Microbial Symbioses 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. Malcolm S. Hill Journal Name: Frontiers in Microbiology ISSN: 1664-302X Article type: Hypothesis & Theory Article Received on: 14 Apr 2014 Accepted on: 25 Jun 2014 Provisional PDF published on: 25 Jun 2014 www.frontiersin.org: www.frontiersin.org Citation: Hill MS(2014) 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.. Front. Microbiol. 5:357. doi:10.3389/fmicb.2014.00357 Copyright statement: © 2014 Hill. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. This Provisional PDF corresponds to the article as it appeared upon acceptance, after rigorous peer-review. Fully formatted PDF and full text (HTML) versions will be made available soon. Running Title: Phototrophic investment strategies as a means to acquire intracellular host habitat 1 TITLE: 2 Production possibility frontiers in phototroph:heterotroph symbioses: trade-offs in 3 allocating fixed carbon pools and the challenges these alternatives present for 4 understanding the acquisition of intracellular habitats. 5 6 AUTHOR: 7 Malcolm S. Hill; Department of Biology; University of Richmond; Richmond, VA 8 9 10 ABSTRACT: 11 Intracellular habitats have been invaded by a remarkable diversity of organisms, and strategies 12 employed to successfully reside in another species’ cellular space are varied. Common selective 13 pressures may be experienced in symbioses involving phototrophic symbionts and heterotrophic 14 hosts. Here I refine and elaborate the Arrested Phagosome Hypothesis that proposes a mechanism 15 that phototrophs use to gain access to their host’s intracellular habitat. I employ the economic 16 concept of production possibility frontiers (PPF) as a useful heuristic to clearly define the trade-offs 17 that an intracellular phototroph is likely to face as it allocates photosynthetically-derived pools of 18 energy. Fixed carbon can fuel basic metabolism/respiration, it can support mitotic division, or it can 19 be translocated to the host. Excess photosynthate can be stored for future use. Thus, gross 20 photosynthetic productivity can be divided among these four general categories, and natural 21 selection will favor phenotypes that best match the demands presented to the symbiont by the host 22 cellular habitat. The PPF highlights trade-offs that exist between investment in growth (i.e., mitosis) 23 or residency (i.e., translocating material to the host). Insights gained from this perspective might help 24 explain phenomena such as coral bleaching because deficits in photosynthetic production are likely 1 Running Title: Phototrophic investment strategies as a means to acquire intracellular host habitat 25 to diminish a symbiont’s ability to “afford” the costs of intracellular residency. I highlight deficits in 26 our current understanding of host:symbiont interactions at the molecular, genetic, and cellular level, 27 and I also discuss how semantic differences among scientists working with different symbiont 28 systems may diminish the rate of increase in our understanding of phototrophic-based associations. 29 I argue that adopting interdisciplinary (in this case, inter-symbiont-system) perspectives will lead to 30 advances in our general understanding of the phototrophic symbiont’s intracellular niche. 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 2 Running Title: Phototrophic investment strategies as a means to acquire intracellular host habitat 49 Hypothesis and Theory 50 51 Background 52 Symbiotic associations between different species with conjoined evolutionary trajectories are among 53 the most common ecological interactions in biological communities (Thompson 2005; Douglas 54 2010). They also represent some of the most important evolutionary moments for life on this planet 55 given that the genesis of the Domain Eukarya involved successful invasion of host cells by bacterial 56 endosymbionts (e.g., mitochondria and chloroplasts - Knoll et al. 2006). Symbiotic interactions are 57 exceptionally diverse and include everything from pollinators/mycorrhizal symbionts and their plant 58 hosts, to parasites that castrate snails, to intracellular mutualists and parasites (e.g., Thompson 2005; 59 Douglas 2010; Vergara et al. 2013). The evolutionary responses of endocytobiological associations 60 are particularly interesting due to the high degree of intimacy between partners, which has the 61 potential to generate complicated evolutionary patterns as the host and symbiont respond to the 62 selective pressures each places on the other (e.g., Thompson 2005). 