Production possibility frontiers in phototroph:heterotroph symbioses: trade-offs in allocating fixed carbon pools and the challenges these alternatives present for understanding the acquisition of intracellular habitats

Abstract

Intracellular habitats have been invaded by a remarkable diversity of organisms, and strategies employed to successfully reside in another species' cellular space are varied. Common selective pressures may be experienced in symbioses involving phototrophic symbionts and heterotrophic hosts. Here I refine and elaborate the Arrested Phagosome Hypothesis that proposes a mechanism that phototrophs use to gain access to their host's intracellular habitat. I employ the economic concept of production possibility frontiers (PPF) as a useful heuristic to clearly define the trade-offs that an intracellular phototroph is likely to face as it allocates photosynthetically-derived pools of energy. Fixed carbon can fuel basic metabolism/respiration, it can support mitotic division, or it can be translocated to the host. Excess photosynthate can be stored for future use. Thus, gross photosynthetic productivity can be divided among these four general categories, and natural selection will favor phenotypes that best match the demands presented to the symbiont by the host cellular habitat. The PPF highlights trade-offs that exist between investment in growth (i.e., mitosis) or residency (i.e., translocating material to the host). Insights gained from this perspective might help explain phenomena such as coral bleaching because deficits in photosynthetic production are likely to diminish a symbiont's ability to “afford” the costs of intracellular residency. I highlight deficits in our current understanding of host:symbiont interactions at the molecular, genetic, and cellular level, and I also discuss how semantic differences among scientists working with different symbiont systems may diminish the rate of increase in our understanding of phototrophic-based associations. I argue that adopting interdisciplinary (in this case, inter-symbiont-system) perspectives will lead to advances in our general understanding of the phototrophic symbiont's intracellular niche.

Population genetics of reef coral endosymbionts (Symbiodinium, Dinophyceae)

“…Silverstein et al 2012;Howells et al 2013). However and in contrast, incoming symbiont genotypes could be deleterious rather than beneficial to the host (Sachs & Wilcox 2006) and competition between symbiont genotypes can reduce the energy available for translocation to the host (Frank 1996;Douglas 1998;Hill 2014). Thus, higher within-host Symbiodinium diversity could paradoxically result in a fitness penalty to the host and its symbionts.…”

Combined Effects of Experimental Acidification and Eutrophication on Reef Sponge Bioerosion Rates

“…This implies that increased eutrophication did not impact the productivity of the symbionts. Sponges, like corals, can exercise control on symbiont growth and abundance by inhibiting division or ingesting them to maintain population size near a carrying capacity (Hill, 2014).…”

The stoichiometry of coral-dinoflagellate symbiosis: carbon and nitrogen cycles are balanced in the recycling and double translocation system

“…In aquatic ecosystems, diverse invertebrates (e.g., corals, sea anemones, tridacnid clams, foraminiferans, jellyfish, sponges, radiolarians, hydrozoans, and ascidians) are symbiotic with microalgae (e.g., the genera Symbiodinium, Chlorella, and Prochloron) and many of them are found in shallow tropical seawaters [1,2]. These symbiotic associations would be advantageous because the animal host can easily acquire energy in the form of autotrophically produced organic carbon (C) from the algal symbionts [3][4][5][6]. This characteristic feature of autotroph-heterotroph symbioses (i.e., the acquisition and allocation of photosynthetically fixed organic C) has been the main target of research for understanding the symbiotic metabolism, which led to the development of C-based theories and models [4,7,8].…”

“…These symbiotic associations would be advantageous because the animal host can easily acquire energy in the form of autotrophically produced organic carbon (C) from the algal symbionts [3][4][5][6]. This characteristic feature of autotroph-heterotroph symbioses (i.e., the acquisition and allocation of photosynthetically fixed organic C) has been the main target of research for understanding the symbiotic metabolism, which led to the development of C-based theories and models [4,7,8].…”