Enslavement in the water body by toxic Aphanizomenon ovalisporum, inducing alkaline phosphatase in phytoplanktons

Abstract

The hepatotoxin cylindrospermopsin (CYN) produced by certain cyanobacteria, including Aphanizomenon ovalisporum (hereafter Aphanizomenon) [1], seriously affects lake water quality [2], but its biological role is not known. Strong correlation between Aphanizomenon abundance in Lake Kinneret, Israel, and alkaline phosphatase (APase) activity suggests that inorganic phosphate (Pi) limitation induces the PHO regulon and APase secretion [3]. Staining lake samples with DAPI [4] revealed a high level of polyphosphate bodies (PPB) in Aphanizomenon. Application of enzyme-labeled fluorescence (ELF-APase) [5] showed APase in various organisms, but not in Aphanizomenon. ELF-APase signals and extracellular APase activity in Aphanizomenon were detected only after exploiting PPB under prolonged Pi deprivation in cultures or toward the end of its autumn bloom. Pi deprivation of Aphanizomenon induces CYN production, high-affinity Pi uptake, and an internal, not external, APase. Addition of Aphanizomenon spent media or CYN to various phytoplanktons, including Chlamydomonas reinhardtii, induced genes typically upregulated under Pi limitation and a rise in extracellular APase activity, despite ample surrounding Pi. Coculturing Aphanizomenon with Chlamydomonas or with Debarya sp. showed positive ELF-APase signals, but not in Aphanizomenon. CYN producers promote Pi supply by inducing APase secretion by other phytoplanktons, possibly explaining their increased abundance despite reduced Pi supply from watersheds.