Endosymbiotic associations within protists

Abstract

The establishment of an endosymbiotic relationship typically seems to be driven through complementation of the host's limited metabolic capabilities by the biochemical versatility of the endosymbiont. The most significant examples of endosymbiosis are represented by the endosymbiotic acquisition of plastids and mitochondria, introducing photosynthesis and respiration to eukaryotes. However, there are numerous other endosymbioses that evolved more recently and repeatedly across the tree of life. Recent advances in genome sequencing technology have led to a better understanding of the physiological basis of many endosymbiotic associations. This review focuses on endosymbionts in protists (unicellular eukaryotes). Selected examples illustrate the incorporation of various new biochemical functions, such as photosynthesis, nitrogen fixation and recycling, and methanogenesis, into protist hosts by prokaryotic endosymbionts. Furthermore, photosynthetic eukaryotic endosymbionts display a great diversity of modes of integration into different protist hosts. In conclusion, endosymbiosis seems to represent a general evolutionary strategy of protists to acquire novel biochemical functions and is thus an important source of genetic innovation.

Figure 1.

Paulinella chromatophora cells. (a) Scanning electron microscopic image. (b) Light microscopic image (differential interference contrast). C, chromatophore; M, mouth opening; N, nucleus; P, plasma membrane and W, cell wall composed of silica scales. Light microscopic images of dinoflagellates with unusual plastids. (c) L. chlorophorum, (d) G. aeruginosum, and (e) K. foliaceum, arrowhead highlights the eyespot. Images kindly provided by Barbara Surek (c,e) and Karl-Heinz Linne von Berg (d). Scale bar, (a,b) 5 µm; (c–e) 10 µm.

Figure 2.

Metabolism of bacterial endosymbionts in protists as deduced from their genome sequences. Arrows in black represent pathways largely encoded and arrows in red represent pathways largely missing. (a) Chromatophore of Paulinella and (b) CfPt1-2 Bacteroides-type endosymbiont of the cellulolytic termite gut flagellate P. grassii (modified from Hongoh et al. 2008b). Question marks denote uncertainties in function or identity of a protein. Amino acids are in bold. COX, cytochrome-c oxidase; FNR, ferredoxin : NADP⁺ reductase; FRD, fumarate reductase; MQ, menaquinone; NDH, NADH dehydrogenase; PQ, plastoquinone and PRPP, 5-phosphoribosyl 1-pyrophosphate.

Figure 3.

Life history of protists with photosynthetic eukaryotic endosymbionts. (a) In P. bursaria aposymbiosis can be induced by DCMU (DCMU = 3-(3,4-Dichlorophenyl)-1,1-dimethylurea) treatment or growth in the dark. Upon availability of Chlorella cells, the symbiosis is reconstituted in the light. (b) Cell division of H. arenicola yields one symbiont-bearing green and one symbiont-lacking colourless cell, which reconstitutes the phototrophic lifestyle by ingestion of a Nephroselmis cell (modified from Okamoto & Inouye 2006). (c) In M. rubra, performance of the cryptophyte-derived kleptoplastids depends on transcriptional activity of the cryptophyte nuclei (symbolized by red arrows). Ageing nuclei are replaced by the uptake of new cryptophyte prey. (d) Dinophysis cell during myzocytotic uptake of kleptoplastids from Myrionecta rubra.