Extracellular polysaccharide-protein complexes of a harmful alga mediate the allelopathic control it exerts within the phytoplankton community

Abstract

The goal of this study was to examine the significance of allelopathy by the raphidophyte Heterosigma akashiwo in a multispecies phytoplankton community in the field. Towards this aim, we sought allelochemicals of H. akashiwo, which had allelopathic effect both in laboratory experiments and in the field. As an initial step, we showed that the allelopathic effects of H. akashiwo filtrate were both species-specific and dependent upon the cell density of the target species. Secondly, we found for the first time that extracellular, high-molecular weight allelochemicals [that is, polysaccharideprotein complexes (APPCs)] were produced by a marine phytoplankton species, H. akashiwo. Thirdly, we indicated that the purified APPCs selectively inhibited the growth of the diatom Skeletonema costatum that is a major competitor of H. akashiwo, and thereby tended to promote the formation of monospecific H. akashiwo blooms. Furthermore, we demonstrated that the inhibitory effect of APPCs on the growth of the diatoms was determined by binding to the cell surface of the target species. Finally, we succeeded in the detection of APPCs in the field samples at concentrations exceeding their experimentally determined action threshold during the H. akashiwo bloom. Strategies for ecosystem control, including mitigation of harmful algal blooms (HABs), should take into account that red-tide organisms like H. akashiwo are already part of complex webs involving inter-specific allelopathic inhibition and ecosystem control during their dense blooms.

Dissolved organic matter (DOM) release by phytoplankton in the contemporary and future ocean

“…Karenia brevis produces multiple small (500 to 1000 Da) allelochemicals containing aromatic groups that inhibit the growth of the diatom Asterionellopsis glacialis (Prince et al, 2010). In contrast, the raphidophyte Heterosigma akashiwo releases a high molecular weight polysaccharide-protein complex (> 1 000 000 Da) that inhibits the growth of the diatom Skeletonema costatum by binding to the surface of the cells (Yamasaki et al, 2009). There is an extensive and rapidly growing literature on allelopathy associated with phytoplankton, which is beyond the scope of this review (see reviews by Gross, 2003;Legrand et al, 2003;Leão et al, 2009).…”

Allelopathy of the raphidophyte Heterosigma akashiwo against the dinoflagellate Akashiwo sanguinea is mediated via allelochemicals and cell contact

“…The fraction containing allelochemicals was prepared following Yamasaki et al (2009). H. akashiwo was inoculated at a density of 1 × 10 2 cells ml −1 into 100 ml glass flasks (n = 3) containing 50 ml of modified SWM-3 medium.…”

“…In spring and summer, allelopathy of centric diatom blooms is an important factor that inhibits the growth of A. sanguinea (Matsubara et al 2008). Recently, Yamasaki et al (2009) reported that allelopathic polysaccharide−protein complexes (APPCs) produced by Heterosigma akashiwo inhibited the growth of the diatom Skeletonema costatum, as the APPCs concentrations in the water exceeded the threshold of allelopathic potential. Thus, it is reasonable to propose that the allelopathic effect of H. akashiwo blooms during spring and early summer plays an important role in bloom formation of A. sanguinea.…”

Isolation of activity and partial characterization of large non-proteinaceous lytic allelochemicals produced by the marine dinoflagellate Alexandrium tamarense

“…Karlotoxins (KmTxs) with hemolytic activity from the dinflagellate Karlodinium veneficum inhibit the growth of several phytoplankton species (Adolf et al, 2006), and the dinoflagellate grazer Oxyrrhis marina (Adolf et al, 2007). The allelochemicals of the raphidophyte H. akashiwo that inhibit its diatom competitors Skeletonema costatum and Thalassiosira rotula were recently identified as high-molecular weight polysaccharide-protein complexes (Yamasaki et al, 2009).…”