Is the coral‐algae symbiosis really ‘mutually beneficial’ for the partners?

Abstract

The consideration of 'mutual benefits' and partner cooperation have long been the accepted standpoint from which to draw inference about the onset, maintenance and breakdown of the coral-algae endosymbiosis. In this paper, I review recent research into the climate-induced breakdown of this important symbiosis (namely 'coral bleaching') that challenges the validity of this long-standing belief. Indeed, I introduce a more parsimonious explanation, in which the coral host exerts a 'controlled parasitism' over its algal symbionts that is akin to an enforced domestication arrangement. Far from being pathogenic, a range of well-established cellular processes are reviewed that support the role of the coral host as an active 'farmer' of the energy-rich photoassimilates from its captive symbionts. Importantly, this new paradigm reposes the deleterious bleaching response in terms of an envelope of environmental conditions in which the exploitative and captive measures of the coral host are severely restricted. The ramification of this new paradigm for developing management strategies that may assist the evolution of bleaching resistance in corals is discussed.

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).…”

“…In the case of coral and algae, however, there is an asymmetry in the share of symbiotic benefits between the two partners, because only corals control the flux of nutrients to the algae. 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).…”

Scleractinian coral cell proliferation is reduced in primary culture of suspended multicellular aggregates compared to polyps

“…Tissue dissociation is likely to disrupt the controls exerted by the coral host cell on its dinoflagellate symbiont proliferation, explaining the rapid and transient rise of CSDs. Restrictions of the intracellular availability of nitrogenous nutrients needed to undertake dinoflagellate cell cytokinesis is one of the processes which maintain dinoflagellates in a growth-limited state (Wooldridge 2010). In single dissociated cell cultures, the dissolved amino-acids contained in the complex cell culture medium are likely to be rapidly assimilated by the dinoflagellates (Grover et al 2008), fueling their cell growth and division.…”

Breakdown of the coral-algae symbiosis: towards formalising a linkage between warm-water bleaching thresholds and the growth rate of the intracellular zooxanthellae

“…The uncoupling of photosynthesis and growth in zooxanthellae is thus predicted to be an essential requirement for the continuous translocation of photosynthates to the coral host, i.e. a stable symbiosis (Dubinsky and Berman-Frank, 2001;Wooldridge, 2010). This condition is most readily achieved in oligotrophic waters that cause zooxanthellae growth rates to be nutrient-limited.…”

“…In this way, a weakening in the potential for autotrophy with respect to carbon can be understood to quickly compromise the stability of the symbiosis, especially during periods of high irradiance. Although a number of negative feedback cycles come into play, Wooldridge (2009aWooldridge ( , 2010 identified the retention of photosynthate for zooxanthellae (re)growth following an initial irradiance-driven expulsion event as the likely dominating feature of the energetic disruption to the host CCMs (summarised by Fig. 3).…”