The acquisition of phototrophy: adaptive strategies of hosting endosymbionts and organelles

Abstract

Many non-photosynthetic species of protists and metazoans are capable of hosting viable algal endosymbionts or their organelles through adaptations of phagocytic pathways. A form of mixotrophy, acquired phototrophy (AcPh) encompasses a sweet of endosymbiotic and organelle retention interactions, that range from facultative to obligate. AcPh is a common phenomenon in aquatic ecosystems, with endosymbiotic associations generally more prevalent in nutrient poor environments, and organelle retention typically associated with more productive ones. All AcPhs benefit from enhanced growth due to access to photosynthetic products, however the degree of metabolic integration and dependency in the host varies widely. AcPhs are mixotrophic, using both heterotrophic and phototrophic carbon sources. AcPh is found in at least four of the major eukaryotic supergroups, and is the driving force in the evolution of secondary and tertiary plastid acquisitions. Mutualistic resource partitioning characterizes most algal endosymbiotic interactions, while organelle retention is a form of predation, characterized by nutrient flow (i.e. growth) in one direction. AcPh involves adaptations to recognize specific prey or endosymbionts and to house organelles or endosymbionts within the endomembrane system but free from digestion. In many cases, hosts depend upon AcPh for the production of essential nutrients, many of which remain obscure. The practice of AcPh has led to multiple independent secondary and tertiary plastid acquisition events among several eukaryote lineages, giving rise to the diverse array of algae found in modern aquatic ecosystems.This review highlights those AcPhs that are model research organisms for both metazoans and protists.Much of the basic biology of AcPhs remains enigmatic, particularly 1) which essential nutrients or factors make certain forms of AcPh obligatory, 2) how hosts regulate and manipulate endosymbionts or sequestered organelles, and 3) what genomic imprint, if any, AcPh leaves on non-photosynthetic host species.2

What makes a chloroplast? Reconstructing the establishment of photosynthetic symbioses

“…1) (Johnson, 2011b;Stoecker et al, 2009). In some lineages, the entire cells of prokaryotic or eukaryotic photosynthetic symbionts are retained, which we refer to here as 'photosymbionts'.…”

The biological and geological contingencies for the rise of oxygen on Earth

“…Indeed, over the ensuing several hundred million years following the GOE, cyanobacteria were serially transferred to several clades of eukaryotic cells, one of which became the founder species for all terrestrial plants. The diversity of eukaryotic algae is enormous, and experimental endosymbiotic events occur continuously; this topic is discussed by both Green (2010) and Johnson (2010). The experimentation in endosymbiotic associations led to several types of antenna chlorophyll protein complexes serving highly conserved reaction center cores.…”

Oxygenic photosynthesis and the distribution of chloroplasts

“…Many of them provide clues that might be useful in alternate considerations of how plastids differentiated and spread. An elaboration of many such examples is illustrated in the chapter by Johnson (2010) dealing with adaptive strategies in hosting cells and their organelles. These adaptive strategies are mutualistic and are generally driven by the sharing of basic metabolic resources.…”

“…Present day chloroplasts, presumably all derived originally from one cyanobacterial endosymbiotic event, have become dispersed in single-celled eukaryotic ''hosts'' with the greatest dispersion among the chlorophyll c-containing algae (Green 2010). Numerous examples of symbiotic stages of photosynthetic organisms in multicellular animals (Johnson 2010) lead to the interesting possibility that many of these are present day examples of chloroplast evolution in action, i.e., possible progressions from the symbiotic toward the endosymbiotic state.…”