Shining a Light on Exploitative Host Control in a Photosynthetic Endosymbiosis

Abstract

Endosymbiosis allows hosts to acquire new functional traits such that the combined host and endosymbiont can exploit vacant ecological niches and occupy novel environments [1, 2]; consequently, endosymbiosis affects the structure and function of ecosystems [3, 4]. However, for many endosymbioses, it is unknown whether their evolutionary basis is mutualism or exploitation [5-9]. We estimated the fitness consequences of symbiosis using the interaction between the protist host Paramecium bursaria and the algal symbiont Chlorella sp. [10]. Host fitness was strongly context dependent: whereas hosts benefited from symbiosis at high light intensity, carrying endosymbionts was costly to hosts in the dark and conferred no benefit over growing autonomously at intermediate light levels. Autonomous Chlorella densities increased monotonically with light intensity, whereas per-host symbiont load and symbiont abundance peaked at intermediate light levels and were lowest at high light intensity. This suggests that hosts controlled the costs of symbiosis by manipulating symbiont load according to light intensity. Photosynthetic efficiency was consistently lower for symbiotic compared to autonomous algae, suggesting nutritional constraints upon algae in symbiosis. At intermediate light levels, we observed the establishment of small populations of free-living algae alongside the hosts with endosymbionts, suggesting that symbionts could escape symbiosis, but only under conditions where hosts didn't benefit from symbiosis. Together, these data suggest that hosts exerted strong control over endosymbionts and that there were no conditions where this nutritional symbiosis was mutually beneficial. Our findings support theoretical predictions (e.g., [5, 9]) that controlled exploitation is an important evolutionary pathway toward stable endosymbiosis.

A Trait-Based Model for Describing the Adaptive Dynamics of Coral-Algae Symbiosis

“…Consistent with a coral-algae symbiotic relationship in which the host benefits but the symbiont gains little from the association (Douglas and Smith, 1989;Kiers and West, 2016;Lowe et al, 2016), we assume the symbiont biomass to be proportional to the host biomass so that the survival of the holobiont depends on the survival of the host. The coral controls the flux of nutrients to the algae and keeps most of the photosynthate products for itself thus preventing the algae to grow unboundedly (Muscatine, 1967;Wooldridge, 2010;Stambler, 2011).…”

“…The symbiotic benefit is by far larger for the coral host, while the benefit provided to the algae is barely enough to ensure survival (Wooldridge, 2010). This asymmetry is common in many host-endosymbiont relationships (Douglas and Smith, 1989;Frank, 1997;Kiers and West, 2016;Lowe et al, 2016). These aspects were addressed by Frean and Abraham (2004) with a model based on a modified prisoner's dilemma approach.…”

Deciphering the genomic toolkit underlying animal-bacteria interactions – insights through the demosponge Amphimedon queenslandica

“…High densities of dinoflagellate symbionts in hard corals predispose their hosts to stress associated with bleaching (Cunning and Baker 2012), indicating that an excessively high population of symbionts is not necessarily beneficial to the host. Indeed, host control over the population density of symbionts is a widespread strategy for regulating symbiosis that has been documented in unicellular eukaryotes as well as in both plants and animals (Prell, et al 2009;Cunning, et al 2015;Lowe, et al 2016). However, prior to the experiment, it was unknown if the native bacteria would be recognised, ignored, ingested or any combination of these three possibilities.…”

Intra-host Symbiont Diversity and Extended Symbiont Maintenance in Photosymbiotic Acantharea (Clade F)

“…When photosymbiotic protists are cultured in high-light and low-prey conditions, as found in oligotrophic surface waters, hosts benefit from an increased growth-rate, but symbiont growth-rate is suppressed and their photosynthetic efficiency is decreased compared to free-living symbionts (Lowe et al, 2016). These results indicate that algal symbionts may actually experience restricted nitrogen availability in hospite and therefore do not benefit from symbiosis (Lowe et al, 2016).…”

“…These results indicate that algal symbionts may actually experience restricted nitrogen availability in hospite and therefore do not benefit from symbiosis (Lowe et al, 2016). Estimated free-living populations of Phaeocystis in oligotrophic conditions (Moon-van der Staay et al, 2000) are much larger than possible symbiotic populations estimated from acantharian abundance and symbiont load (Michaels, 1991).…”