Dissolved esterase activity as a tracer of phytoplankton lysis: Evidence of high phytoplankton lysis rates in the northwestern Mediterranean

Abstract

Phytoplankton cell lysis is perceived to be an important loss process in the sea, although a quantification of this process has proved elusive. A recently developed method, based on the measurement of dissolved esterase activity (EA), was used to estimate the release of esterases following phytoplankton cell lysis in an effort to evaluate the importance of this process as a loss factor in the summer phytoplankton of the northwestern Mediterranean Sea. Implicit in this method was the assumption that only the lysis of phytoplankton cells caused these enzymes to be released to the medium. This assumption was tested by analyzing the presence and release of esterases by marine bacteria, heterotrophic flagellates, and heterotrophic ciliates, all isolated from the Blanes Bay (northwestern Mediterranean, Spain), and by phytoplankton grown in culture (Synechococcus elongatus, Dunaliella sp., Chlorella sp., Phaeodactyllum tricornutum, and Chaetoceros decipiens). The dissolved EA found during the growth, stationary, and decay phases of microheterotrophs (bacteria, flagellate, and ciliate) was negligible when compared to that found for phytoplanktonic cultures. Differences in cell volume explained the differences in cell EA among the organisms, but heterotrophs showed lower cell EA (10‐50‐fold) than phytoplanktonic cells of similar cell size. These results support the assumption that microheterotrophs do not contribute significant amounts of EA to the dissolved pool, allowing the use of the method to estimate phytoplankton lysis. Independent estimates of cell loss in phytoplankton cultures, derived from cell cycle analysis, confirmed the estimates of cell lysis obtained from the measurement of dissolved EA.During the study conducted in the Mediterranean Sea, the water column was strongly stratified, showing a deep (40–55 m) chlorophyll a (Chl a) maximum (DCM; 1.25 ± 0.09 µg liter−1) and low surface Chl a concentrations (0.09 ± 0.008 µg liter−1). Phytoplankton lysis rates ranged between 0.026 d−1 and 1.9 d−1, and they declined significantly with depth; the fastest rates were found in surface waters and the slowest ones at the DCM. Despite the fast gross growth rates of surface phytoplankton (as calculated from phytoplankton biovolume and oxygen production), the calculated lysis rates represented a considerable proportion of gross phytoplankton growth rate (50%) at the surface, whereas they were comparatively less important at the DCM (7%). These results provide strong evidence that phytoplankton lysis can bc an important loss factor in the surface waters of this stratified, oligotrophic sea. Phytoplankton lysis could provide the loss factor needed to explain the low phytoplankton biomass despite fast growth and low grazing rates in the northwestern Mediterranean surface waters. The high lysis rate of phytoplankton in surface waters represents an important path by which primary production may fuel the growth of microheterophic organisms, consistent with the high respiration rate of the surface community examined. The conclusion that phytoplankton lysis rates can occur at rates high enough to influence food web dynamics and biogeochemical cycles in the oligotrophic ocean should stimulate research on this largely neglected loss factor in phytoplankton ecology.