Grazing of Nuclearia thermophila and Nuclearia delicatula (Nucleariidae, Opisthokonta) on the toxic cyanobacterium Planktothrix rubescens

Abstract

During the last decades, the planktonic cyanobacterium Planktothrix rubescens became a dominant primary producer in many deep pre-alpine lakes. While altered physiochemical conditions due to lake warming seem to favour this cyanobacterial species, its dominance is partly attributed to factors conferring grazing resistance. The rigid structure of the cyanobacterial filaments and toxic secondary metabolites (e.g. microcystins) protect against diverse grazers. Nonetheless, species of the protistan genus Nuclearia (Nucleariidae, Opisthokonta) are able to overcome this grazing protection. Time lapse video documentation served as tool to record slow feeding processes of N. thermophila and N. delicatula. Three different feeding strategies could be distinguished: (i) Phagocytosis of small fragments, (ii) serial break-ups of cyanobacterial cells and (iii) bending and breaking of filaments. While observations revealed mechanical manipulation to be important for the efficient breakdown of P. rubescens filaments, the toxin microcystin had no pronounced negative effects on nucleariid cells. Growth experiments with N. thermophila/N. delicatula and different accompanying bacterial assemblages pointed to a pivotal role of distinct prokaryotic species for toxin degradation and for the growth success of the protists. Thus, the synergistic effect of nucleariids and specific bacteria favours an efficient degradation of P. rubescens along with its toxin.

Combined cultivation and single-cell approaches to the phylogenomics of nucleariid amoebae, close relatives of fungi

“…Nuclearia species are capable of growing in eutrophic and/ or contaminated environments. For example, they can ingest toxic filamentous cyanobacteria that can thrive in perturbed environments as their sole food source [29,41]. This capability appears to be related to their association with symbiotic bacteria that degrade toxic metabolites, as microcystin, contained in the cyanobacteria ingested by Nuclearia [28,29,67].…”

“…For example, they can ingest toxic filamentous cyanobacteria that can thrive in perturbed environments as their sole food source [29,41]. This capability appears to be related to their association with symbiotic bacteria that degrade toxic metabolites, as microcystin, contained in the cyanobacteria ingested by Nuclearia [28,29,67]. Our N. pattersoni single cell was recovered by micromanipulation from the gut content of a dissected X. tropicalis tadpole grown in the laboratory.…”

“…The non-polarized and plastic cell shape surrounded by hyaline pseudopodia (branching filopodia) of nucleariids seems concomitant with the loss of flagella. Although there are few studies on nucleariid biology, cell movement by 'walking' on the benthos [29] and planktonic stages with equally radiating filopodia (electronic supplementary material, figures S1-S3) arise as major common features of nucleariids, together with a mucilaginous coat involved in different functions (from encystation to encapsulation of ectosymbionts or scales [1,14,29,67]. Although the current knowledge about this group is limited, we can already speculate about evolutionary patterns regarding cell size, food royalsocietypublishing.org/journal/rstb Phil.…”

“…Historically, owing to the lack of clear external features distinguishable under optical microscopy, nucleariids have been assigned to a variety of amoeboid taxa [26,27]. Nuclearia Cienkowski, 1865, is the most commonly observed and characterized genus [1,28,29]. Until the late twentieth century, this genus was associated with other naked filose amoebae in several different and conflicting taxonomies [8,30,31].…”

Reconstruction of trophic state shifts over the past 90 years in a eutrophicated lake in western Switzerland, inferred from the sedimentary record of photosynthetic pigments

“…This can be attributed to biological degradation in the water column. Studies have shown that zooplankton species have developed adaptive responses to co-exist with P. rubescens (Kurmayer and Jüttner 1999) and that certain eukaryotes including protists (e.g ciliates) are able to degrade the cyanobacterium and its toxin with the synergetic effect of specific bacteria (Dirren et al 2017). Thus, the absence of the cyanobacterium in the fossil record under low biomasses can be justified.…”