Abstract
We studied the impact of protist grazing and exudation on the growth and transcriptomic response of the prokaryotic prey species Polynucleobacter asymbioticus. Different single- and multi-species communities of chrysophytes were used to determine a species-specific response to the predators and the effect of chrysophyte diversity. We sequenced the mRNA of Pn. asymbioticus in communities with three single chrysophyte species (Chlorochromonas danica, Poterioochromonas malhamensis and Poteriospumella lacustris) and all combinations. The molecular responses of Pn. asymbioticus significantly changed in the presence of predators with different trophic modes and combinations of species. In the single-species samples we observed significant differences related to the relative importance of grazing and exudation in the protist-bacteria interaction, i.e., to the presence of either the heterotrophic Ps. lacustris or the mixotrophic C. danica. When grazing dominates the interaction, as in the presence of Ps. lacustris, genes acting in stress response are up-regulated. Further genes associated with transcription and translation are down-regulated indicating a reduced growth of Pn. asymbioticus. In contrast, when the potential use of algal exudates dominates the interaction, genes affiliated with iron transport are up-regulated. Rapid phototrophic growth of chrysophytes, with a high demand on soluble iron, could thus lead to iron-limitation and cause changes in the iron metabolism of Pn. asymbioticus. Additionally, we observe a benefit for Pn. asymbioticus from a more diverse protistan community, which could be due to shifts in the relative importance of phototrophy in the mixotrophic chrysophytes when competing for food with other species. Our study highlights the importance of biotic interactions and the specificity of such interactions, in particular the differential effect of grazing and algal exudation in the interaction of bacteria with mixotrophic protists.
Highlights
Many ecological processes and patterns in aquatic systems such as competition, community structure, and nutrient flow are influenced by predation and modulated by interactions between aquatic microorganisms
All of the chrysophytes feed on bacteria, whereby the grazing pressure is correlated with cell size and optimization of the predator-prey size ratio and is associated with the extent of reduction of the chloroplast (Graupner et al, 2018; Olefeld et al, 2018)
Grazing on ultramicrobacteria is strongest for the smallest species Ps. lacustris and lowest for the species C. danica with the species P. malhamensis in between - corresponding to the decreasing cell size and the decreasing contribution of phototrophy in the nutrition from C. danica over P. malhamensis to Ps. lacustris (Boenigk et al, 2004, 2006; Schmidtke et al, 2006; Foster and Chrzanowski, 2012; Johnke et al, 2017)
Summary
Many ecological processes and patterns in aquatic systems such as competition, community structure, and nutrient flow are influenced by predation and modulated by interactions between aquatic microorganisms. Heterotrophic and mixotrophic chrysomonads are abundant members of freshwater communities (Carrick and Fahnenstiel, 1989; Carrias et al, 1998; Auer and Arndt, 2001; Boenigk and Arndt, 2002; Weitere and Arndt, 2003) and by grazing on bacteria, function as a link between microbial secondary production and higher trophic levels Among their prey organisms are ultramicrobacteria from the genus Polynucleobacter. The genus Polynucleobacter is described as being chemo-organotrophic and aerobic, with some strains being capable of facultative anaerobic growth It is ubiquitous in a very broad range lake systems including alkaline, acidic, oligotrophic high mountain and eutrophic shallow lakes, rivers, ponds and raised bogs (Hahn et al, 2009; Jezberová et al, 2010; Jezbera et al, 2011 and within). The species Pn. asymbioticus is adapted to slightly acidic conditions and dwells in shallow ponds (Hahn et al, 2012, 2016b)
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