significant fraction of these cyanobacteria accumulate at the sea surface and cover very large areas of the Baltic Sea where the N : P ratio is low (Kononen et al. 1996; Moisander et al. 2003; Stal et al. 2003). N. spumigena and Aphanizomenon sp. often compose 20–30% of the cyanobacterial biomass, the remaining being represented by picocyanobacteria. However, the contribution to primary production by large cyanobacteria was 44% (Stal et al. 1999; Stal and Walsby 2000). The large cyanobacteria are the main N2-fixing organisms in the Baltic Sea (Stal and Walsby 2000; Boström et al. 2007). The large cyanobacteria fix excess N2 relative to their own nitrogen demand and channel the surplus nitrogen through the microbial food web and to picocyanobacteria (Larsson et al. 2001). Cyanobaterial aggregates N. spumigena and Aphanizomenon sp. are colonized by a diverse community of bacteria that show high ectoenzymatic activities (Hoppe 1981; Stoecker et al. 2005; Tuomainen et al. 2006). The tight physical association of autotrophic and heterotrophic organisms implies tight couplings of biological processes. Up to 40% of the primary production measured by the use of HCO3 in N. spumigena aggregates from the Baltic Sea was incorporated in the associated bacteria (Hoppe 1981). Blooms of N. spumigena and Aphanizomenon sp. thus support a large and active food web dominated by microheterotrophs, which also appear to remineralize much of the cyanobacterial biomass within the water column (Forsskåhl et al. 1982; Sellner 1997). Isotopic signatures of sedimenting organic matter, however, have revealed that a large fraction of nitrogen fixed by pelagic cyanobacteria is exported to sediments in the Baltic Sea (Struck et al. 2004). Hence, large cyanobacteria play an important role for primary production and input of nitrogen to the pelagic surface waters and sediments. The accumulation of millimeter-thin layers of cyanobacterial biomass at the air–water interface in lakes leads to significant gradients of oxygen and pH within these aggregates (Ibelings and Maberly 1998). The physical and chemical microenvironment and growth conditions for the cyanobacteria and their associated heterotrophic community are, therefore, significantly different from that of the 1 Present address: Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, D-27570 Bremerhaven, Germany ([email protected]).