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.
Highlights
Symbiotic associations between different species with conjoined evolutionary trajectories are among the most common ecological interactions in biological communities (Thompson, 2005; Douglas, 2010)
By emphasizing the reciprocal dynamics of host:symbiont interactions in terms of material goods that are exchanged between partners, an opportunity exists to consider one mechanism that might lead to specialization between partners
Adopting an explicitly comparative perspective that unites the findings from different symbioses may elucidate pathways common to intracellularlity sensu lato. The purpose of this perspective is to focus attention on significant trade-offs that exist for phototrophic symbionts residing in heterotrophic host cells
Summary
Symbiotic associations between different species with conjoined evolutionary trajectories are among the most common ecological interactions in biological communities (Thompson, 2005; Douglas, 2010). Common selective pressures may be experienced in symbioses involving phototrophic symbionts and heterotrophic hosts. If variability in the release rates of these and other compounds exists among phototrophs within a population of symbionts, natural selection could operate to favor variants with strategies that optimally match the characteristics of the host cellular machinery—a process that might lead to host specialization (Thornhill et al, 2014).
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