Effects of phosphorus loading on interactions of algae and bacteria: reinvestigation of the ‘phytoplankton-bacteria paradox’ in a continuous cultivation system

Abstract

The effect of different phosphorus loads (LP) on the phosphorus (P) and carbon (C) con- tent (biomass) of algae and bacteria was assessed in continuous culture. We tested if a mixed fresh- water microbial assemblage co-cultured with a phytoflagellate (Cryptomonas phaseolus) would com- ply with the 'phytoplankton-bacteria paradox' (sensu Bratbak & Thingstad 1985). This hypothesis states that the ratio of bacterial to algal abundance changes to the benefit of bacteria with decreasing LP. However, the phenomenon was originally investigated by simultaneously altering LP and micro- bial growth rates, and it is unclear to which extent it can be assigned to either parameter. Therefore, we set up 3 chemostat systems in triplicate at equal dilution rates, but with daily LP of 21, 41 or 62 µg l -1 d -1 (corresponding to 50, 100 and 150 µg P l -1 ). Higher LP led to a 5-fold increase in total algal abundance and biomass but to less than a doubling of these parameters in the bacterial assemblage. Total biomass ratios of bacteria to algae changed from 0.18 to 0.06 with increasing LP, while the bac- teria-algae total phosphorus ratios decreased from 0.80 to 0.17. The cellular C:P ratio of algae remained similar at all P concentrations, whereas the molar C:P ratios of bacterial cells significantly increased at higher LP (from 44 to 73). An enrichment experiment with the 50 µg P l -1 treatment demonstrated that bacteria at the lowest LP were co-limited by P and C, and that increased P stimu- lated mainly the algal fraction. The phytoplankton-bacteria paradox at the level of a mixed microbial assemblage is thus characterised by the following aspects: (1) bacteria profit from their high affinity to P and are better competitors at lower LP; (2) although algae compete with bacteria for P, P-limited algae release extracellular C that stimulates growth of their bacterial competitors; (3) when bacteria depend on algae as their sole source of organic C, this provides a feedback mechanism by which algae limit the abundance of their competitors at higher LP; (4) large oscillations in the bacteria-algae ratios at the lowest LP point to a greater instability of this interaction with stronger P competition. However, bacteria were not able to outcompete C. phaseolus, as algae were their only C source.