"Three to tango" makes yet another appearance in endosymbioses, this time in the form of a purple-green ciliate that is home to both purple bacteria and green algae. At first glance, this seems like a paradox. Purple bacteria are anaerobic and anoxygenic photosynthesizers, but green algae are aerobic and oxygenic photosynthesizers. To add to the bafflement, the respective purple and green photosynthetic pigments absorb at non-overlapping wavelengths. So how is it that this little ciliated paradox came to be?
Pseudoblepharisma tenue is a paramecium that was first described in 1926 by Alfred Kahl. It then sat in obscurity for nearly a century until Muños-Gómez et al. recovered the ciliate from its home in the Simmelried sphagnum ponds in Germany, where it coexists with purple bacteria within hypoxic sediments. Microscopy revealed that P. tenue is itself home to numerous purple bacterial cells and green algal cells, some of which could be imaged in the middle of division (Figure 1). The purple bacteria make up the majority of the intracellular dwellers; each host contains 900 to 1300 of them.
P. tenue is a curious hodgepodge of metabolism. The green algae have chloroplasts with pyrenoid-like structures, mitochondria, and cytosolic fermentative pathways. The purple bacteria have lost some metabolic pathways found in other purple sulfur bacteria (sulfur dissimilation and nitrogen fixation), but they can perform aerobic respiration, anoxygenic photosynthesis, and fermentation. The host itself has both mitochondria and pathways for fermentation, plus food vacuoles that suggest that it also phagocytoses food. So many modes of energy production! Whether aerobic or anaerobic, light or dark, autotrophic or heterotrophic, P. tenue seems to have something for everything.
Muños‑Gómez et al. suggest that despite all this apparent metabolic flexibility, P. tenue is quite picky. The ciliate is more of a Jekyll-and-Hyde mixotroph. The authors suggest that during the daytime, it is in anoxygenic mode, in which its mitochondria and green algae ferment and produce hydrogen and small organic molecules that the purple bacteria then use for photosynthesis. During the nighttime, all three partners turn to aerobic respiration, using the food that's been stockpiled during the day through photosynthesis and phagocytosis. All in all, here is an unusual microbial partnership that reconciles diverse modes of living.
A lingering question – how old and how stable is this tripartite endosymbiosis? Deep-sea Riftia tubeworms degrade and digest their endosymbionts as a major source of energy; could a similar turnover be happening in P. tenue, the host perhaps picking up replacement residents through phagocytosis?