63 64 Organisms that occupy intracellular habitats must avoid the host’s cellular defenses (e.g., 65 immunological response, phagotrophy – Scott et al. 2003; Martirosyan et al. 2011; Sibley 2011). 66 Despite the challenges of living inside a cell, many symbionts have successfully invaded this habitat 67 as parasites and mutualists (e.g., Schwarz 2008; Nowack and Melkonian 2010; Heinekamp et al. 68 2013; Romano et al. 2013). The dynamic adaptive landscapes associated with endocytobiological 69 interactions can generate tight integration between the partners such that the evolutionary 70 manifestation is an obligate association for one or both species (e.g., Amann et al. 1997). From an 71 evolutionary perspective, however, the earliest stages of intracellular occupancy must, to some 72 degree, involve facultative associations. It is clear that we do not fully understand nuanced aspects of 3 Running Title: Phototrophic investment strategies as a means to acquire intracellular host habitat 73 evolutionary processes that shape many intracellular interactions, and thus the patterns (e.g., host 74 specialization; Thornhill et al. 2014) that emerge from them. 75 76 Symbioses between phototrophs and heterotrophs are common in many ecosystems (e.g., lichens, 77 Chlorella- and Symbiodinium-based symbioses). These ancient associations have been a focus of study 78 for decades in a variety of systems (e.g., Karakashian and Karakashian 1965; Kremer 1980; Weis 79 1980; Wilkerson 1980; Brodo et al. 2001; Yuan et al. 2005). The algal partners often contribute 80 substantial energy reserves to their hosts, and in many cases are located intracellularly. In some cases, 81 adaptations for symbiotic life styles have been detected (e.g., Blanc et al. 2010). The dynamics of 82 establishing the partnership from one generation to the next are complex, and depend upon 83 characteristics of the species involved in the association. In many cases, algae re-infect hosts each 84 generation from environmental sources. The route of entry into the host for intracellular 85 partnerships is often phagotrophic (Fig. 1), but the mechanisms that prevent activation of host 86 defenses as a response to the foreign agent (i.e., symbiont) are often unknown. A common narrative 87 can be found in much of the literature. Host cells lack particular vital nutrients, which they obtain 88 from an endosymbiont. Through its beneficence (e.g., preferentially shutting down immunological 89 or digestive processes in response to appropriate algal partners), the host creates a microhabitat, 90 often within specialized cells, that favors algal growth, but only up to a point. If the symbiont 91 population becomes too large, the host imposes some type of control to maintain symbiont 92 population size near a carrying capacity. Under this scenario, hosts must coordinate a complicated 93 choreography of genetic and cellular events in response to symbiont presence. In this context, algae 94 play a limited role in this association, and some have gone so far as to liken them to prisoners 95 involved in “enforced domestication” (Wooldridge 2010; Damore and Gore 2011). 96 4 Running Title: Phototrophic investment strategies as a means to acquire intracellular host habitat 97 Two hypotheses that afford symbionts a larger role in initiating and maintaining populations within 98 host cells were presented recently (Hill and Hill 2012). One of those hypotheses, the Arrested 99 Phagosome Hypothesis (APH), proposes that phototrophs enter a host cell through phagocytosis 100 (Fig. 1). However, the APH states that the symbiont can then subvert normal endomembrane 101 processes that lead to exocytosis by mimicking an organelle typically associated with digestion (e.g., 102 the phagosome) through the perpetual release of photosynthetically-derived compounds. Thus, 103 under the APH, symbionts have evolved a strategy involving the release of photosynthate so they 104 may remain within the host cell (i.e., occupy habitat) for extended periods of time. It is important to 105 note that the focus here will be on carbon-based photosynthate. This perspective builds on the work 106 of biologists like Muscatine et al. (1981) who examined carbon contributions that zooxanthellae 107 make to coral animal respiration.